B I O L O G I C A L C O N S E RVAT I O N
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Arthropod responses to harvesting and wildfire: Implications
for emulation of natural disturbance in forest management
Christopher M. Buddlea,*, David W. Langorb, Greg R. Pohlb, John R. Spencec
a
Department of Natural Resource Sciences, McGill University – Macdonald Campus, 21,111 Lakeshore Rd., Ste Anne de
Bellevue, Que., Canada H9X 3V9
b
Natural Resources Canada, Canadian Forest Service, Northern Forestry Centre, 5320-122 Street, Edmonton, Alb., Canada T6H 3S5
c
Department of Renewable Resources, 751 General Services Building, University of Alberta, Edmonton, Alb., Canada T6G 2H1
A R T I C L E I N F O
A B S T R A C T
Article history:
Although natural disturbance has been widely adopted as a template for forest manage-
Received 6 January 2005
ment that protects biodiversity, this hypothesis has not been adequately tested. We com-
Received in revised form
pared litter-dwelling arthropod assemblages (Coleoptera: Carabidae and Staphylinidae;
21 September 2005
Araneae) in aspen-dominated stands originating as clear-cuts or wildfires across three
Accepted 4 October 2005
age classes (1–2, 14–15, and 28–29 years old) to test whether the post-harvest and post-fire
Available online 15 November 2005
assemblages converged following disturbances, and to compare faunal succession. These
findings were compared to data about epigaeic arthropods in old and mature pyrogenic
Keywords:
aspen stands (>70 years old) to determine whether diversity and community composition
Beetles
of arthropods from the younger age-classes approached what may have been typical pre-
Biodiversity
disturbance conditions. The resulting data-set of almost 27,000 arthropods and 230 species
Boreal forests
showed convergence in most taxa, and some general similarities between 28- and 29-year-
Coarse-filter management
old stands and old and mature stands. However, not all taxa responded similarly, and fau-
Natural disturbance hypothesis
nal succession following clear-cutting appeared to progress more rapidly than following
Spiders
wildfire. Rarefaction-estimated diversity was elevated in 1–2-year-old stands, compared
to unharvested stands, reflecting a mix of closed-canopy and open-habitat species. Nonmetric multi-dimensional scaling ordinations showed that samples from young wildfire
disturbed stands (1–2 years old) included more variable assemblages than all other study
sites, and contained species that may depend on unique post-fire habitat characteristics.
The fauna of old and mature stands exhibited low diversity, but contained species with limited dispersal abilities, and species tied to old-growth habitats such as dead wood. Harvesting systems that do not allow adequate recovery following a first harvesting pass, or do not
maintain microhabitat features associated with older fire-origin forests, may threaten persistence of some elements of boreal arthropod faunas.
Ó 2005 Elsevier Ltd. All rights reserved.
1.
Introduction
Emulation of natural disturbances as a strategy for forest
management (Perry, 1998; Simberloff, 1999; Franklin et al.,
2002; Harvey et al., 2002; Armstrong et al., 2003; Work et al.,
2003, 2004) flows from the observation that the flora and fauna of many forest types are adapted to conditions associated
with large-scale disturbances such as wind-throw, insect outbreaks and wildfire. Thus, forestry practices that mimic some
obvious macro-characteristics of these natural disturbances
* Corresponding author: Tel.: +1 514 398 8026; fax: +1 514 398 7990.
E-mail address: [email protected] (C.M. Buddle).
0006-3207/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2005.10.002
B I O L O G I C A L C O N S E RVAT I O N
(e.g., through variable retention, design of cutting patterns,
rotation schedule, maintenance of dead wood) might be a
useful for retaining biodiversity (Hunter, 1993; Haila et al.,
1994; DeLong and Tanner, 1996; Angelstam, 1998; Armstrong,
1999; Bergeron et al., 2002).
Management of forest biodiversity species-by-species is
impossible and so we seek to manage various system characteristics (e.g., ‘coarse filters’ like the mix of cover-types or the
amount of coarse woody debris) to emulate patterns left by
natural disturbances, and expect them to benefit biodiversity.
However, the main differences that we observe in forest types
may not adequately reflect relevant variation as perceived by
organisms operating on scales that differ from ours (Angelstam et al., 2004). Thus, the choice of coarse filters that best
helps us achieve chosen biodiversity objectives is best identified through a regimen of testing and refinement.
Although a growing body of literature permits comparison
of the effects of natural disturbance and various forestry practices (Bunnell, 1995; Beaudry et al., 1997; Hobson and Shieck,
1999; Buddle et al., 2000; Reich et al., 2001; Simard et al.,
2001; Saint-Germain et al., 2005), there are few long-term comparisons between harvested areas and those affected by natural disturbance, especially in terms of effects on non-timber
values such as biodiversity. In fact, the ‘natural disturbance
hypothesis’ remains largely uncorroborated with respect to
the main emulations being presently employed by the forest
industry throughout the boreal region (Larsson and Danell,
2001; Spence, 2001; Work et al., 2003). It is important that we
understand the impact of forest practices on biodiversity,
since there is mounting evidence that the number and identity
of species occurring in an ecosystem relates in a meaningful
way to ecosystem stability and resilience (Tilman, 1999;
Naeem, 2002).
Terrestrial arthropods are a useful taxon for testing aspects
of the natural disturbance hypothesis. Arthropods contribute
to numerous ecosystem functions (e.g., nutrient cycling, litter
decomposition and pollination), and their diversity is unmatched by other multi-cellular taxa (May, 1988; Wilson,
1992). However, with the exception of a few pest species, most
arthropods have not been managed intentionally, which
means they provide an independent measure of how management practices might inadvertently alter biodiversity, especially at the stand scale (Spence et al., 1999). Furthermore,
there is a large body of literature on how forest harvesting influences arthropods (Niemelä et al., 1993; Pajunen et al., 1995;
Martikainen et al., 1999; Spence et al., 1999; Buddle et al.,
2000; Setälä et al., 2000; Work et al., 2004). In particular, litterdwelling (epigaeic) arthropods, such as spiders (Arachnida:
Araneae) and beetles (Coleoptera: Carabidae and Staphylinidae) are useful ecological or biodiversity indicators (McGeoch,
1998; Dale and Beyeler, 2001), and these taxa have been adopted
as suitable bioindicators (Rainio and Niemelä, 2003) to help
evaluate conservation of biodiversity in landscapes subjected
to forest harvesting (Niemelä, 2000). Using more than one taxon has the advantage of testing the generality of any observed
patterns, and it is recommended to broaden the taxonomic
scope when using bioindicators (Rainio and Niemelä, 2003).
Rove beetles, ground beetles, and spiders are widely distributed but show distinct associations with specific habitat types.
They are also diverse, relatively well-known taxonomically,
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
347
and sensitive to habitat modification. Many of these epigaeic
taxa are also important predators of forest pest insects (Cameron and Reeves, 1990; DuDevoir and Reeves, 1990; Jennings
et al., 1990; Mason et al., 1997; Raymond et al., 2002), and are
tied to critical and disturbance-sensitive habitat features in
the boreal forests, including downed woody material (Hammond, 1997; Buddle, 2001; Grove, 2002).
Using a chronosequence approach, we have examined
how the diversity and structure of epigaeic arthropod assemblages occurring in boreal-mixedwood stands of north-central Alberta (Canada) differ following forest harvesting and
natural disturbance (wildfire). We also asked whether the fauna shows recovery towards a condition representative of a
pre-disturbance state after several decades. In the first stage
of this work, we compared the fauna among 1–2, 14–15, and
28–29-year-old stands originating from either wildfire or
clear-cutting. We expected arthropod biodiversity to differ
immediately following these disturbances since each alters
the biophysical properties of the forest in very different ways
(Nguyen-Xuan et al., 2000; Reich et al., 2001), and since research with ground beetles has supported this prediction
(Holliday, 1991; Saint-Germain et al., 2005). However, comparisons after three decades also test the hypothesis that the
faunas associated with the two disturbance types will converge on similar species assemblages, supporting one of the
tenets of the natural disturbance hypothesis. In the second
stage of this work, arthropods were sampled in mature and
old-growth mixedwood stands representative of the conditions that likely existed in forests long after (minimally 70
years) origin by wildfire. Comparing the fauna of younger
stands to that of these older stands allows us to assess the
degree of faunal recovery following disturbance.
