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A shade tolerance index for common
understory species of northeastern North
America
Article in Ecological Indicators · January 2007
DOI: 10.1016/j.ecolind.2005.12.002 · Source: OAI
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Ecological Indicators 7 (2007) 195–207
This article is also available online at:
www.elsevier.com/locate/ecolind
A shade tolerance index for common understory
species of northeastern North America
Lionel Humbert *, Daniel Gagnon, Daniel Kneeshaw, Christian Messier
Groupe de Recherche en Écologie Forestière Interuniversitaire (GREFi), Département des Sciences Biologiques,
Université du Québec à Montréal, Case Postale 8888, Succursale Centre-Ville, Montréal, Qc., Canada H3C 3P8
Received 12 June 2005; received in revised form 29 November 2005; accepted 2 December 2005
Abstract
Since Baker’s [Baker, F.S., 1949. A revised tolerance table. J. For. 47, 179–181] classic contribution, shade tolerance indices
have not been much modified for North American plant species. While many common tree and shrub species are included in the
shade tolerance index, much less is known about this characteristic for the abundant and rich understory vascular and
nonvascular plant layers. The classification of the shade tolerance is widely used to compare relative growth and survival among
plant species under closed canopies and is also fundamental to an understanding of stand development following small and large
scale disturbances. Although qualitative, it is frequently used both in research and management implications. Here we provide a
significant revision to Baker’s shade tolerance table to include the most common forest understory plant species found in
northeastern North America forests. Our index is based on: (1) the compilation of the opinions of five experts, (2) a comparison
with Ellenberg’s index from Europe as well as, (3) information from current literature. For most of the 347 plant species
investigated, a consistent and robust shade tolerance index, ranging between 1 (very tolerant) and 9 (very intolerant), was found.
Here we present revised shade indices for 71 tree and shrub species, 185 herbaceous species, and 91 bryophyte and lichen
species.
# 2005 Elsevier Ltd. All rights reserved.
Keywords: Shade tolerance; Understory species; Ellenberg L index; Baker shade tolerance table
1. Introduction
Light is one of the most studied ecological factors in
plant ecophysiology due to its essential function
autotrophic plants. It has been characterized under a
wide variety of atmospheric conditions and under
* Corresponding author. Tel.: +1 514 9873000.
E-mail address: humbert.lionel@courrier.uqam.ca
(L. Humbert).
various plant covers (e.g. Hutchison and Matt, 1977;
Gendron et al., 1998). We now know that not only its
quantity, but also its quality and variability are
important characteristics for plant growth. Similarly,
many basic characteristics of plant functional acclimatation and adaptation to light have been reported
(Messier et al., 1999). However, even with our extensive
documentation of the range of light conditions, the
fundamental mechanisms of shade tolerance are still
not fully understood (Lin et al., 2001). What we know is
1470-160X/$ – see front matter # 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecolind.2005.12.002
196
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
that shade tolerance includes a suite of traits that can
take different forms depending on the species and the
environments. However, generally, shade tolerance
indicates the degree to which a plant can survive and
grow in low light conditions (Shirley, 1943; Kobe et al.,
1995), and plants have been classified into three broad
categories: shade tolerant, intermediately shade tolerant
and shade intolerant species (Anderson et al., 1969).
Although imperfect and rather coarse, such a classification has proven very useful in classifying trees into
broad functional types (Baker, 1949).
However, useful such a classification has been for
tree and shrub species, there is no North American
equivalent for understory herbaceous plants, bryophytes and lichens. In Europe, Ellenberg (c.f.
Ellenberg, 1979; Ellenberg et al., 1992) has successfully characterized the shade tolerance of most plants
using an index from 1 to 9. This classification has
proven to be very useful not only to better understand
the autecology of plant species, but also to use the
presence or absence of various understory plant
species as an indicator of understory light levels.
This paper proposes a shade tolerance index of
common understory species present in the temperate
hardwood forest of southern Quebec, Canada, and, in
fact, common in northeastern North America.
2. Methods
An index of shade tolerance was developed for
common forest understory species where shade
tolerance was based on three independent sources
of information. First, a group of five experts was
surveyed and asked to rank the shade tolerance of a
number of plant species (see below). Secondly, these
responses were validated with published information
available for understory species, mostly studied in
North America. Thirdly, these results were compared
with the ranking proposed by Ellenberg in Europe for
co-occurring species.
2.1. Using the opinions of experts
As with Baker (1949) and, more recently, Hess and
King (2002), a questionnaire was sent to five expert
plant ecologists who have extensive field experience
with most plants found in the northeastern North
American forest. The list included close to 400
species, including bryophytes and lichens. For woody
species, only the seedling stage was considered.
