This study measured and compared the leaf thickness of four Salix taxa from the Athabasca sand dunes in northern Saskatchewan, Canada to their widespread progenitors. Leaf thickness was measured using light microscopy. Results showed leaf thickness varied among species and between each derivative-progenitor pair, with the two amphistomatic taxa from Yakow Lake dunes, S. turnorii and S. planifolia subsp. tyrrellii, having significantly thicker leaves than their widespread progenitors. A relationship was found between amphistomatic leaves and greater leaf thickness among the Salix taxa.

1. NOTE / NOTE
Leaf thickness of Salix spp. (Salicaceae) from the
Athabasca sand dunes of northern Saskatchewan,
Canada
R.L. Cooper, J.V. Ware, and D.D. Cass
Abstract: Leaf thicknesses of Salix taxa (Salix brachycarpa Nutt. var. psammophila Raup, Salix planifolia Pursh subsp.
tyrrellii (Raup) Argus, Salix silicicola Raup, and Salix turnorii Raup) from the Athabasca sand dunes in northern Sas-
katchewan, Canada, were evaluated and compared with those of their respective widespread progenitors (S. brachycarpa
Nutt. var. brachycarpa, S. planifolia Pursh subsp. planifolia, Salix alaxensis (Anders.), and Salix eriocephala Michx.
var. famelica (C. R. Ball) Dorn). Leaf thickness was measured using standard light microscopy, and results were com-
pared with the occurrence of amphistomaty in these Salix species. Leaf thickness values varied among the species and
differed significantly within each derivative–progenitor Salix pair. The two amphistomatic taxa from Yakow Lake
dunes, S. turnorii and S. planifolia subsp. tyrrellii, had significantly thicker leaves (337.65 ± 5.99 µm and 226.00 ±
5.22 µm, respectively) than their widespread progenitors, as well as the thickest leaves overall. The data comparison in-
dicates a relationship between amphistomaty and leaf thickness among the Salix taxa, as thicker leaves tend to be
amphistomatic.
Key words: amphistomaty, Athabasca sand dunes, leaf thickness, Salix, willow.
Résumé : Les auteurs ont évalué l’épaisseur de la feuille chez les taxons de Salix (Salix brachycarpa Nutt. var. psam-
mophila Raup, Salix planifolia Pursh subsp. tyrrellii (Raup) Argus, Salix silicicola Raup et Salix turnorii Raup) venant
sur les dunes de sable d’Athabasca dans le nord de la Saskatchewan, au Canada, et l’ont comparé avec celle de leurs
progéniteurs respectifs, largement répandus (S. brachycarpa Nutt. var. brachycarpa, S. planifolia Pursh subsp. planifo-
lia, Salix alexensis (Anders.) et Salix eriocephala Michx. var. famelica (C. R. Ball) Dorn). Ils ont mesuré l’épaisseur
de la feuille en utilisant la microscopie photonique standard, et ont comparé les résultats avec la présence d’amphis-
tomatie chez ces espèces de Salix. Les valeurs de l’épaisseur des feuilles varient selon les espèces et différent significa-
tivement pour chaque paire, dérivé–progéniteur, de Salix considérée. Les deux taxons amphistomatiques provenant des
dunes du lac Yakow, les S. turnorii et S. planifolia subsp. tyrrellii, montrent des feuilles significativement plus épaisses
(337,65 ± 5,99 µm et 226,00 ± 5,22 µm, respectivement) que leurs progéniteurs largement répandus, ainsi que les feuil-
les les plus épaisses parmi toutes celles étudiées. Une comparaison des données indique une relation entre
l’amphistomatie et l’épaisseur des feuilles chez les taxons der Salix, les feuilles plus épaisses tendant vers
l’amphistomatie.
Mots clés : amphistomatie, dunes de sable de l’Athabasca, épaisseur des feuilles, Salix, saule.
[Traduit par la Rédaction] Cooper et al. 1686
Introduction
Studies have critically examined leaf characters of the
Athabasca sand dune Salix species, including one taxonomic
(Argus and Steele 1979) and two structural investigations
(Cooper 2001; Cooper and Cass 2003). Plants endemic to
the Athabasca sand dunes, including the four willow shrubs,
were first described by Raup (1936). These rare taxa have
morphological features that distinguish them from their
respective widespread counterparts. For example, endemic
Salix species have been described as having thicker and
more highly cuticularized leaves than their progenitors (e.g.,
Can. J. Bot. 82: 1682–1686 (2004) doi: 10.1139/B04-132 © 2004 NRC Canada
1682
Received 10 June 2004. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 3 December 2004.