2.
Methods
2.1.
Study design and study forests
We studied four age-classes of Populus forest stands originating following wildfire (herein referred to as pyrogenic stands);
1–2, 14–15, 28–29, and (>70 years in age), and three age-classes
of stands originating following clear-cutting (1–2, 14–15, and
28–29 years). Stands selected for study were deciduous-dominated at the time of harvest and were regenerated without
site preparation or planting. Given the relatively recent practice of harvesting Populus in Alberta (Pratt and Urquhart,
1994), clear-cuts older than 30 years were not available for
study. Within each age-class/disturbance type, we studied
two stands, to give a total of 14 study stands distributed over
the seven possible age/disturbance treatments (Table 1). Additional details of the 12 study sites <30 years in age can be
found in Buddle et al. (2000); old and mature stands (i.e., those
>70 years) were studied as part of a separate research program on regional diversity of beetles. These stands provide
a control for the strictly natural situation, rapidly disappearing across the boreal. They are pyrogenic, having never been
cut, and near the upper rotation-age being proposed for
industrial forestry in this region.
All study stands were in the mid-boreal ecoregion of
Alberta (Strong and Leggat, 1992; Buddle et al., 2000), which
is generally classified as mixedwood forest, representing a
348
B I O L O G I C A L C O N S E RVAT I O N
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
Table 1 – Stand location, mean trap days, relative abundance, and species richness of three litter-dwelling arthropod taxa
[spiders (Araneae), ground beetles (Carabidae), rove beetles (Staphylinidae), and all taxa together] collected over two years
(12 pitfall traps per stand type) in stands of differing age-class initiated by clear-cutting or wildfire
Clear-cut
1–2 years
Wildfire
14–15 years 28–29 years
1–2 years
14–15 years 28–29 years
Total
>70 years
Stand 1 location
55.3°N,
113.5°W
Mean (±SE) trap days 201.5 ± 4.94
55.6°N,
114.8°W
217.2 ± 14.9
55.4°N,
114.7°W
225.3 ± 6.15
56.3°N, 111.8°W 56.6°N,
115.9°W
180.8 ± 7.05
232.2 ± 7.33
55.2°N,
114.8°W
177.4 ± 8.10
55.2°N,
114.7°W
272.5 ± 12.18
Stand 2 location
55.0°N,
113.7°W
Mean (±SE) trap days 233.7 ± 3.60
55.4°N,
114.6°W
230.0 ± 7.04
55.2°N,
114.7°W
232.7 ± 3.67
56.2°N,
111.8°W
186.8 ± 14.3
56.3°N,
111.9°W
188.3 ± 7.92
55.2°N,
113.3°W
160.0 ± 14.00
55.3°N,
114.9°W
262.0 ± 9.53
Relative abundancea
Spiders
Ground beetles
Rove beetles
All taxa
Meanb
1755 (1352.1)
832 (641.0)
721 (555.5)
3308 (2548.5)
275.7 ± 26.79
1524 (1136.0)
722 (538.2)
1869 (1393.2)
4115 (3067.5)
342.9 ± 24.66
1269 (923.6)
2553 (1858.1)
2591 (1885.7)
6413 (4667.4)
534.4 ± 44.24
1007 (913.0)
1019 (923.8)
213 (193.1)
2239 (2029.9)
186.6 ± 21.33
865 (721.7)
320 (267.0)
1261 (1052.1)
2446 (2040.9)
203.8 ± 16.64
967 (1033.7)
755 (807.1)
1203 (1285.9)
2925 (3126.7)
243.8 ± 54.69
1833 (1143.1)
1463 (912.4)
2225 (1387.6)
5521 (3443.1)
460.1 ± 27.17
9220
7664
10,083
26,967
321.0 ± 18.1
Species richness
Spidersc
Ground beetles
Rove beetlesd
All taxa
58
25
48
131
58
17
48
123
57
23
43
123
49
22
35
106
58
14
39
111
48
14
42
104
47
16
40
103
110
45
75
230
a
b
c
d
Standardized total provided in parentheses (number collected per 2000 trap-days).
Means for all taxa, as number (±SE) per pitfall trap.
Immature spider specimens not included for measures of species richness.
Aleocharinae not included for measures of species richness.
range of postfire succession from young deciduous stands to
much older conifer-dominated stands (Rowe, 1972). Overall
forest composition of our stands was similar. Younger stands
(<30 years) were dominated (>90% of stems) by trembling aspen, Populus tremuloides Michx. and were all >30 ha in area.
Forests >70 years of age contained a more mixed species composition. The first of these stands (Table 1, Stand 1) was about
70 years old, 25 ha in area, and was composed of 70% trembling aspen, 13% birch Betula species, 9% balsam poplar (Populus balsamifera Linnaeus), and 8% Salix species. The second
(Table 1, Stand 2) was >130 years old, 20 ha in area, and contained about 42% Betula species, 32% balsam poplar, 24%
trembling aspen, and 2% Salix species.
Our chronosequence study has some design limitations.
For example, with harvest of aspen stands rare in Alberta until the past decade and the uncontrolled placement of wildfires, replication requires that stands be widely separated.
Thus, geographic variation may confound results and the degree of replication is more limited by fiscal constraints. Furthermore, old and mature stands are rare on our pyrogenic
landscape and tend to become more mixed in species composition over time than younger stands. These are natural
features of the biological template that work against a consistent signal in the data. Nonetheless, signals that we can interpret provide reasonable starting data about long-term
temporal dynamics of systems on which we can base our best
practices for management.
2.2.
Arthropod sampling
Epigaeic arthropods were collected over two snow-free seasons in 1996 and 1997 for all but the old and mature stands
– these we sampled using the same protocols during 1992
and 1993. Arthropods were sampled using standard pitfall
traps containing ethylene glycol (Spence and Niemelä, 1994;
Buddle et al., 2000). One transect of six pitfall traps (40–50 m
separating traps) was placed in each of the 14 study stands.
Samples were sorted and the three focal taxa (spiders, ground
beetles, and rove beetles) were identified to species. Larvae of
carabid and rove beetles were excluded from all analyses as
they could not be identified beyond family level. Immature
specimens of spiders and adult rove beetles in the subfamily
Aleocharinae were excluded from all analyses, except in the
context of relative abundance of groups within the spiders
and rove beetles, as accurate species identifications were
not possible with these groups. Voucher specimens have been
deposited in the Strickland Entomological Museum (University of Alberta) and the Northern Forestry Centre Arthropod
Collection, both in Edmonton, Alberta, Canada.
2.3.
Data analyses
For all statistics relating to relative abundance of arthropods
at the stand-type level, trap data were standardized to 2000
trap-days to compensate for differences in trapping effort
among stands.
Diversity estimates, especially raw species richness, are
sensitive to sample size (i.e., number of samples collected
or number of individuals collected) (Gotelli and Colwell,
2001; Magurran, 2004; Buddle et al., 2005). Therefore, rarefaction analyses were conducted to compare species richness
while adjusting for variation in sample size among the stand
types. The resulting estimates of the species richness can be
interpreted as a diversity index since both species richness
B I O L O G I C A L C O N S E RVAT I O N
and relative abundance data are used in the analysis. Additionally, statistical comparisons are possible since measures
of variance are generated around each species richness estimate for each sub-sample size. Rarefaction curves were generated using Internet-based software (Brzustowski, 2003) for
carabids, staphylinids, spiders, and for all groups together.