The questionnaire required respondents to rank the
light environment where the species grow and survive
most commonly on a scale of one to five. The five
levels were: (1) deep shade, (2) shade, (3) moderate
shade, (4) partly open and (5) completely open. No
indications of the light environment (percent of full
sunlight) was required or requested. Due to the nature
of the question, the answers did not provide a direct
shade tolerance ranking, but rather an evaluation of the
overall light environment in which the species were
found to grow well. According to Brissot (1972), the
light environment is the sum of three environmental
factors: light, temperature and desiccation. In addition, the common occurrence of a species at a
particular light level does not mean that this species is
at its physiological optimum, but only that it is the best
competitor in this environment. Consequently, we
have determined the ‘‘ecological existence’’ not the
‘‘ecological potential’’ (Ellenberg, 1996; Whittaker
et al., 1973) of each plant species at a given light level.
All results were then adjusted to a nine level scale
for comparisons with Ellenberg’s index. This transformation did not change the mean of the values;
consequently, comparisons between data were not
affected. An overall result was compiled from the
questionnaires and the mean (X̄e ) and standard
deviation (s e ) were calculated.
2.2. Using published data
Published results have focused primarily on the
response of tree species, rarely are herbaceous
species and bryophytes reported in shade tolerance
studies. In this paper, the following references were
used: Grandtner (1997), Burns and Honkala (1990a,
b), Minnesota Department of Transportation (2002),
Ritchie (1996), Bakuzis and Hansen (1959), Haussler and Coates (1986), Beaudry et al. (1999),
Jobidon (1995), Ellenberg et al. (1992). The
publication by Ellenberg et al. (1992) is important
because of the vast number of species described and
the strong correspondence between bryophytes in
Europe and North America, as well as of some
introduced vascular plants. The Ellenberg L index is
based on phyto-sociological relevés combined with
197
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
light measurements taken during the summer.
Nearly 140 species, of which half are bryophytes,
are present in both Quebec and Europe and could
then be compared.
As with the previous section for the experts, all
results were then adjusted to a nine level scale, the
mean (X̄p ) and the standard deviation (s p ) were
calculated.
2.3. Compilation
We chose to compile these data into a synthetical
index based on the comparison of the mean and the
standard deviation of the different sources. The kind of
system used here is a hierarchical one which allows us
to automatize the ranking, and the different levels in
the hierarchy are used to optimize the usefulness of the
data. We first classified results into two categories :
homogeneous and nonhomogeneous, and this is done
for the expert part of the data and the published part.
This homogeneity is simply related to s. When both
expert and published data were homogeneous we
compared means, and if the difference was no more
than two, we used the expert result as the index. If not,
this result was rejected and a second level of
integration was conducted. This second level mixed
together expert and published data. To do this we
calculated s, and as in the upper level (explained
above) we deduced the homogeneity from it. When it
was homogeneous, we took the X̄ as the index.
Rejected results were analysed in a final level case by
case. When the general result was close (one or two
points higher or lower) to the Ellenberg index we
systematically chose the Ellenberg index. This choice
was driven by the fact that Ellenberg’s index is more
precise (nine levels) compared to our questionnaire
(five levels).
3. Results and discussion
3.1. Questionnaire and data from the literature
Table 1 shows a compilation of the classification
given by the five experts. At least one expert evaluated
all woody species, both tree seedlings and shrubs. The
family Salicaceae and the genus Amelanchier received
the fewest responses. We received responses for nearly
Table 1
Comparison between the original list of species, collected data and
the resulting number of species with an attributed shade tolerant
index value
Original list
Botanist A
Botanist B
Botanist C
Botanist D
Botanist E
Published
Ellenberg
Synthetic index
Total
species
Trees and
shrubs
Herbaceous
plants
Bryophytes
and lichens
405
96
239
223
291
172
128
139
347
72
42
67
47
71
53
57
3
71
201
48
141
151
187
119
57
50
185
132
6
31
25
33
0
14
86
91
all the herbaceous species included in the survey. Only
five species (2%) could not be evaluated by any of the
experts. An additional 23 species (11%) received
evaluations from only one expert. Among herbaceous
plants, the Poaceae and Renonculaceae families
received the fewest responses. Among the bryophytes,
however, the response level was much lower, with no
responses being provided for 74 species and only one
answer for 34 other species.
The responses of the experts (Table 2) are very
similar for 48% of the species and can be qualified as
homogeneous. This homogeneity is defined by a low
s, in this case less than 1.75, 1.50, 1.25 and 1.00
depending on the number of responses. For 16% of the
species, the responses of the experts are different
(s e > 2.25), for 6% of the species the responses are
very different (s e > 3.00).
From the literature reviewed, data was obtained for
128 species (57 woody species, 57 herbaceous species,
and 14 bryophytes and lichens) (Table 1). However, 76
of these species (59%) were found in only one
publication. Similar to the questionnaire, information
from literature (Table 2) was homogeneous for 28% of
the species, different for 4%, and very different for one
species. In light of this variation, results from the
experts and the literature were compared to produce a
synthetic index (Column I in Table 2).