R.L. Cooper1,2
and J.V. Ware.3
Department of Biology, University of Tennessee at Martin, Martin, TN 38238, USA.
D.D. Cass. Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada.
1
Corresponding author (e-mail: Ranessa.Cooper@hillsdale.edu).
2
Present address: Biology Department, Hillsdale College, Hillsdale, MI 49242, USA.
3
Present address: Department of Animal Sciences, University of Kentucky, Lexington, KY 40546-0215, USA.

2. Argus and Steele 1979). Most recently, Cooper and Cass
(2003) quantified several leaf epidermis characters, includ-
ing cuticle thickness, of the four Athabasca sand dune Salix
species and compared them with those of the associated pu-
tative progenitors.
Recent observations indicated that two of the previously
described “endemic” Athabasca sand dune willows no lon-
ger have endemic status. Salix planifolia Pursh subsp. tyr-
rellii (Raup) Argus and Salix silicicola Raup have a small
geographic range outside of the Athabasca sand dunes
(G.W. Argus, personal communication) and will be called
“derivatives”. Salix brachycarpa Nutt. var. psammophila
Raup and Salix turnorii Raup maintain their endemic status
and are noted as such. All four of these willow species
(as listed in Table 1) will collectively be referred to as
“Athabasca sand dune willows”, as presented by Cooper and
Cass (2003). In addition, this study also recognizes that the
putative widespread progenitor of S. turnorii is most likely
Salix eriocephala Michx. var. famelica (C.R. Ball) Dorn,
(not Salix lutea Nutt. as cited in earlier studies), based on
Dorn’s (1995) taxonomic study of Salix section Cordatae
subsection Luteae.
Overall leaf thickness is one character that remains to be
quantified in the Athabasca sand dune willows for compari-
son with their putative widespread progenitors (S. brachy-
carpa Nutt. var. brachycarpa, S. planifolia Pursh subsp.
planifolia, Salix alaxensis (Anders.) Coville, and S. erioce-
phala var. famelica), and each is presented with its respec-
tive derivative (Table 1). The Athabasca sand dune willows
are confined primarily to dune interiors, but S. planifolia
subsp. tyrrellii also shares a localized distribution on the
Thomson Bay dune shore (Fig. 1) with its putative progeni-
tor, S. planifolia subsp. planifolia.
The primary objective of this study was to determine if
the Athabasca sand dune willows (from the inner dune and
(or) open sand habitat) have thicker leaves than their wide-
spread progenitors, as suggested by earlier field observations
(e.g., Raup and Argus 1982). A preliminary statistical com-
parison revealed differences in leaf thickness between speci-
mens of S. planifolia subsp. tyrrellii from the Yakow Lake
inner dunes and the Thomson Bay shore (Fig. 1). As a
result, three additional comparisons were made within the
S. planifolia group: (i) S. planifolia subsp. tyrrellii from both
the inner dune and shore habitats, (ii) S. planifolia subsp.
planifolia from Thomson Bay shore and widespread locali-
ties, and (iii) S. planifolia subsp. tyrrellii and its putative
progenitor from the Thomson Bay dune shore site.
The secondary objective of this study was to assess
whether a correlation exists between leaf thickness and
amphistomaty, the occurrence of stomata on both leaf sur-
faces. We extended the definition of amphistomaty to in-
clude that stomata must be distributed over the entire adaxial
and abaxial surfaces. Another authority has offered an addi-
tional amphistomaty-related term, “hemiamphistomaty”,
which describes an amphistomatic leaf whose adaxial
stomata distributions are confined to the leaf tip and (or)
midrib area (G.W. Argus, personal communication).
Previously, Cooper and Cass (2003) evaluated the occur-
rence of amphistomaty, while quantifying stomatal densities,
in the four derivative–progenitor Salix pairs using SEM.
Salix brachycarpa var. brachycarpa, S. planifolia subsp. tyr-
rellii (from both the inner dunes and Thomson Bay dune
shore), S. planifolia subsp. planifolia from the Thomson Bay
dune shore, and S. turnorii have amphistomatic leaves
(Argus and Steele 1979; Cooper and Cass 2003). Earlier
studies have indicated a correlation between leaf thickness
and amphistomaty in other taxa (e.g., Smith et al. 1998). The
potential relationship between leaf thickness and the pres-
ence of amphistomaty was examined among these Salix
taxa. Overall, this study will provide a better understanding
of structural adaptations of the Athabasca sand dune willows
to their open sand habitat.