These were compared among stand ages and between disturbance types.
Changes in composition of the arthropod fauna by stand
type were compared using non-metric multi-dimensional
scaling (NMDS), as implemented by the PCOrd software
(McCune and Mefford, 1999). Standardized abundance data
were used for NMDS, but standardization was completed on
a per-trap basis (i.e., number of individuals collected per
212.5 trap-days; this number of trapping days was the experiment-wide average, see Table 1). Additionally, data were
log(x + 1) transformed prior to the ordination to reduce the
effects caused by the dominant species. A six-dimensional
ordination was first performed to evaluate how many axes
were optimal for a final solution (determined by reduction
in stress), and Monte-Carlo tests (n = 100) evaluated the significance of the final ordination. Final stress values were evaluated using 25 runs of real data.
Species-specific responses were analyzed using indicator
species analysis (Dufrêne and Legendre, 1997). This method
combines information on species abundance in a particular
stand type with its relative occurrence in other stand types,
and the resulting indicator value provides an indication of
the strength of a species affinity to a stand type. Indicator values were tested for statistical significance using Monte-Carlo
procedures (1000 permutations) using PCOrd (McCune and
Mefford, 1999).
3.
Results
A total of 26,976 specimens, representing 230 species, was
identified (Table 1). The majority of species, especially those
that were most frequently collected, are typical ‘boreal’ species (e.g., Lindroth, 1961–1969; Dondale and Redner, 1990),
widespread in their distribution, with ranges extended across
Canada, and certainly across the entire boreal plains region of
Alberta. Given this, the patterns uncovered in our analyses
likely reflect differences due to stand-age or origin rather
than the geographic separation of some of the study stands
(Table1).
Rove beetles were numerically most dominant, followed
closely by spiders. Patterns in relative abundance among
stand types varied by taxon, but overall the most individual
arthropods were collected in 28–29-year-old clear-cut stands
and the fewest were taken in the two youngest age classes
of pyrogenic stands. Rove beetles, in particular, were infrequently collected in 1–2-year-old pyrogenic stands (Table 1).
Excluding stands >70 years in age, standardized catches
were about 1.4 times higher in clear-cuts compared to pyrogenic stands (10283.4 and 7197.5 individuals, respectively)
(Table 1).
In terms of actual number of species collected, spiders
were the most species-rich taxon, followed, respectively, by
rove beetles and ground beetles (Table 1). Overall, harvestorigin stands had greater raw species richness than pyro-
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
349
genic stands of the same age, and this pattern was generally
apparent in each individual taxon (Table 1). Rarefaction estimates of species richness standardized to sample size varied
by taxon (Fig. 1). At a sub-sample size of about 800 individuals, spider diversity was lowest in pyrogenic stands >70
years of age, and clearly the highest in 14–15-year-old pyrogenic stands. In stands originating from clear-cuts, spider
species richness was much more similar among stands of
different ages, but lowest in the youngest stands. For both
groups of beetles, patterns of species richness were more
diffuse: species richness was highest in the 1–2-year-old
stands for both harvested and pyrogenic treatments,
although the small number of staphylinids caught in 1–2year-old burned stands leaves the question of whether this
pattern would be evident with additional sampling. However, for older stands, there was no general pattern in rarefied species richness for carabids or staphylinids.
Depiction of rarefaction curves for all three taxa combined
(sub-sample of almost 2000 individuals) showed that epigaeic
arthropod species richness was highest in 1–2-year-old clearcut and 14–15-year-old wildfire stands. The lowest values of
rarefied species richness were found in pyrogenic stands
>70 years in age, and in clear-cut stands 28–29 years old
(Fig. 2). The high species richness in 1–2-year-old clear-cut
stands was largely a reflection of the beetle data, and the high
species richness in 14–15-year-old pyrogenic stands reflected
mainly the spider data. In general, stands >70 years were
characterized by low species richness for all arthropods combined and for individual taxa.
Two-dimensional ordination solutions were deemed optimal for all taxa and for ground beetle ordinations; final stress
values were 42.07 (axis 1, all taxa), 20.3 (axis 2, all taxa), 40.8
(axis 1, ground beetles), and 19.4 (axis 2, ground beetles).
Three-dimensional solutions were deemed optimal for the
spider and rove beetle data. Final stress values for spider data
were 47.7 (axis 1), 23.9 (axis 2), and 19.1 (axis 3); stress values
for rove beetle data were 44.7 (axis 1), 24.3 (axis 2), and 19.4
(axis 3). Given the small reduction in stress for the third axis
for these solutions, two-dimensional ordinations are presented; interpretation did not change with the addition of a
third axis (not shown). Total variance explained by the final
solutions (Fig. 3) was 85.3% (all taxa), 84.8% (spiders, two
axes), 85.5% (ground beetles), and 79.2% (rove beetles, two
axes); all axes for all ordinations differed significantly from
what could be expected by chance (Monte-Carlo simulation,
n = 100, P < 0.01).
For all ordinations, the highest variation among traps was
found for the 1–2 and 14–15-year-old pyrogenic stands and
the amount of variation tended to decrease among samples
as stands aged (Fig. 3(a)–(d)). Immediately following disturbance (1–2-year-old stands) the arthropod faunas (all taxa
combined) of harvest-origin stands differed from those collected from pyrogenic stands along axis 1 (Fig. 3(a)). By 14–
15 years post-disturbance, the fauna from harvested stands
was very close in species composition to those collected in
28–29-year-old stands (Fig. 3(a)), but the composition of
arthropods from 14- to 15-year-old wildfire stands remain distinct along the first axis.
Faunal recovery of all taxa appeared most rapid following
clear-cutting as samples from 14- to 15-year-old clear-cut
350
B I O L O G I C A L C O N S E RVAT I O N
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
Wildfire
Clear-cut
60
Species richness
50
40
30
20
10
Spiders
0
0
400
800
1200
1600
0
400
800
1200
1600
25
Species richness
20
Stand age
15
1-2 years
14-15 years
10
28-29 years
>70 years
5
Ground beetles
0
50
0
400
800
1200
2400
0
400
800
1200
2400
2600
Species richness
40
30
20
10
Rove beetles
0
0
400
800
1200
1600
2000
0
Sub-sample size
400
800
1200
1600
2000
Sub-sample size
Fig. 1 – Rarefaction estimates of the expected species richness (±1SD) by subsample size (number of individuals) of spiders
(Araneae, top), ground beetles (Carabidae, middle), and rove beetles (Staphylinidae, bottom), collected by pitfall traps placed
in pyrogenic and clear-cut aspen-mixedwood stands of differing age.
stands were close in species composition to those from
28- to 29-year-old burned stands (Fig. 3(a)). The ordination
of spider data yielded a similar pattern to that for all arthropods (Fig. 3(b)), suggesting convergence in the spider fauna
following clear-cutting and wildfire, as samples from 28- to
29-year-old stands from the two disturbance types occupy
similar ordination space relative to younger age-classes.
There was good overlap with the catches of spiders from pitfall traps placed in the oldest stands compared to those from
the 28-to 29-year-old stands of both disturbance types
(Fig. 3(b)). Ground beetle assemblages also diverged between
younger wildfire stands (i.e., 1–2-year-old stands) and other
stand types, and there was some evidence of convergence
after the two disturbance types by 28–29 years post-disturbance (Fig. 3(c)). However, there was more variation in 28–
29-year-old pyrogenic stands with ground beetle samples
compared to spiders. Collections of carabid beetles in stands
>70 years of age were relatively indistinguishable from those
in 28- to 29-year-old wildfire and clear-cut stands. Variation
among rove beetle assemblages was also high in both 1–2year-old clear-cut and pyrogenic stands (Fig. 3(d)), and
although rove beetle assemblages from 28- to 29-year-old
wildfire and clear-cut stands occupied similar ordination
space, the fauna from stands >70 years in age was distinct
from 28- to 29-year-old stands along axis 1, and the composition of old and mature stands was close to what was collected
from 1- to 2-year-old clear-cut stands (Fig. 3(d)).