3.2. Comparisons
Comparisons between the published data and the
expert opinions show a difference greater or equal to
three light levels for 19 species. Eight of these are
198
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2
Shade tolerance index for common understory species in the temperate hardwood forest of southern Quebec
Species
Achillea millefolium
Actaea pachypoda
Actaea rubra
Adiantum pedatum
Ageratina altissima
Agrimonia gryposepala
Agrimonia striata
Agrostis capillaries
Agrostis gigantean
Anaphalis margaritacea
Anemone canadensis
Anemone virginiana var. alba
Antennaria parlinii ssp. fallax
Apocynum androsaemifolium
Aquilegia canadensis
Arabis drummondii
Aralia nudicaulis
Asplenium viride
Aster puniceus
Athyrium filix-femina
Botrychium virginianum
Calamagrostis canadensis
Calypso bulbosa
Cardamine diphylla
Carex arctata
Carex brunnescens
Carex communis
Carex deweyana
Carex intumescens
Carex pensylvanica
Carex retrorsa
Carex trisperma
Centaurea nigra
Chimaphila umbellate
Chrysosplenium americanum
Cinna latifolia
Circaea alpina
Cirsium muticum
Claytonia caroliniana
Clinopodium vulgare
Clintonia borealis
Coeloglossum viride var. virescens
Comandra umbellate ssp. umbellate
Conioselinum chinense
Coptis trifolia
Corallorhiza maculata
Corallorhiza trifida
Cryptogramma stelleri
Cypripedium acaule
Cystopteris bulbifera
Cystopteris fragilis
Danthonia spicata
Str
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Int
s
s
s
s
Experts
Literature
n
se
X̄e
n
sp
X̄p
4
3
4
4
3
2
2
2
1
4
3
1
1
5
2
2
5
4
4
5
4
4
3
3
4
1
2
2
4
1
1
2
1
4
2
3
4
3
4
2
5
2
3
3
5
4
5
2
4
3
3
3
0
1.53
1.26
1
1
3.54
4.24
0
9
2.7
2.8
2.5
6
5.5
6
9
9
8.5
8
8
9
8.6
8.5
9
4.6
5
6
3.4
3
9
1.7
2.7
3.3
4
3.5
3.5
4.3
8
9
6
9
3.8
4
5.7
2.8
7.7
8.5
7
3.6
3
6.7
4
3.2
1.5
2.6
5
4.3
3.3
4
7.7
3
1.15
7.7
2
0
3
2
1.41
8
1
1
0.89
0.71
0
1.67
3.65
2.58
1.67
0
0
1.15
0.58
1.71
0.71
0.71
1.89
1.41
0.96
1.41
3.06
0.5
1.15
1
2.83
0.89
0
3.21
2.65
0.45
1
1.67
2.83
1.89
1.53
1
2.31
1
7
1
7
1
3
Ell.
I
8
8
3
3
2
6
X
X
9
7
9
8
8
9
9
8
9
5
4
X
3
3
9
2
3
3
9
4
4
3
X
9
6
8
4
4
X
4
8
9
7
4
3
X
X
3
1
3
X
3
3
5
9
7
7
4
4
1
0.96
1.8
3
6
6
9
1
3
1
7
1
1
3
1
4
1
7
7
8
4
x
1
3
5
199
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Deschampsia flexuosa
Dicentra cucullaria
Draba arabisans
Drosera rotundifolia
Dryopteris carthusiana
Dryopteris marginalis
Elymus trachycaulus ssp. trachycaulus
Empetrum nigrum
Epigaea repens
Epilobium angustifolium
Epilobium ciliatum ssp. glandulosum
Epilobium palustre
Equisetum arvense
Equisetum hyemale
Equisetum pratense
Equisetum scirpoides
Equisetum sylvaticum
Eriophorum virginicum
Eupatorium maculatum
Eurybia macrophylla
Fragaria virginiana
Galeopsis tetrahit
Galium asprellum
Galium trifolium
Gaultheria hispidula
Gaultheria procumbens
Geum rivale
Glyceria striata
Goodyera oblongifolia
Goodyera repens
Gymnocarpium disjunctum
Heracleum sphondylium ssp. montanum
Hieracium caespitosum
Hieracium scabrum
Huperzia lucidula
Hypericum perforatum
Impatiens capensis
Iris versicolor
Lactuca biennis
Lactuca canadensis
Leucanthemum vulgare
Linnaea borealis
Listera convallarioides
Listera cordata
Lycopodium annotinum
Lycopodium clavatum
Lycopodium complanatum
Lycopodium obscurum
Lycopodium tristachyum
Maianthemum canadense
Maianthemum trifolium
Matteuccia struthiopteris
Medeola virginiana
Str
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Int
$
s
s
s
s
Experts
Literature
n
se
X̄e
n
2
3
2
4
5
4
2
4
4
5
3
3
4
4
3
3
5
4
4
4
5
5
5
5
5
5
3
3
3
4
4
4
3
3
5
4
4
5
4
2
4
5
4
4
5
4
4
5
4
5
4
4
4
0
3.46
1.41
1
1.1
2.22
1.41
0
2.31
0
1.15
2
2.75
2.22
2.65
0.58
0.89
0
1
1.63
0.89
1.1
2.61
2.19
2.24
2.19
1.15
2
0
1.15
1.26
1
0
1.15
0.89
1
2.22
1.67
2
0
0
2.28
1.63
1.63
0.89
2.22
1
0.45
1.26
1.79
1.91
2.06
1.26
9
7
8
8.5
2.8
3.8
8
9
5
9
8.3
7
5.8
6.3
6
2.7
3.6
9
8.5
5
8.6
8.2
5.4
3.6
4
5.4
5.7
7
1
2
2.8
8.5
9
8.3
2.6
8.5
3.8
7.6
8
9
9
3.8
3
3
4.4
5.8
4.5
3.2
5.3
3.8
7.5
4.8
2.8
1
sp
Ell.