Materials and methods
Twenty or more stem cuttings (1–3 years in age) of each
Athabasca sand dune Salix species were collected from
Yakow Lake inner dunes and the Thomson Bay dune shore
in northern Saskatchewan, Canada (Fig. 1), and those (1–
10 years in age) of widespread progenitors were collected
from various localities throughout Alberta, Canada (Cooper
2001). Stem cuttings of the progenitor, S. planifolia spp.
planifolia, were also collected from the Thomson Bay dune
shore (Cooper 2001). Leaves (approx. 1.0–1.5 cm × 0.5 cm)
were removed from all species’ cuttings at similar node posi-
tions and fixed in FAA (formalin – acetic acid – alcohol)
while in the field; in the lab, leaves were embedded in paraf-
fin and prepared for light microscopy (see Cooper and Cass
2003). Cross-sections (7–10 µm in thickness) were made at
the midsection of each leaf for a study of cuticle thickness
(Cooper and Cass 2003), and leaf thickness measurements
were obtained from these earlier preparations for the current
investigation.
Leaf cross-sections were examined using a Swift M3200
compound light microscope at 100× magnification. Only
those sections that were complete and intact were examined,
and several leaves for each Salix species were measured (Ta-
ble 1). A thickness measurement, from epidermis to epider-
mis, was made immediately adjacent to each side of the leaf
midrib, and these two values were averaged to obtain overall
thickness per leaf. Average leaf thickness and SE were
calculated per species. Data sets were analyzed statistically
© 2004 NRC Canada
Cooper et al. 1683
Leaf thickness (µm)
Taxon N Mean ± SE
S. brachycarpa var. psammophila (D) 58 173.19±4.69a
S. brachycarpa var. brachycarpa* (P) 64 193.44±3.79b
S. planifolia subsp. tyrrellii* (D) 67 226.00±5.22a
S. planifolia subsp. planifolia (P) 75 115.29±4.80b
S. silicicola (D) 76 145.67±3.33a
S. alaxensis (P) 23 189.13±6.58b
S. turnorii* (D) 69 337.65±5.99a
S. eriocephala var. famelica (P) 66 215.53±5.60b
Note: D, derivative; P, progenitor; N, number of leaves. Different let-
ters after leaf thickness means indicate a significant difference within
derivative–progenitor Salix pairs (p < 0.001 for all comparisons).
*Denotes amphistomaty (see Cooper and Cass 2003).
Table 1. Leaf thickness of the Athabasca sand dune Salix species
(from the inner dunes) and their widespread putative progenitors.

3. using t tests within derivative–progenitor Salix pairs. Addi-
tional t tests were used to compare data sets for the S. plan-
ifolia group as outlined earlier.
Results
Leaf thickness data varied among all Salix taxa in this
study (Table 1). Salix brachycarpa var. psammophila had
significantly thinner leaves than those of its progenitor,
S. brachycarpa var. brachycarpa (p < 0.001; Table 1). Salix
planifolia subsp. tyrrellii from the inner dune habitat had
significantly thicker leaves than those of its widespread pro-
genitor, S. planifolia subsp. planifolia (p < 0.001; Table 1).
Leaves of S. silicicola were significantly thinner than those
of its progenitor, and S. turnorii had significantly thicker
leaves than those of its progenitor (p < 0.001 for both com-
parisons; Table 1). Salix turnorii had the thickest leaves of
all of the Salix specimens evaluated in this study (Table 1).
Leaf thickness of S. planifolia subsp. planifolia from the
Thomson Bay dune shore was significantly greater than that
of non-dune specimens and was similar to that of its deriva-
tive from Thomson Bay (p < 0.001 and p > 0.05, respec-
tively; Table 2). Overall, S. planifolia subsp. tyrrellii from
the Yakow lake dune had the thickest leaves of the
S. planifolia group (p < 0.001; Tables 1, 2). The widespread
progenitor, S. planifolia subsp. planifolia, had the thinnest
leaves of the S. planifolia group (p < 0.001; Tables 1, 2).
Amphistomaty is present in three of the four derivative–
progenitor Salix pairs (see Cooper and Cass 2003). One pro-
genitor (S. brachycarpa var. brachycarpa), one derivative
(S. planifolia subsp. tyrrellii), and one endemic (S. turnorii)
have amphistomatic leaves (Cooper and Cass 2003), and
these are noted (Tables 1, 2; refer to stomatal frequency data
in Table 3). The progenitor from the Thomson Bay dune
shore, S. planifolia subsp. planifolia, was amphistomatic,
while the widespread counterpart was not (Cooper and Cass
© 2004 NRC Canada
1684 Can. J. Bot. Vol. 82, 2004
Fig. 1. Location of the Athabasca sand dunes on the south shore of Lake Athabasca in northern Saskatchewan, Canada. Dunes are rep-
resented by stippled areas.