Seventy-eight species were significant indicators (Indicator
Species Analysis, P < 0.05) of stand type (seven stand types,
four age-classes of pyrogenic stands and three age-classes of
harvested stands). Focusing on species with indicator values
>40, nine species were strongly associated with 1–2-year-old
pyrogenic stands, and 13 species were associated with the
oldest pyrogenic stands (Table 2). In contrast, only five species
B I O L O G I C A L C O N S E RVAT I O N
Wildfire
140
Clear-cut
1-2 yrs
14-15 yrs
120
Species richness
351
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
14-15 yrs
1-2 yrs
28-29 yrs
100
28-29 yrs
> 70 yrs
80
60
40
20
0
0
1000
2000
3000
4000
5000
6000 0
1000
Sub-sample size
2000
3000
4000
5000
6000
Sub-sample size
Species richness
120
110
100
90
80
1-2
14-15
28-29
Stand age (years)
>70
1-2
14-15
28-29
Stand age (years)
>70
Fig. 2 – Rarefaction estimates of the expected species richness (±1SD) by subsample size (number of individuals) of three
litter-dwelling arthropod taxa (Araneae, Carabidae, and Staphylinidae) collected by pitfall traps placed in pyrogenic and
clear-cut aspen-mixedwood stands of differing age. Bottom figures represent estimates at maximum sub-sample size
common to all stand types (arrows in top figures, 1950 individuals).
were strongly associated with clear-cut stands (all ages
combined) (Table 2). Many of the species associated with 1–
2-year-old pyrogenic stands are typically known from coniferous and/or moist habitats (Table 2), even though the study
stands were primarily deciduous. Also noted was the presence
of the pyrophilic species Sericoda quadripunctata exclusively in
young pyrogenic stands. While spiders and ground beetles
showed strong affinities to young stand age-classes, six species of rove beetles exhibited strong affinities to old and mature stands (Table 2). Many of these rove beetles are known
mostly from moist, leaf-litter habitats, although Gabrius brevipennis is associated with dead wood.
4.
Discussion
Litter-dwelling arthropod assemblages from young clear-cut
stands converged towards a composition similar to the
fauna of stands generated by wildfire about 28–29 years postdisturbance. However, both the starting point and the resulting
successional trajectory depended on the disturbance type. We
noted high variation in stands of younger age-classes (i.e., 1–2
years post-disturbance, Fig. 3), a finding similar to that reported in Finland (Niemelä et al., 1996). Species diversity and
many species-specific responses also differed substantially
between harvested and burned stands, especially in the younger age-classes of forests. Some elements of the fauna occurring early in the succession of wildfire-origin stands are
missing altogether from stands originating as clear-cuts. For
example, species associated with open mineral soil and
charred organic matter were not common in stands regenerating after harvest. The importance of young pyrogenic stands
was also evident from Indicator Species Analysis, which depicted a high number of species with elevated indicator values
in these stands. This includes species such as the carabids
Harpalus egregious, Harpalus laticeps, and S. quadripunctata
(Table 2), all species which have previously been documented
as having strong affinities to young stands originating from
wildfire (Holliday, 1991; Wikars, 1995).
352
B I O L O G I C A L C O N S E RVAT I O N
2.0
2.0
a
All taxa
Spiders
1.5
1.5
1.0
1.0
Axis 2 (27.0%)
Axis 2 (29.9%)
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
0.5
0.0
-0.5
-1.0
b
0.5
0.0
-0.5
-1.0
-1.5
-1.5
-1.0
-0.5
0.0
0.5
1.0
-1.5
-1.5
1.5
-1.0
-0.5
Axis 1(55.4%)
2.0
1.5
0.5
1.0
1.5
2.0
1.5
c
Ground beetles
1.0
1.0
0.5
0.0
-0.5
-1.0
0.0
-0.5
-1.0
-1.5
-1.5
-2.0
-2.5
d
Rove beetles
0.5
Axis 2 (37.2%)
Axis 2 (27.2%)
0.0
Axis 1(57.8%)
-2.0
-2.0
-1.5
-1.0
-0.5
0.0
0.5
1.0
1.5
-2.5
-2.0
-1.5
-1.0
Axis 1(58.3%)
-0.5
0.0
0.5
1.0
1.5
2.0
Axis 1(42.0%)
.
Wildfire
Clear-cut
1-2 years
14-15 years
28-29 years
>70 years
1-2 years
14-15 years
28-29 years
Fig. 3 – Non-metric multi-dimensional scaling ordination plots of: (a) all taxa (230 species), (b) spiders (Araneae, 110 species),
(c) ground beetles (Carabidae, 45 species), and (d) rove beetles (Staphylinidae, 75 species) collected by pitfall traps placed in
pyrogenic and clear-cut aspen-mixedwood stands of differing age. Symbols represent the mean (x, y) coordinates (±95% CI) by
stand type, based on 6 pitfall traps per stand (note: 28–29-year-old wildfire stand contains only 5 pitfall traps due to high trap
disturbance for one trap). Percent variation explained by each axis given in brackets. Ordination differs from randomly
derived matrices at P < 0.05 (Monte-Carlo test, 100 permutations).
Epigaeic arthropod assemblages show partial recovery to
‘pre-disturbance’ conditions after 30 years, as the fauna (all
taxa combined) from old and mature mixedwood forests
was similar in species composition (and contained less species-rich assemblages) than the fauna from younger forest
age-classes. Although we know little about the natural habitat
affinities for most species we collected, several species-specific patterns point to specific habitat features (e.g., moisture
and dead wood) (Table 2) that may be missing from or reduced
in younger-age classes. Patterns evident from pooled data of
all three arthropod groups were not completely evident when
spiders, ground beetles, and rove beetles were analyzed separately. Taxon-specific patterns were less clear, and much
more variable, as depicted by rarefied estimates of species
richness (Figs. 1 and 2) and overall community composition
(Fig. 3). In particular, the degree of recovery to pre-disturbance
conditions was less strong for rove beetles than for spiders or
ground beetles (Fig. 3(b)–(d)).
For almost three decades post-disturbance, fewer arthropods were caught in pyrogenic stands than in those developing after harvest, a finding supported with other research on
soil invertebrates and ground beetles (Holliday, 1992; Wikars
and Schimmel, 2001; Saint-Germain et al., 2005). This is
probably due, in part, to the complete or partial reduction
of the organic horizon that occurs following most wildfires
(Simard et al., 2001). Re-establishment of this horizon may
require many years and it is one of the primary habitats
for epigaeic boreal arthropods (Huhta, 1971; Spence and Niemelä, 1994; Buddle et al., 2000). Our findings are generally
supported by other work with ground beetles during postfire regeneration in the boreal forests of Manitoba, Canada;
here, it is reported that ground beetle establishment following wildfires may be delayed in comparison to unburned
controls (Holliday, 1992). Holliday (1992) suggested that the
relatively simple habitat in post-fire sites may delay the
establishment of species common to control sites. Niemelä
(1999) also suggested that the impact of wildfire on boreal
forest biota is harsher which may cause a successional ‘delay’ compared to succession post-harvest. Our work strongly
supports this interpretation, as succession of beetles and
spiders in clear-cut stands progresses more rapidly than
after wildfire. Stated differently, the divergence from the
pre-disturbance condition is simply less following clear-cutting than following wildfire.