I
6
9
X
8
8
3
X
8
9
X
8
8
7
6
5
5
3
3
9
9
6
9
7
X
X
3
X
6
7
1
2
3
7
8
8
3
7
X
8
9
9
9
5
3
3
3
8
5
3
5
4
8
5
3
X̄p
7
8
5
1
1
7
7
7
7.6
8
1
1
7
3
7
6
5
5
1
3
3
1
7
1
1
5
9
1
1
3
3
1
7
1
1
3
5
1
7
7
8
1
8
7
5
0.89
7
6
7
5
3
3
8
2
0
3
5
200
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Melampyrum lineare
Mentha arvensis
Mentha canadensis
Milium effusum
Mitchella repens
Mitella nuda
Moneses uniflora
Monotropa hypopithys
Monotropa uniflora
Onoclea sensibilis
Orthilia secunda
Oryzopsis asperifolia
Oryzopsis pungens
Osmorhiza berteroi
Osmorhiza longistylis
Osmunda cinnamomea
Osmunda claytoniana
Oxalis acetosella
Panicum acuminatum var. acuminatum
Pedicularis canadensis
Petasites frigidus var. palmatus
Phegopteris connectilis
Platanthera dilatata var. dilatata
Platanthera obtusata
Platanthera orbiculata
Poa interior
Polygala paucifolia
Polygonatum pubescens
Polypodium virginianum
Polystichum braunii
Polystichum lonchitis
Potentilla norvegica
Potentilla recta
Potentilla simplex
Prenanthes altissima
Prenanthes trifoliolata
Prunella vulgaris
Pteridium aquilinum
Pteridium aquilinum var. latiusculum
Pyrola asarifolia
Pyrola chlorantha
Pyrola elliptica
Pyrola rotundifolia
Ranunculus abortivus
Ranunculus acris
Ranunculus repens
Rubus allengheniensis
Rubus chamaemorus
Rubus idaeus
Rubus pubescens
Rumex aquaticus var. fenestratus
Sanguisorba canadensis
Sanicula marilandica
Str
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Int
s
s
s
Experts
Literature
Ell.
n
se
X̄e
n
4
2
2
3
4
5
4
4
5
5
3
4
2
3
3
5
4
4
2
2
4
4
2
3
3
1
4
4
4
4
3
4
1
1
4
3
4
3
4
4
3
5
5
3
3
2
2
4
5
5
2
4
3
1.5
0.71
0.71
3.46
1.26
0.89
0.96
0.96
0.45
1.79
1
1.5
3.54
1.53
1.53
2.97
2.22
1.63
0
4.24
3.46
1.26
2.83
1.15
5.8
8.5
8.5
5
2.8
2.4
2.3
1.8
1.2
5.2
2
4.3
5.5
2.7
2.7
5.4
4.3
3
9
4
6
2.8
5
3.7
3
9
4.8
3.8
2.8
3
3
8.5
9
9
4.3
2.7
6
7.7
7
2.8
3.7
3.6
4
6.3
9
7
9
8
8.4
3.4
9
8.5
3.3
1
1
3
7
6
1
3
4
1
1
1
2
3
3
3
3
3.3
2.5
1.26
1.63
0
1
3.4
1.53
3.46
1.15
1.63
0.5
1.15
0.89
1
1.15
0
2.83
0
1.15
0.89
1.67
0
1
2.52
sp
4
0
1
3
1
1
1
2
1
3
1
3
4
1
3
6
7
9
1
3
2
1.73
2.83
9
6
5
7
6
1
5
1
3
4
1
5
7
6
7.2
9
7
5
1
1.1
I
X̄p
3
5
8
8
4
3
2
4
2
1
5
2
4
X
3
3
X
5
1
9
X
X
3
X
4
3
9
X
X
3
3
3
7
9
9
X
3
7
6
7
3
4
4
4
6
9
6
9
9
7
3
9
9
4
201
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Saxifraga paniculata ssp. neogaea
Schizachne purpurascens
Scutellaria lateriflora
Senecio aureus
Smilacina racemosa
Solidago hispida
Solidago juncea
Solidago macrophylla
Solidago rugosa
Streptopus amplexifolius
Streptopus lanceolatus var. roseus
Taraxacum officinale
Thalictrum pubescens
Thelypteris noveboracensis
Trientalis borealis
Trillium cernuum
Trillium erectum
Trillium undulatum
Urochloa xantholeuca
Viola adunca
Viola cucullata