Leaf thickness (µm)
Taxon N Mean ± SE
S. planifolia subsp. tyrrellii* 67 226.00±5.22a
S. planifolia subsp. tyrrellii* (T-Bay) 36 160.42±5.23b
S. planifolia subsp. planifolia* (T-Bay) 58 167.42±3.38a
S. planifolia subsp. planifolia 75 115.29±4.80b
S. planifolia subsp. tyrrellii* (T-Bay) 36 160.42±5.23a
S. planifolia subsp. planifolia* (T-Bay) 58 167.42±3.38a
Note: N, number of leaves; T-Bay, Thomson Bay dune shore. Different
letters after leaf thickness means indicate a significant difference within
the Salix pair (p < 0.001 when significance noted).
*Denotes amphistomaty (see Cooper and Cass 2003).
Table 2. Leaf thickness comparisons within the Salix planifolia
group.

4. 2003; Table 2). Salix silicicola and its progenitor are not
amphistomatic (Cooper and Cass 2003).
Discussion
Leaf thickness
Leaf thickness was significantly greater in the derivative
Salix planifolia subsp. tyrrellii and the endemic S. turnorii,
as compared with that of the widespread putative progenitor
of each (Table 1); however, S. brachycarpa var. psam-
mophila and S. silicicola had significantly thinner leaves
than their respective progenitors (Table 1). Leaves of
S. planifolia subsp. tyrrellii and S. turnorii are characterized
by amphistomatic leaves, waxy cuticles, and few to no tri-
chomes, while the other two Athabasca sand dune willows
are tomentose (Cooper 2001; Cooper and Cass 2003). Coo-
per and Cass (2003) discussed that the dense trichome cov-
erings of S. brachycarpa var. psammophila and S. silicicola
were likely adaptive to the open sand habitat, and the present
study suggests that thicker leaves may be another adaptive
features for the amphistomatic Athabasca sand dune Salix
taxa.
Leaf anatomy of sun and shade leaves has been compara-
tively examined within species (e.g., Jackson 1967; Carpen-
ter and Smith 1981; Ashton and Berlyn 1994), and results
showed that sun leaves are generally thicker. Almost all
leaves of the Athabasca sand dune willows could be consid-
ered “sun leaves”, as the upright, shrub habit of these plants
enables most, if not all, leaves to be exposed to full sun. In a
study of Quercus, Ashton and Berlyn (1994) showed that
sun leaves were thicker and more cuticularized than shade
leaves, with thicker leaves having a higher water-use effi-
ciency and lower evapotranspiration under high light condi-
tions. However, two of the Athabasca sand dune derivatives
have amphistomatic leaves (Cooper and Cass 2003), and a
simulation study revealed that amphistomaty will likely have
a lower water-use efficiency when compared with hypost-
omaty (Foster and Smith 1986).
The endemic, S. brachycarpa var. psammophila, has rela-
tively thick leaves (173.19 ± 4.69 µm) compared with the
other willows in this study, although they were significantly
thinner than those of their putative progenitor (Table 1).
This endemic did have adaxial stomata distributions, but
they only occurred near the leaf apex (R.L. Cooper and
D.D. Cass, unpublished results). Thus, this taxon was not
considered to be amphistomatic by our definition, but
hemiamphistomatic instead (Cooper and Cass 2003).
Considerations for the Salix planifolia group
Salix planifolia subsp. tyrrellii from the Yakow Lake inner
dune habitat had significantly thicker leaves than its wide-
spread progenitor, S. planifolia subsp. planifolia (Table 1),
and leaf thickness for each species from the Thomson Bay
dune shore was similar (Table 2). Although more water is
available along the dune shore, willows on the inner dunes
are rooted in the water table (Raup and Argus 1982). Water
is not likely the critical variable in this particular compari-
son. The dune shore and inner dune habitats may differ
enough ecologically to influence leaf thickness variability
of S. planifolia subsp. tyrrellii and S. planifolia subsp.
planifolia.
Another consideration for this group is the possibility of
hybridization of these two subspecies at the Thomson Bay
shore site. These two willows shared similarities in vessel el-
ement characters (Cooper and Cass 2001) and leaf epidermis
features, including amphistomatic leaves (Cooper and Cass
2003). Further taxonomic studies, including a detailed ge-
netic analysis, would be useful to confirm the taxonomic
identities of individuals at the Thomson Bay dune shore site.