We noted the strongest reduction in catch rates for rove
beetles immediately following wildfire. Some rove beetles
B I O L O G I C A L C O N S E RVAT I O N
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
353
Table 2 – Spider (Araneae), ground beetle (Carabidae), and rove beetle (Staphylinidae,) species exhibiting significant
indicator values (IndVal) >40, by stand type (origin – Wildfire, WF, or Clear-cut, CC; age – years)
Stand type
Taxa
Species
Sericoda quadripunctata
Pardosa uintana
P. hyperborea
Pirata bryantae
Harpalus egregius
Arctosa alpigena
H. laticeps
P. xerampelina
Loricera pilicornis
IndVal
P
Known habitat affinities and/or natural history
100
89.4
70
56.6
52.8
51.4
45.5
44.4
41
0.001
0.001
0.001
0.001
0.002
0.001
0.002
0.001
0.006
Pyrophilousa,b
Spruce/fir forests, sphagnum bogs, tundrac
Coniferous forests, sphagnum bogs, tundrac
Hygrophilous, sphagnum bogs, black-spruce forestsc
Dry ground, burned forestsb,d,e
Sphagnum bogs, tundra, coniferous forests, alpine meadowsc
Sandy, upland forests, burned forestsb,d,e
Exposed habitats, sometimes hygrophilousc
Hygrophilous, rich and shaded soilsd,e
WF, 1–2
Ground
Spider
Spider
Spider
Ground
Spider
Ground
Spider
Ground
CC, 1–2
Spider
P. fuscula
Spider
P. moesta
Ground Agonum sordens
65
55.8
41.7
0.001
0.001
0.002
Hygrophilousc
Eurytopic; exposed habitats (grassland, meadows), forest edges, interiorsc
Hygrophilousd,e
WF, 14–15
Spider
Alopecosa aculeata
62.1
0.001
Forest glades, meadows, shrublandc
CC, 14–15
Rove
Acrolocha diffusa
54.2
0.001
Forest litter, fungi, carrionf
WF, 28–29
Rove
Nitidotachinus tachyporoides
Ground Playtnus mannerheimi
Spider
Zornella cultrigera
52
50
47.8
0.001
0.001
0.001
Riparian zone litter, sphagnum, mossg
Hygrophilous, sphagnum, can be arboreald,e
n/a
CC, 28–29
Ground Pterostichus riparius
77.8
0.001
Forests, sometimes hygrophilousd,e
WF, >70
Spider
Rove
Rove
Rove
Rove
Ground
Rove
Spider
Rove
Ground
Ground
Spider
Ground
66.7
61.9
59.2
58.8
51.6
50
47.8
46.1
44.5
43.7
42.6
40.9
40.2
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.005
Deciduous and coniferous forest litterh
Forest litter, rotten wood, bark, lichen, mossi
Forest litter, dungj
Hygrophilous, various litter types, flightlessk
n/a
Euryotopic, leaf litter, sometimes dry areasd,e
Forest leaf litterl
Low-growing vegetationm
n/a
Dry ground, forest leaf litterbd,e
Forest leaf litterd,e
Forest leaf litter, moss, bogsn
Mature forest specialistd,e
Xysticus obscurus
Gabrius brevipennis
Quedius caseyi caseyi
Acidota quadrata
Lathrobium washingtoni
Trechus apicalis
Ischnosoma splendidum
Helophora insignis
Lathrobium fauveli
Synuchus impunctatus
Agonum retractum
Allomengea dentisetis
Trechus chalybeus
Species arranged in order of decreasing indicator values. P-values based on Monte-Carlo test with 1000 permutations.
a Wikars (1995).
b Holliday (1991).
c Dondale and Redner (1990).
d Larochelle (1990).
e Lindroth (1961–1969).
f Hatch (1957).
g Campbell (1973).
h Dondale and Redner (1978).
i Smetana (1995).
j Smetana (1971).
k Campbell (1982).
l Campbell (1991).
m Kaston (1948).
n Van Helsdingen (1974).
are fungivorous or otherwise dependent on fungi (Klimaszewski, 2000), and thus populations residing within
and near surface mushrooms, would be highly vulnerable
to wildfire. Additionally, fungus-dependent species may be
hampered by a shortage of available fungi immediately after
wildfire, whereas generalist predators, such as most ground
beetles and spiders and some rove beetles, may not have the
same constraint. We also noted that some hygrophilous, and
conifer-associated epigaeic species, such as Arctosa alpigena,
Pardosa uintana, P. hyperborea, Pirata bryantae, and Loricera pilicornis, were associated with the youngest wildfire stands.
These species may be re-colonizing the wildfire landscape
from wet, conifer regions that were missed by fire (‘fireskips’) (Buddle et al., 2000). Fire-skips are important habitat
refuges for ground and rove beetles in subalpine forests of
western Alberta (Gandhi et al., 2001). It is unlikely they
represent residual populations surviving wildfire since the
organic horizon was largely burned during the wildfire
events (pers. obs.), and other research with ground beetles
in post-fire boreal forests of Canada suggest most populations go locally extinct after an intense forest fire (Holliday,
1991).
354
B I O L O G I C A L C O N S E RVAT I O N
Compared to recent burns, epigaeic arthropods were more
common in our traps immediately after harvesting, and rarefaction estimates of beetle diversity were high 1–2 years after
clear-cutting. Buddle et al. (2000) argued that spiders re-colonize quickly following clear-cutting, as source populations
(i.e., adjacent forested areas) are relatively close to the open
cut-blocks (clear-cuts were generally 30–60 ha in area whereas
wildfires were substantially larger and our sites were more
isolated from unburned habitats). The recent harvesting occurred in winter, when most arthropods were safely in the
frozen litter layer, hence many likely survived. In lodgepole
pine stands in western Alberta, for example, many ground
beetles survive harvest treatments, and are collected in pitfall
traps for 1–2 years after cutting (Niemelä et al., 1993). However, such populations are apparently unable to breed at
replacement rates and do not survive over the long term in
these stands (Spence et al., 1996). The mixing of ‘old-growth’
species and open-habitat specialists, can also explain elevated beetle diversity following clear-cutting (Niemelä et al.,
1993; Koivula and Niemelä, 2003), and probably explains in
part why the ordination analyses revealed a relatively similar
rove beetle species composition between old and mature
stands and 1–2-year-old clear-cuts (Fig. 3(d)).
Although the ordination analyses generally revealed partial to complete recovery of the arthropod to conditions that
may have been typical prior to disturbance, there remain
some unique elements to our old and mature forest fauna.
In particular, this fauna differed from that of all younger
stands in its low overall diversity, and in some of the species-specific patterns uncovered. Lower diversity in older
forests may reflect action of forces envisioned by the intermediate disturbance hypothesis (Connell, 1978; Petraitis et al.,
1989). Low disturbance conditions would provide stable
conditions favoring fewer species that have a competitive
advantage over other species [e.g., a ‘dominance controlled
community’, sensu (Yodzis, 1986)]. Lower diversity, however,
does not reflect a less specialized or less unique fauna in older
forests (Simberloff, 1999). In fact, the indicator species analysis illustrated that many species from each taxon had strong
affinities to older forest stands (Table 2). Thus, composition of
the fauna in these habitats is extremely important, and the
knowledge gained from species identity and associated natural history offers deeper insights than species richness alone
(Simberloff, 1999; Work et al., 2004).
The rove beetles exhibited the strongest affinities to old
and mature forest stands. Owing to their strong association
with fungi, many staphylinid species have more specific habitat requirements than spiders or ground beetles (Klimaszewski, 2000; Newton et al., 2001). Certain rove beetles with
limited dispersal ability (e.g., the flightless species Acidota
quadrata) and species associated with particular habitats such
as dead and decaying wood (e.g., G. brevipennis) are closely
tied to old and mature stands. Such taxa are likely to be at increased risk of local extinction under scenarios of increased
harvesting pressure (Niemelä et al., 1993; Spence et al., 1996).