Viola incognita
Viola macloskeyi ssp. pallens
Viola pubescens
Viola renifolia
Viola selkirkii
Waldsteinia fragarioides
Aulacomnium palustre
Barbilophozia barbata
Barbilophozia hatchery
Bazzania trilobata
Blepharostoma trichophyllum
Brachythecium populeum
Brachythecium reflexum
Brachythecium rutabulum
Brachythecium salebrosum
Brachythecium velutinum
Buellia disciformis
Callicladium haldanianum
Calypogeia neesiana
Campylium chrysophyllum
Campylium stellatum
Cladina rangiferina
Cladina stellaris
Cladonia cenotea
Cladonia coniocraea
Cladonia deformis
Cladonia mitis
Cladonia rangiferina
Cladonia squamosa
Cladonia uncialis
Climacium dendroides
Dicranum flagellare
Str
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
Int
s
Experts
Literature
n
se
X̄e
4
3
4
1
4
3
1
4
4
4
3
5
4
4
5
5
4
3
1
1
1
3
4
3
4
3
3
1
0
2.31
2.06
9
7.7
5.3
9
4.3
7
9
5.5
7
3
3.7
9
4
3.8
3.4
3
4.5
3
9
7
3
3
3.5
3.7
3.5
3.7
6.7
3
3
1.89
2
3
1.63
1.63
1.15
0
1.15
2.5
0.89
1.41
1.91
0
0
1
1.15
1
1.15
1.53
1.15
3
1
9
0
1.15
1
1
sp
Ell.
9
8.3
5
5
1
9
1
3
1
6
1
7
3
3
3
1.15
1.15
8.3
8.3
1
2
1
1.41
9
2
3
7
8
6
5
5
4
4
6
5
4
6
5
9
8
1
I
X̄p
2.3
1
2
3
n
3
6
5
7
9
6
6
8
7
6
9
9
X
9
3
6
9
X
7
5
4
9
4
X
3
3
4
3
9
7
3
3
3
4
3
4
7
7
8
6
3
5
4
4
X
6
5
4
6
5
9
8
X
8
6
5
7
9
8
6
8
7
6
202
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Dicranum fuscescens
Dicranum majus
Dicranum montanum
Dicranum polysetum
Dicranum scoparium
Eurhynchium pulchellum
Graphis scripta
Herzogiella striatella
Heterocladium dimorphum
Hylocomium splendens
Hypnum lindbergii
Hypnum pallescens
Hypnum pratense
Hypogymnia physodes
Hypogymnia tubulosa
Jungermania leiantha
Lepidozia reptans
Leucobryum glaucum
Lobaria pulmonaria
Marchantia polymorpha
Mnium spinulosum
Neckera pennata
Oncophorus wahlenbergii
Paraleucobryum longifolium
Parmelia saxatilis
Parmelia sulcata
Parmeliopsis ambigua
Peltigera aphtosa
Peltigera canina
Peltigera horizontalis
Peltigera leucophlebia
Pertusaria amara
Plagiochila asplenioides
Plagiothecium denticulatum
Plagiothecium laetum
Platismatia glauca
Pleurozium schreberi
Pohlia nutans
Polytrichum commune
Polytrichum formosum
Polytrichum juniperinum
Polytrichum piliferum
Ptilidium ciliare
Ptilidium pulcherrimum
Ptilium crista-castrensis
Radula complanata
Ramalina fastigiata
Rhizomnium magnifolium
Rhytidiadelphus triquetrus
Sphagnum centrale
Sphagnum fuscum
Sphagnum girgensohnii
Sphagnum magellanicum
Str
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
Int
Experts
Literature
n
se
X̄e
3
1.15
2.3
n
sp
1
2
2
2
2
0
2.83
1.41
0.71
3
5
2
4.5
4
1.26
2.8
1
1
1
7
1
2
3
4.24
3.61
1
2
2
3
6
4
1
1
1.41
4
7
3
2.83
2.83
1
5
5
6
1
1
3
2.52
3
3
5.3
4
1.5
6.3
2
2
1
1.41
0
8
9
3
3
1.15
2.3
1
3
1
2
1
1
2
4.16
1.41
3
4.3
5
8
3
5
Ell.