Amphistomaty correlations
Amphistomaty has been correlated with high light inten-
sity (Mott et al. 1982), and it has been described as being an
adaptation of plants growing in the Athabasca sand dunes
(Argus and Steele 1979; Cooper and Cass 2003). Mott and
Michaelson (1991) demonstrated that Ambrosia cordifolia
(Gray) Payne was able to adapt to high light intensities; after
high light treatment, new leaves were thicker and amphist-
omatic. Salix planifolia subsp. tyrrellii and S. turnorii seem
to respond similarly to the high light conditions of the open
sand habitat. Argus and Steele (1979) presented results from
a common garden study that suggested a genetic basis for
© 2004 NRC Canada
Cooper et al. 1685
Adaxial (no./mm2
) Abaxial (no./mm2
)
Taxon N Mean ± SD N Mean ± SD
S. brachycarpa var. psammophila (D) 12 38±37a 12 505±99a
S. brachycarpa var. brachycarpa (P) 5 130±22b 5 286±38b
S. planifolia subsp. tyrrellii (D) 24 126±36a 22 228±68a
S. planifolia subsp. planifolia* (P; T-Bay) 12 144±66a 12 299±92a
S. planifolia subsp. planifolia (P) 7 36±44b 7 610±142b
S. silicicola (D) 12 0±1a 8 581±135a
S. alaxensis (P) 5 11±12a 5 201±24b
S. turnorii (D) 11 127±43a 13 195±54a
S. eriocephala var. famelica (P) 5 44±27b 5 942±235b
Note: D, derivative; P, progenitor; T-Bay, Thomson Bay dune shore. Different letters after the means
indicate a significant difference within derivative–progenitor Salix pairs for adaxial and abaxial data sets
separately. Data reproduced from Cooper and Cass (2003).
Table 3. Stomatal frequencies of the Athabasca sand dune Salix species and their wide-
spread putative progenitors.

5. amphistomaty in S. planifolia subsp. tyrrelli, although we
recognize and even suggest that plasticity may also play a
role, as S. planifolia subsp. planifolia from Thomson Bay
has amphistomatic leaves.
Previously, Sundberg (1986) evaluated stomatal density
and length in 134 desert taxa at the Desert Botanical Garden
in Phoenix, Arizona, USA. He reported a common occur-
rence of amphistomaty amongst the xerophytes, but it was
more commonly found in succulent species than in decidu-
ous ones (Sundberg 1986). The Athabasca sand dune wil-
lows are not only deciduous, but they could be considered
mesophytic in the inner dune environment, as they are
rooted in the water table (Raup and Argus 1982). Reports of
amphistomatic leaves in northern willow taxa (Cooper 2001;
Cooper and Cass 2003) show that the occurrence of amphist-
omaty has a greater biogeographic range than previously
thought.
Parkhurst (1978) suggested that amphistomaty may be
adaptive in reducing internal CO2 diffusion rates in thicker
leaves. In a one-dimensional modeling study of CO2 diffu-
sion, the resistance to CO2 diffusion was determined mathe-
matically and was found to be less limiting to photosynthetic
rates in amphistomatic leaves when compared with hyposto-
matic leaves (Terashima et al. 2001). The presence of
stomata on adaxial leaf surfaces may aid in maximum con-
ductance of CO2 for photosynthesis (Peat and Fitter 1994),
and it is possible that leaf thickness and amphistomaty are
positively correlated with each other (Parkhurst 1978; Mott
et al. 1982).
Our data seem to support a relationship between leaf
thickness and amphistomaty, as the thicker-leaved Salix taxa
tended to be amphistomatic (Tables 1, 2). Preliminary analy-
ses comparing the two data sets suggest a slight negative
correlation between leaf thickness (Tables 1, 2) and stomatal
densities (Table 3) for amphistomatic Salix taxa (R.L. Coo-
per, unpublished data). However, it is important to note that
the leaf thickness data and stomatal density data were gener-
ated from different sets of leaves, and thus, these results can-
not be formally published. Moreover, the preliminary
analyses have provided a basis to further examine this rela-
tionship and its physiological implications for the Athabasca
sand dune willows.
Acknowledgements
We thank George Argus, Markus Thormann, and anony-
mous reviewers for reviewing earlier drafts of this manu-
script. We acknowledge the University of Tennessee at
Martin and Hillsdale College for providing laboratory and
computer facilities. Research was funded at the University of
Alberta by a Canadian Circumpolar Institute C/BAR grant
and a Karling graduate student research award to R.L.C., as
well as a Natural Sciences and Engineering Research Coun-
cil grant to D.D.C.
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