Lack of congruence in response (especially degree of faunal convergence) among the three taxa sampled in this study
emphasizes potential risks of using single taxa to study of impacts of disturbances on forest biodiversity (Jonsson and Jonsell, 1999). The pooled arthropod data-set showed strong
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
convergence and recovery following wildfire and clear-cutting, and this pattern was largely driven by the spiders and
ground beetles, which separately indicated the same pattern.
Data about rove beetles suggest a less definitive recovery to
pre-disturbance conditions and a similarity between young
clear-cuts and old and mature forests. This similarity may
be due to residual old-growth populations of rove beetle species left on the landscape following harvesting. This may explain the slower recovery in a post-wildfire landscape
compared to post-harvest (Niemelä, 1999).
Our knowledge is now sufficient to dispel the notion that
we can manage ‘biodiversity’ with simple plans based on
how some aspects of natural disturbance affect a single taxon, whether it be spiders, beetles, fungi or songbirds. Single
taxon studies undoubtedly miss aspects that are critical from
the perspective of unstudied biotic elements. Likewise, concentration of effort on the ‘landscape’ scale (see Angelstam
et al., 2004) may blind us to biologically significant variation
on more local scales. Various ‘coarse filter’ approaches to biodiversity conservation minimize the importance of withinstand, fine-scale variation and, thus, offer cold comfort to
those who understand the importance of microhabitat variation for arthropods. This will be especially so when management is developed and monitored mainly with data about
vertebrates (Haeussler and Kneeshaw, 2003). For example,
use of a coarse filter biodiversity management approach, like
forest cover type, could do an excellent job at maintaining
organisms that treat the landscape as a coarse-grained mosaic, but still fail miserably with respect to creatures that respond to more fine-grained aspects of habitat variation
(MacNally et al., 2003). Nonetheless, there is some evidence
that coarse filter approaches to biodiversity conservation
may have some benefit for invertebrates (e.g., Blake et al.,
2003; Oliver et al., 2004). Clearly, programs that rigorously test
various proposals for management of biodiversity, in the
inevitable context of ongoing industrial forestry, are badly
needed.
This work underscores several considerations for management of boreal mixedwood forests. In particular, we offer evidence that wildfire is crucial to some unique elements of the
litter-dwelling arthropod fauna in young aspen forests. In
stands within with first 14–15 years of age, clear-cutting precludes habitat development and microhabitat variation typical
of post-fire situations and thus a number of arthropod species
that characterize early post-fire succession are missing. The
post-clear-cut fauna, with relatively high diversity, represents
a mix between open-habitat and closed-canopy species, the
latter of which may be a ‘shadow’ of the pre-harvest fauna.
By 28–29 years post-disturbance, however, elements of the fauna converge between wildfire and clear-cutting, which means
epigaeic arthropods of older stands may be relatively resilient
despite differences in the younger age-classes. The long-term
implications of losing or seriously reducing species closely tied
to the environmental heterogeneity of young wildfire stands,
however, remains unknown.
Our data also show that there is further development of the
arthropod fauna between 30 and 70 years post-disturbance. At
this point, however, it remains unknown when recovery is
complete for arthropod biodiversity in boreal systems. Old
mixedwood stands contain a unique fauna, including species
B I O L O G I C A L C O N S E RVAT I O N
with limited dispersal abilities and those dependent on dead
wood, which is lacking in younger harvested stands. These
species-specific findings illustrate further the role of natural
history information in guiding the biodiversity aspects of sustainable forest management. As shown with work in Fennoscandia, the lack of old forests, and the concurrent
reductions in dead wood, are major threats to biodiversity (Siitonen and Martikainen, 1994; Martikainen et al., 1999; Siitonen, 2001). In the boreal forests of Canada, we have an
opportunity to preserve these forest characteristics before
their reduction causes loss of species associated with them.
Acknowledgments
We thank the following agencies for funding and support:
Manning Diversified Forest Products Research Trust Fund,
the Sustainable Forest Management Network (Networks of
Centres of Excellence), the National Sciences and Engineering
Research Council of Canada (NSERC), a Challenge Grant in
Biodiversity (Department of Biological Sciences, University
of Alberta and the Alberta Conservation Association), the
Department of Biological Sciences (University of Alberta),
and Natural Resources Canada. We are indebted to following
people who helped with various aspects of this work: J. Hammond, K. Cryer, E. Nijenhuis, D. Williams, H. Cárcamo, T.
Spanton, P. Rodriguez, P. Lee, S. Crites. Additionally, D. Buckle,
R. Bennett, C.D. Dondale, R. Leech assisted with spider identifications; A. Smetana, A. Davies, J.M. Campbell, G. Ball and D.
Shpeley assisted with beetle identifications.
R E F E R E N C E S
Angelstam, P., Boutin, S., Schmiegelow, F.K.A., Villard, M.-A.,
Drapeau, P., Host, G., Innes, J., Isachenko, G., Kuuluvainen, T.,
Mönkkönen, M., Niemelä, J., Niemi, G., Roberge, J.-M., Spence,
J., Stone, D., 2004. Targets for boreal forest biodiversity
conservation – a rationale for macroecological research and
adaptive management. Ecological Bulletins 51, 487–509.
Angelstam, P.K., 1998. Maintaining and restoring biodiversity in
European boreal forests by developing natural disturbance
regimes. Journal of Vegetation Science 9, 593–602.
Armstrong, G.W., 1999. A stochastic characterisation of the
natural disturbance regime of the boreal mixedwood forest
with implications for sustainable forest management.
Canadian Journal of Forest Research 29, 424–433.
Armstrong, G.W., Adamowicz, W.L., Beck, J.A., Cumming, S.G.,
Schmiegelow, F.K.A., 2003. Coarse filter ecosystem
management in a nonequilibrium forest. Forest Science 49,
209–223.
Beaudry, S., Duschesne, L.C., Côté, B., 1997. Short-term effects of
three forestry practices on carabid assemblages in a jack pine
forest. Canadian Journal of Forest Research 27, 2065–2071.
Bergeron, Y., Leduc, A., Harvey, B.D., Gauthier, S., 2002. Natural fire
regime: a guide for sustainable management of the Canadian
boreal forest. Silva Fennica 36, 81–95.
Blake, S., McCracken, D.I., Eyre, M.D., Garside, A., Foster, G.N.,
2003. The relationship between the classification of Scottish
ground beetle assemblages (Coleoptera: Carabidae) and the
National Vegetation Classification of British plant species.
Ecography 26, 602–616.
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
355
Brzustowski, J., 2003. Rarefaction Calculator. Available from:
<http://www2.biology.ualberta.ca/jbrzusto/rarefact.php>.
Buddle, C.M., 2001. Spiders (Araneae) associated with downed
woody material in deciduous forest in central Alberta, Canada.
Agricultural and Forest Entomology 3, 241–251.
Buddle, C.M., Beguin, J., Bolduc, E., Mercado, A., Sackett, T.E.,
Selby, R.D., Varady-Szabo, H., Zeran, R.M., 2005. The
importance and use of taxon sampling curves for comparative
biodiversity research with forest arthropod assemblages. The
Canadian Entomologist 137, 120–127.
Buddle, C.M., Spence, J.R., Langor, D.W., 2000. Succession of boreal
forest spider assemblages following wildfire and harvesting.
Ecography 23, 424–436.
Bunnell, F.L., 1995. Forest-dwelling vertebrate faunas and natural
fire regimes in British Columbia: patterns and implications for
conservation. Conservation Biology 9, 636–644.
Cameron, E.A., Reeves, R.M., 1990. Carabidae (Coleoptera)
associated with gypsy moth Lymantria dispar (L.) (Lepidoptera:
Lymantriidae) populations subjected to Bacillus thurigiensis
Berliner treatments in Pennsylvania. The Canadian
Entomologist 122, 123–129.
Campbell, J.M., 1973. A revision of the genus Tachinus (Coleoptera:
Staphylinidae) of North and Central America. Memoirs of the
Entomological Society of Canada 90, 1–137.