I
7
5
6
6
5
6
3
6
8
6
8
5
8
7
7
4
4
5
5
8
5
5
5
4
6
7
6
2
5
3
6
5
6
3
6
8
3
8
5
8
7
7
4
4
5
5
8
5
5
5
4
6
7
6
X
6
5
5
6
4
5
4
7
6
5
7
4
8
9
8
7
4
7
7
5
7
6
9
4
9
X̄p
1
3
1
7
1
1
3
7
1
3
1
3
1
3
6
5
5
6
4
5
4
7
6
5
7
4
8
9
8
7
4
7
7
5
7
6
9
4
9
203
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Str
Int
Experts
n
Sphagnum rubellum
Sphagnum russowii
Sphagnum squarrosum
Tetraphis pellucida
Thuidium delicatulum
Thuidium recognitum
Tortella tortuosa
Trichocolea tomentella
Ulota coarctata
Ulota crispa
Usnea filipendula
Usnea subfloridana
Abies balsamea
Acer pensylvanicum
Acer rubrum
Acer saccharum
Acer spicatum
Alnus incana ssp. rugosa
Alnus viridis ssp. crispa
Amelanchier alnifolia
Amelanchier arborea
Amelanchier bartramiana
Amelanchier laevis
Amelanchier sanguinea var. gaspensis
Amelanchier sanguinea var. sanguinea
Andromeda polifolia var. glaucophylla
Aronia melanocarpa
Betula alleghaniensis
Betula papyrifera
Cassandra calyculata
Chamaedaphne calyculata
Comptonia peregrina
Cornus alternifolia
Cornus canadensis
Cornus sericea ssp. sericea
Corylus cornuta
Diervilla lonicera
Fagus grandifolia
Fraxinus nigra
Ilex mucronata
Kalmia angustifolia
Kalmia polifolia
Larix laricina
Ledum groenlandicum
Lonicera canadensis
Myrica gale
Ostrya virginiana
Picea glauca
Picea mariana
Pinus banksiana
Pinus resinosa
Pinus strobus
Populus balsamifera
M
M
M
M
M
M
M
M
M
M
M
M
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
Literature
se
1
1
1
2
$
$
X̄e
7
5
3
1.41
sp
1
1
1
1
4
2
4
4
5
5
5
2
3
3
3
3
2
4
4
5
2
5
3
5
5
5
5
4
5
3
4
5
5
5
4
5
5
5
2
4
4
5
4
4
4
9
9
3
4
5.5
4
5.2
7.2
7.6
8
5.3
6.7
5.3
7.3
6.5
8.5
8.5
5.2
7
7.8
8.3
7.4
3.6
4.6
6.6
3.8
5.8
4.3
5
5.8
7
7.8
9
7
3
9
5
4
5
8.8
8.5
6
9
Ell.
I
9
6
5
3
7
5
5
6
6
4
9
6
5
3
7
5
5
6
6
4
9
7
3
3
5
4
5
7
8
8
X
7
X
8
X
9
9
5
7
8
7
7
4
X
7
4
6
2
5
5
8
8
9
7
X
8
X
4
X
9
8
6
9
X̄p
5
2
1
0
1.41
1
1.15
1.48
1.48
1.67
1.41
2.52
1.53
2.52
2.08
2.12
1
1
1.48
0
1.79
1.15
1.67
1.67
1.67
1.67
0.96
1.79
2.31
0
1.79
2
1.79
0
1.41
2
0
2.83
1.15
2.31
0.45
1
1.15
0
n
7
4
2
6
4
4
6
2
2
1
1.26
0
1.67
0.5
1.26
1.75
2.12
0.71
2.8
1
5
1.3
3.3
6.3
6.5
7.5
1
2
1
2
1
1
5
8
0
1.64
1.13
1
8
5.5
9
7
3.8
7.1
2
1.41
8
1
2
1
3
1
3
5
3.54
2.83
1.73
0.58
2.59
1
7
1
3
9
6
7
1.3
5.8
3
6
4
0.52
1.5
8.7
7.8
5
4
5
5
5
6
6
1.34
1.29
1.82
1.67
1.22
1.03
1.1
2.4
4.5
4.6
7.6
7
5.3
8
8
8
204
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
Table 2 (Continued )
Species
Populus grandidentata
Populus tremuloides
Prunus pensylvanica
Prunus serotina
Prunus virginiana
Quercus rubra
Ribes glandulosum
Ribes hirtellum
Ribes lacustre
Ribes triste
Rosa acicularis
Salix bebbiana
Salix discolor
Salix eriocephala
Salix humilis
Sambucus racemosa ssp. pubens
Shepherdia canadensis
Sorbus americana
Sorbus decora
Taxus canadensis
Thuja occidentalis
Tsuga canadensis
Ulmus americana
Vaccinium angustifolium
Vaccinium myrtilloides
Vaccinium ovalifolium
Vaccinium oxycocos
Viburnum cassinoides
Viburnum edule
Viburnum opulus var. americanum
Str
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
Int
$
$
Experts
Literature
Ell.
n
se
X̄e
n
sp
X̄p
4
3
4
2
5
5
5
4
5
4
4
4
2
1
1
4
3
5
4
5
5
3
3
5
5
3
4
4
4
3
0
0
1
1.41
2.41
1.1
1.79
1.91
1.41
2.52
2.87
1.15
1.41
9
9
8.5
8
3.6
6.8
3.8
3.5
3
3.5
7.3
8
8
9
9
4.8
8.3
5.4
6.5
1.6
3.4
3
7
6.8
6.8
3
7
5.8
5.5
7
5
8
4
5
2
4
1
1.22
0.83
0.5
2
0.71
1.29
8
8.1
8.8
6
7.5
5.5
5
1.71
1.15
0.89
1.91
0.89
1.67
2
2
1.79
2.68
2
2.83
2.22
3.42
2
1
4
2
1
2
1
1
2
1
4
4
4
1
6
0.82
0.71
1.41
2.83
2.16
0.96
1.71
8
8.5
9
6
9
8
7
3
4
1.8
5.3
3
2
1
0
1
9
2
2.12
5.5
I
9
9
9
8
X
7
4
4
3
3
X
8
8
9
9
5
8
5
X
2
3
3
6
7
X
3
X
X
X
7
Strata (Column Str) refers to woody species (W ¼ tree seedlings and shrubs), Herbaceous plants (H) and Bryophytes (M). Int column describe
species native to Europe (s) and North American species introduced to Europe ($). n is the number of responses, s the standard deviation and X̄ is
the mean. The Ell. column lists the Ellenberg index. The last column, I, lists our proposed synthetic index and X indicates species with broad
amplitudes.
woody species: Acer pensylvanicum, Amelanchier
arborea, Amelanchier laevis, Fagus grandifolia,
Kalmia angustifolia, Prunus virginiana, Ribes lacustre and Vaccinium angustifolium. There was, however,
little data for the genus Amelanchier which may
explain its high variability. A. pensylvanicum and P.
virginiana are non-commercial species and were not
well documented in published data. The case of F.
grandifolia is different because only one divergent
response was given compared to five homogeneous
ones. Thus, without this one ‘‘outlier’’ point, the result
is very good. Furthermore, the value for F. grandifolia
did match Ellenberg’s index for Fagus sylvatica. The
herbaceous species that were treated in the literature
included Calamagrostis Canadensis, Carex pensylvanica, Equisetum hyemale, Fragaria virginiana, Goodyera repens, Petasites frigidus var. palmatus, Prunella
vulgaris and Sanguisorba canadensis. There was a
high variation in classification and this is probably due
to lack of data and the fact that some families are not
well-known (e.g. Poaceae). The same was true for the
bryophytes and lichens (Aulacomnium palustre,
Cladina rangiferina and Marchantia polymorpha).
Ellenberg et al. (1992) provides comparable data
for three woody species, 50 herbaceous species and 86
bryophytes and lichens. The bryophyte layer alone
contains 42 species for which we found no North
American data, and four other species that have no
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
American counterpart. In most cases the value
obtained for North America is lower than Ellenberg’s
index, but given that there are few data we feel that it is
not appropriate to reject Ellenberg’s value and thus we
preferred to use the Ellenberg value as a final index.
However, this should be taken into account when
applying the index, and further testing of the given
value and the North American result should be
pursued. For woody and herbaceous species, there is a
strong similarity between Ellenberg’s index and the
experts’ responses reported here. It is similar for 64%
of the species (difference < 1.50), and very similar
for 26% (difference < 1.00), with only 9% of species
that were very different. Some of the vascular species
are native to Europe but were introduced to North
America (Rousseau, 1968, 1974): Achillea millefolium, Agrostis capillaris, Agrostis gigantean,
Centaurea nigra, Galeopsis tetrahit, Hieracium
caespitosum, Hypericum perforatum, Leucanthemum
vulgare, Potentilla recta, Ranunculus acris, Ranunculus repens and Taraxacum officinale. Only the
results for A. capillaris and R. acris show a two point
difference with Ellenberg, whereas the others species
are similar to the European index. There are also North
American species that were introduced in Europe:
Cornus sericea ssp. sericea, Epilobium ciliatum ssp.
glandulosum, Pinus strobes, Prunus serotina and
Quercus rubra. Ellenberg has investigated E. ciliatum
ssp. glandulosum and P. serotina, and his results are
similar to those obtained here, with a difference of one
point and two points, respectively. Surprisingly,
Landolt (1977) gives a light level value of three in
a nine level scale for P. serotina, that can be substantial
since this species invades forest understories and
supresses regeneration of other species (Starfinger,
1991, 1997; Starfinger et al., 2003). However, this
behaviour may be simply a transitional stage. He also
investigates Q. rubra, and his ranking was identical to
ours and that of Gerhard Karrer (personal communication). However, C. sericea ssp. sericea seems to be
very shade tolerant in Europe (Landolt, 1977). No
European data were found for P. strobus.