Campbell, J.M., 1982. A revision of the North American Omaliinae
(Coleoptera: Staphylinidae) 3. The genus Acidota Stephens. The
Canadian Entomologist 114, 1003–1029.
Campbell, J.M., 1991. A revision of the genera Mycetoporus
Mannerheim and Ischnosoma Stephens (Coleoptera:
Staphylinidae: Tachyporinae) of North and Central America.
Memoirs of the Entomological Society of Canada 156, 1–169.
Connell, J.H., 1978. Diversity in tropical rain forests and coral
reefs. Science 199, 1302–1310.
Dale, V.H., Beyeler, S.C., 2001. Challenges in the development and
use of ecological indicators. Ecological Indicators 1, 3–10.
DeLong, S.C., Tanner, D., 1996. Managing the pattern of forest
harvest: lessons from wildfire. Biodiversity and Conservation
5, 1191–1205.
Dondale, C.D., Redner, J.H., 1978. The crab spiders of Canada and
Alaska (Araneae: Philodromidae and Thomisidae). The Insects
and Arachnids of Canada. Part 5. Agriculture Canada, Ottawa.
Dondale, C.D., Redner, J.H., 1990. The wolf spiders, nurseryweb
spiders, and lynx spiders of Canada and Alaska (Araneae:
Lycosidae, Pisauridae, and Oxyopidae). The Insects and
Arachnids of Canada. Part 17. Agriculture Canada, Ottawa.
DuDevoir, D.S., Reeves, R.M., 1990. Feeding activity of carabid
beetles and spiders on gypsy moth larvae (Lepidoptera:
Lymantriidae) at high-density prey populations. Journal of
Entomological Science 25, 341–356.
Dufrêne, M., Legendre, P., 1997. Species assemblages and
indicator species: the need for a flexible asymmetrical
approach. Ecological Monographs 67, 345–366.
Franklin, J.F., Spies, T.A., Pelt, R.V., Carey, A.B., Thornburgh, D.A.,
Berg, D.R., Lindenmayer, D.B., Harmon, M.E., Keeton, W.S.,
Shaw, D.C., Bible, K., Chen, J., 2002. Disturbances and
structural development of natural forest ecosystems with
silvicultural implications using Douglas-fir forests as an
example. Forest Ecology and Management 155, 399–423.
Gandhi, K.J.K., Spence, J.R., Langor, D.W., Morgantini, L.E., 2001.
Fire residuals as habitat reserves for epigaeic beetles
(Coleoptera: Carabidae and Staphylinidae). Biological
Conservation 102, 131–141.
Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity:
procedures and pitfalls in the measurement and comparison
of species richness. Ecology Letters 4, 379–391.
Grove, S.J., 2002. Saproxylic insect ecology and the sustainable
management of forests. Annual Review of Ecology and
Systematics 33, 1–23.
356
B I O L O G I C A L C O N S E RVAT I O N
Haeussler, S., Kneeshaw, D., 2003. Comparing forest
management to natural processes. In: Burton, P.J., Messier,
C., Smith, D.W., Adamowicz, W.L. (Eds.), Towards Sustainable
Management of the Boreal Forest. NRC Research Press,
Ottawa, pp. 307–368.
Haila, Y., Hanski, I.K., Niemelä, J., Punttila, P., Raivio, S., Tukia, H.,
1994. Forestry and the boreal fauna: matching management
with natural forest dynamics. Annales Zoologica Fennici 31,
187–202.
Hammond, H.E.J., 1997. Arthropod biodiversity from Populus coarse
woody material in north-central Alberta: a review of taxa and
collection methods. Canadian Entomologist 129, 1009–1033.
Harvey, B.D., Leduc, A., Gauthier, S., Bergeron, Y., 2002. Standlandacape integration in natural disturbance-based
management of the southern boreal forest. Forest Ecology and
Management 155, 369–385.
Hatch, M.H., 1957. The Beetles of the Pacific Northwest, Part II:
Staphyliniformia, University of Washington Publications in
Biology, Vol. 16, ix + 384pp. Seattle, WA.
Hobson, K.A., Shieck, J., 1999. Changes in bird communities in
boreal mixedwood forest: harvest and wildfire effects over 30
years. Ecological Applications 9, 849–863.
Holliday, N.J., 1991. Species responses of carabid beetles
(Coleoptera: Carabidae) during post-fire regeneration of boreal
forest. The Canadian Entomologist 123, 1369–1389.
Holliday, N.J., 1992. The carabid fauna (Coleoptera: Carabidae)
during postfire regeneration of boreal forests: properties and
dynamics of species assemblages. Canadian Journal of
Zoology 70, 440–452.
Huhta, V., 1971. Succession in the spider communities of the
forest floor after clear-cutting and prescribed burning. Annales
Zoologici Fennici 8, 483–542.
Hunter Jr., M.L., 1993. Natural fire regimes as spatial models for
managing boreal forests. Biological Conservation 65, 115–120.
Jennings, D.T., Dimond, J.B., Watt, B.A., 1990. Population densities
of spiders (Araneae) and spruce budworms (Lepidoptera,
Tortricidae) on foliage of balsam fir and red spruce in
east-central Maine. Journal of Arachnology 18, 181–193.
Jonsson, B.G., Jonsell, M., 1999. Exploring potential biodiversity
indicators in boreal forests. Biodiversity and Conservation 8,
1417–1433.
Kaston, B.J., 1948. Spiders of Connecticut. State Geological and
Natural History Survey, Bulletin 70. Hartford, CT.
Klimaszewski, J., 2000. Diversity of the rove beetles in Canada and
Alaska (Coleoptera: Staphylinidae). Memoire de la Societe
Royal Belge d’Entomologie 39, 3–126.
Koivula, M., Niemelä, J., 2003. Gap felling as a forest harvesting
method in boreal forests: responses of carabid beetles
(Coleoptera: Carabidae). Ecography 26, 179–187.
Larochelle, A., 1990. The food of carabid beetles (Coleoptera:
Carabidae, including Cicindelinae). Association des
Entomologistes Amateurs du Quebec, Fabreries Supplement 5:
1–132.
Larsson, S., Danell, K., 2001. Science and the management of
boreal forest biodiversity. Scandinavian Journal of Forest
Research 3, 5–9.
Lindroth, C.H., 1961–1969. The ground-beetles of Canada and
Alaska. Opuscula Entomologica (Supplement) 20, 24, 29, 33,
1–1192.
MacNally, R., Bennett, R.F., Brown, G.W., Lumsden, L.F., Yen, A.,
Hinkley, S., Lillywhite, P., Ward, D., 2003. How well do
ecosystem-based planning units represent different
components of biodiversity? Ecological Applications 12,
900–912.
Magurran, A.E., 2004. Measuring Biological Diversity. Blackwell,
Malden, MA.
Martikainen, P., Siitonen, J., Kaila, L., Punttila, P., Rauth, J., 1999.
Bark beetles (Coleoptera, Scolytidae) and associated beetle
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
species in mature managed and old-growth boreal forests
in southern Finland. Forest Ecology and Management 116,
233–245.
Mason, R.R., Jennings, D.T., Paul, H.G., Wickman, B.E., 1997.
Patterns of spider (Araneae) abundance during an outbreak of
western spruce budworm (Lepidoptera: Tortricidae).
Environmental Entomology 26, 507–518.
May, R.M., 1988. How many species are there on earth? Science
241, 1441–1449.
McCune, B., Mefford, M.J., 1999. PC-Ord: Multivariate Analysis of
Ecological Data. MjM Software Design, Gleneden Beach,
Oregon.
McGeoch, M.A., 1998. The selection, testing and application of
terrestrial insects as bioindicators. Biological Reviews 73,
181–201.
Naeem, S., 2002. Ecosystem consequences of biodiversity loss: the
evolution of a paradigm. Ecology 83, 1537–1552.