Some species have a world-wide distributions and
are consequently found in the Northern hemisphere as
well as in the Southern hemisphere, such as
Cystopteris fragilis, Deschampsia flexuosa, Dryopteris carthusiana and Equisetum arvense (Rousseau,
1974). For these species, expert responses and
205
published data are similar to the European data. In
the case of D. flexuosa, we used no published data,
Rameau et al. (1989) who indicated a rank of midtolerant to intolerant, which is consistent with our
ranking. Interestingly, all of these species are midtolerant and are found generally at the edge of forest
paths. In the case of D. flexuosa Rameau et al. (1989)
indicated a rank of mid-tolerant to intolerant and a
wide range of different habitats such as forests of oak,
beech, pine, alpine meadows or moors, which is
consistent with our ranking. However, in Central
Europe this species seems to be more shade tolerant
and the corresponding Ellenberg’s value is 6. As well
as D. flexuosa, D. carthusiana has a wide range of
habitats from pine forests and deciduous forests, to
moors in Europe (Rameau et al., 1989). And as in
Europe these species also covered a wide range of
habitats in North America.
Other co-occuring species are either world-wide in
distribution or they are circumboreal species, as is the
case for most of the bryophytes and some of the
vascular species (e.g. Linnaea borealis). It is possible
that some are invasive species, but during the last 30
years the new intruders in North America originate
mostly from Asia and have mostly become established
along coasts and rivers, and not in forested areas
(Claudi et al., 2002).
3.3. Examples of ranking
In many cases the general rule failed to give a
consistent index, but we tried to capitalize on all of the
available data. This task was done by studying each
species case by case. As stated before for Fagus
grandifolia, we obtained an answer outside of the
range which drove the standard deviation away from
our selection criteria. Raw results for experts were 3, 3
and 7, and for published data they were 1, 1 and 2. X̄
are respectively 4.3 and 1.3 with s equal to 2.3 and 0.6,
and since these values do not match, the overall s
(2.23) is still too high. In this case we chose to
eliminate the outlier, and an index of 2 was assigned.
Concerning the choice between our results and
Ellenberg’s, two different cases appear. The first
one is when our result is within two points of
Ellenberg’s, the second occurs when the difference is
> 2. The first case can be illustrated by the results for
Equisetum hyemale. The raw data were 7, 5, 4 and 9
206
L. Humbert et al. / Ecological Indicators 7 (2007) 195–207
for the expert opinion, which gives a mean response of
6.3. This can be contrasted with one published datum
with a value of 3 and with Ellenberg’s, value of 5. In
this case, our result is near Ellenberg’s but as
mentioned earlier Ellenberg used a nine point scale
level whereas we used a five point scale, which must
then be expanded to nine for our results. Consequently,
in cases of contrasts we favoured the more precise
Ellenberg index. However, in the second case, our
results are prefered and thus indicate a difference
between the continents.
we acknowledge that the ecological preference of a
species can vary within its geographical range. As
stated before, the ‘‘ecological existence’’ was evaluated and not the ‘‘ecological potential’’ (Ellenberg,
1996; Whittaker et al., 1973) of each species, the
former reflecting the ability of a species to generally
persist at a given light level. If the light conditions
change, the species may survive under stress for quite
a long time. Consequently, this index should be used
with caution when attempting to characterize light
conditions using understory species as indicators.
3.4. Robustness and adaptability
Acknowledgements
The procedure presented here has been applied to
reduce or level out subjective interpersonal differences, but also to address smaller interspecific
differences due to genetics or other geographical
differences in ecological behaviour. The diversity of
information that is integrated, experts’ opinions as
well as published data, make this index robust and
widely applicable. This is the main difference with the
Ellenberg approach (which is based primarily on
experts’ opinions and which has led to much criticism
(Dierschke, 1994). The approach by indicator values
has been extensively discussed (see Diekmann (2003)
for a review), but despite criticism it is stated that ‘‘the
beauty of the system lies in its generality and
robustness’’ (Ewald, 2003). Moreover, it is possible
to calibrate the values obtained for other parts of North
America. Such a calibration has been made on
Ellenberg’s Central Europe indices for Britain (Hill
et al., 1999, 2000), Sweden (Diekmann, 1995;
Diekmann and Falkengren-Grerup, 1998), the Netherlands (Schaffers and Sykora, 2000) and Denmark
(Lawesson and Mark, 2000). The methods they used
have improved Ellenberg’s values, and this is
supported by the good correlation among all of these
studies (Diekmann, 2003).
4. Conclusion
Our goal was to develop a shade tolerance index for
understory plant species in northeastern North
America as was done by Ellenberg et al. (1992) in
Europe. An index was developed that will be
consistent, robust and widely applicable. However,
We gratefully acknowledge the collaboration of
Miroslav Grandtner, Brian Harvey, Gerhard Karrer,
Roger Larivière, Zoran Majcen and Pierre Martineau.
Thanks to two anonymous reviewers and to Timothy
Work for there helpful comments and suggestions. We
also thank the webmasters of the Ellenberg indices
database website, as well as of all the other websites
cited.
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