Newton, A.F., Thayer, M.K., Ashe, J.S., Chandler, D.S., 2001.
Staphylinidae Latreille, 1802. In: Arnett, R.H., Jr.Jr., Thomas,
M.C. (Eds.), American Beetles, vol. 1. CRC Press, Washington,
DC.
Nguyen-Xuan, T., Bergeron, Y., Simard, D., Fyles, J.W., Pare, D.,
2000. The importance of forest floor disturbance in the early
regeneration patterns of the boreal forest of western and
central Quebec: a wildfire versus logging comparison.
Canadian Journal of Forest Research 30, 1353–1364.
Niemelä, J., 1999. Management in relation to disturbance in the
boreal forest. Forest Ecology and Management 115, 127–134.
Niemelä, J., 2000. Biodiversity monitoring for decision-making.
Annales Zoologica Fennici 37, 307–317.
Niemelä, J., Haila, Y., Punttila, P., 1996. The importance of smallscale heterogeneity in boreal forests: variation in diversity in
forest-floor invertebrates across the succession gradient.
Ecography 19, 352–368.
Niemelä, J., Langor, D., Spence, J.R., 1993. Effects of clear-cut
harvesting on boreal ground-beetle assemblages (Coleoptera:
Carabidae) in western Canada. Conservation Biology 7,
551–561.
Oliver, I., Holmes, A., Dangerfield, J.M., Gillings, M., Pik, A.J.,
Britton, D.R., Holley, M., Montgomery, M.E., Raison, M., Logan,
V., Pressey, R.L., Beattie, A.J., 2004. Land systems as surrogates
for biodiversity in conservation planning. Ecological
Applications 14, 485–503.
Pajunen, T., Haila, Y., Halme, E., Niemelä, J., Punttila, P., 1995.
Ground-dwelling spiders (Arachnida, Araneae) in fragmented
old forests and surrounding managed forests in southern
Finland. Ecography 18, 62–72.
Perry, D.A., 1998. The scientific basis of forestry. Annual Review of
Ecology and Systematics 29, 435–466.
Petraitis, P.S., Latham, R.E., Niesenbaum, R.A., 1989. The
mainenance of species diversity by disturbance. The Quarterly
Review of Biology 64, 393–418.
Pratt, L., Urquhart, I., 1994. The Last Great Forest. NeWest Press,
Edmonton.
Rainio, J., Niemelä, J., 2003. Ground beetles (Coleoptera: Carabidae)
as bioindicators. Biodiversity and Conservation 12, 487–506.
Raymond, B., Venbergen, A., Watt, A., Hartley, S.E., Cory, J.S., Hails,
R.S., 2002. Escape from pupal predation as a potential cause of
outbreaks of the winter moth Operophtera brumata. Oikos 98,
219–228.
Reich, P.B., Bakken, P., Carlson, D., Frelich, L.E., Friedman, S.K.,
Grigal, D.F., 2001. Influence of logging, fire, and forest type on
biodiversity and productivity in southern boreal forests.
Ecology 82, 2731–2748.
Rowe, J.S., 1972. Forest Regions of Canada. Canadian Forest
Service Publications, Ottawa, Canada.
Saint-Germain, M., Larrivée, M., Drapeau, P., Fahrig, L., Buddle,
C.M., 2005. Short-term response of ground beetles
B I O L O G I C A L C O N S E RVAT I O N
(Coleoptera: Carabidae) to fire and logging in a sprucedominated boreal landscape. Forest Ecology and
Management 212, 118–126.
Setälä, H., Haimi, J., Sirra-Pietikäinen, A., 2000. Sensitivity of soil
processes in northern forest soils: are management practices a
threat? Forest Ecology and Management 133, 5–11.
Siitonen, J., 2001. Forest management, coarse woody debris and
saproxylic organisms: Fennoscandian boreal forests as an
example. Ecological Bulletins 49, 11–41.
Siitonen, J., Martikainen, P., 1994. Occurrence of rare and
threatened insects living on decaying Populus tremula: a
comparison between Finnish and Russian Karelia.
Scandinavian Journal of Forest Research 9, 185–191.
Simard, D.G., Fyles, J.W., Pare, D., Nguyen, T., 2001. Impacts of
clearcut harvesting and wildfire on soil nutrient status in the
Quebec boreal forest. Canadian Journal of Soil Science 81, 229–
237.
Simberloff, D., 1999. The role of science in the preservation of
forest biodiversity. Forest Ecology and Management 115, 101–
111.
Smetana, A., 1971. Revision of the tribe Quediini of America North
of Mexico (Coleoptera: Staphylinidae). Memoirs of the
Entomological Society of Canada 79, 1–303.
Smetana, A., 1995. Rove beetles of the subtribe Philonthina of
America North of Mexico (Coleoptera: Staphylinidae).
Classification, phylogeny, and taxonomic revision. Memoirs
on Entomology International 3, 1–946.
Spence, J.R., 2001. The new boreal forestry: adjusting timber
management to accomodate biodiversity. Trends in Ecology
and Evolution 16, 591–593.
Spence, J.R., Buddle, C.M., Gandhi, K., Langor, D.W., Volney, W.J.A.,
Hammond, H.E.J., Pohl, G.R., 1999. Invertebrate biodiversity,
forestry and emulation of natural disturbance: a down-toearth perspective. In: Pacific Northwest Forest and Rangeland
Soil Organism Symposium. USDA Forest Service, Technical
Report PNW-GTR-461, Pacific NW Research Station, Portland,
OR, pp. 80–90.
1 2 8 ( 2 0 0 6 ) 3 4 6 –3 5 7
357
Spence, J.R., Langor, D.W., Niemelä, J., Cárcamo, H.A., Currie, C.R.,
1996. Northern forestry and carabids: the case for concern
about old-growth species. Annales Zoologici Fennici 33,
173–184.
Spence, J.R., Niemelä, J.K., 1994. Sampling carabid assemblages
with pitfall traps: the madness and the method. Canadian
Entomologist 126, 881–894.
Strong, W.L., Leggat, K.R., 1992. Ecoregions of Alberta Alberta
Forest Lands and Wildlife, Edmonton.
Tilman, D., 1999. The ecological consequences of changes in
biodiversity: a search for general principles. Ecology 80,
1455–1474.
Van Helsdingen, P.J., 1974. The affinities of Wabana and Allomengea
with some notes on the latter genus (Araneae, Linyphiidae).
Zoologische Mededelingen 46, 295–321.
Wikars, L.-O., 1995. Clear-cutting before burning prevents
establishment of the fire-adapted Agonum quadripunctatum
(Coleoptera: Carabidae). Annales Zoologica Fennici 32, 375–384.
Wikars, L.-O., Schimmel, J., 2001. Immediate effects of fire severity
on soil invertebrates in cut and uncut pine forests. Forest
Ecology and Management 141, 189–200.
Wilson, E.O., 1992. The Diversity of Life. W.W. Norton & Company,
New York.
Work, T.T., Shorthouse, D.P., Spence, J.R., Volney, W.J.A., Langor, D.,
2004. Stand composition and structure of the boreal
mixedwood and epigaeic arthropods of the Ecosystem
Management Emulating Natural Disturbance (EMEND)
landbase in northwestern Alberta. Canadian Journal of Forest
Research 34, 417–430.
Work, T.T., Spence, J.R., Volney, W.J.A., Burton, P.J., 2003.
Sustainable forest management as license to think and to try
something different. In: Burton, P.J., Messier, C., Smith, D.W.,
Adamowicz, W.L. (Eds.), Towards Sustainable Management of
the Boreal Forest. NRC Research Press, Ottawa, pp. 953–970.
Yodzis, P., 1986. Competition, mortality and community structure.
In: Diamond, J.M., Case, T.J. (Eds.), Community Ecology. Harper
& Row, New York, pp. 480–491.