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FOLIA OECOLOGICA – vol. 49, no. 2 (2022), doi: 10.2478/foecol-2022-0020
Geometric Morphometrics use in the examination of subgenus
Quercus leaf shape variation in Algeria
LAPAPEZA, Université Batna 1, ISVSA, Batna, Algeria
Abstract
ABDELDJALIL, A., BEGHAMI, Y., 2022. Geometric Morphometrics use in the examination of subgenus Quercus leaf
shape variation in Algeria. Folia Oecologica, 49 (2): 175–181.
The latest fi ndings on the taxonomic review of Quercus faginea Lam. complex using ‘traditional morphometrics’,
demonstrating that the species is represented in Algeria by both Q. faginea and Q. canariensis Willd. Signifi cant
variations of the leaf form were also discernible among both species. In this study, the landmark-based geometric
morphometrics analysis was used to assess the shape variation of the leaves found on oak stands. 2,600 leaves
per 13 stands were collected and scanned, and then using Tps range and MorphoJ software, 11 landmarks—that
represent the leaf morphological features—were recorded on leaf images. Shape components and non-forms varia-
tions were obtained through a full Procrustes fi t followed by creating a leaf-superimposed confi guration. Principal
component analysis, canonical variate analysis, and discriminate analysis were used to statistically evaluate the leaf
shape variability. The results revealed no clear distinction between the two species based on leaf shape. Climate
change and environmental factors also appear to have possibly caused a divergent morphological evolution; a re-
duced leaf size with enduring indumentum—among other Q. faginea traits—could be an effi cient mean of adapting
to Mediterranean xeric conditions.
Keywords
adaptation traits, Q. canariensis Willd., Q. faginea Lam., landmarks, morphological evolution
Abdeldjalil Aissi*, Yassine Beghami
Introduction
The systematic classifi cation of taxa of the genus Quercus
(Fagaceae) is usually presented using morphological and
morpho-anatomical analyses of fl oral organs and leaves
(e.g., CAMUS, 1938), and micro-morphological analyses (e.g.,
TSCHAN and DENK, 2012). This “traditional” morphological
method (see DEAN et al., 2004) involves measuring the lin-
ear distances between different points to analyze the varia-
tions in shape within and among the populations under study,
thus conducting descriptive multivariate statistical analyses
(BLACKITH and REYMENT, 1971). However, the strong correla-
tion between linear distances and sample size (BOOKSTEIN,
1986) makes it diffi cult to distinguish between taxa (JENSEN,
1990; KREMER et al., 2002). This indicates that the linear
points do not precisely correspond to the geometry of the sub-
ject under study, and therefore a graphical representation of
the subject cannot be produced (DEAN et al., 2004).
To overcome these issues, new morphometric tech-
niques—now known as “Geometric Morphometrics (GM)”—
have been developed to study, quantitatively compare the
morphological variations between each species, and effec-
tively visualize the shape/form deformations, while maintain-
ing the complete geometric data of the subject (ROHLF and
MARCUS, 1993; KENDALL, 1989; BOOKSTEIN, 1996). Using a
combination of both previous and present morphometric tech-
niques (two recognized styles: landmark-based and outline)
will provide greater examination of the existing relationships
between different species and will lead to a better under-
standing of the morphological variations within and among
species, thus improving future taxonomic, phylogenetic, and
eco-physiological studies (VISCOSI et al., 2009a).
Bearing this in mind, studies on the white oaks of the
sub-genus Quercus show the signifi cance of these “revolu-
tionary” methods (ROHLF and MARCUS, 1993). Not only do
these studies highlight the substantial differences between
176
Fig. 1. Map of the studied stands (represented by Q. canariensis and Q. faginea) in Algeria.
Stands Abbreviation Rainfall (mm) Elevation (m) Bioclimate
Terni Trn 688 1,300–1,350 Cool sub-humid
Hafi r and Zarifet Hfr 600–750 1,100–1,300 Cool sub-humid
Balloul Bll 430 850 Cool semi-arid
Safalou Sfl 620 950–1,100 Cool sub-humid
Thniet el Hed Teh 630–870 1,300–1.600 Cool sub-humid
El hamdania Hmd 1,100–1,300 1,150–1,600 Cool humid
Errich Err 630 500–600 Cool sub-humid
Akfadou Akf 1,078–1,132 750–1,300 Cool humid
Babor Bbr 1,200–1,500 1,200–1,650 Cool humid
Hamza Hza 922 450-500 Mild Humid
Ghorra Gra 950 700–850 Cool humid
Machrouha Mch 625 850–1,000 Cool sub-humid
Chelia Chl 360–523 1,200–1,700 Cold semi-arid
Table 1. Study stands main ecological factors
the analyzed species, but also demonstrate the intermediate
morphological status of hybrid leaves (VISCOSI et al., 2009a;
2009b; VISCOSI et al., 2010; ALBARRÁN-LARA et al., 2010;
PEÑALOZA-RAMÍREZ et al., 2010). These studies were carried
out without considering qualitative traits, which have been re-
garded in some studies as necessary for interspecifi c distinc-
tion (BRUSCHI et al., 2000; KREMER et al., 2002).
In Algeria, the oak stands of the Quercus subgenus are
represented by the Quercus faginea Lam. Complex, compris-
ing of forms (species, subspecies and variety) that are diffi -
cult to distinguish and whose taxonomic history is extremely
complex (see AISSI et al., 2021). The results from the morpho-
logical and micromorphological study of this complex group
found in AISSI et al. (2021) reveal that the analyzed popula-
tions (13 stands spread out over the entire distribution area;
Fig. 1) belong to two species: Quercus canariensis Willd. and
Q. faginea Lam. (Fig. 1). The latter is represented by two of
its subspecies: faginea and broteroi. Thus, intermediate leaf
type and signifi cant form variation within and between the
two groups were discernible. Therefore, these quantitative
traits alone do not constitute a practical criterion that can distin-
guish between both species. However, qualitative traits related
to the indumentum type on the abaxial side of leaves seem to
be effective, i.e. deciduous for Q. canariensis and persistent for
Q. faginea. Furthermore, at the intraspecifi c scale, leaf margins,
namely toothed leaves differs faginea subspecies from broteroi,
characterized by lobed leaves (AISSI et al., 2021).
The purpose of this study is to apply landmark-based
geometric morphometrics to the systematics of the sub-genus
Quercus found in Algeria, examine the morphometric relation-
ship existing between Q. canariensis and Q. faginea, and fi nd
intermediate forms between these species.
Materials and methods
Sampling procedures
Throughout the entire distribution area of the two oak stands
(Fig. 1), 2,600 mature leaves were collected from 100 mature
177
Landmark Description
1 The start of the petiole
2 Beginning at the petiole, the midrib intersects with vein of the fi rst basal lobe (referred to landmark 1)
3 At the widest point of the leaf blade, the midrib meets the vein of the lobe (referred to landmark 8)
4 Immediately above the apex of the leaf blade, the midrib meets the vein of the fi rst lobe (referred to landmark 7)
5 The leaf blade’s apex
6 The sinus’s base is directly above the leaf blade’s apex.
7 The tip of the lobe just above the leaf blade’s apex.
8 At the widest point of the leaf blade, the tip of the lobe.
9 Just above the lobe of landmark 8, the base of the sinus
10 Starting from the petiole, the tip of the fi rst lobe
11 Petiole-blade junction
Table 2. Description of landmarks recorded on the right half of Q. canariensis and Q. faginea leaves (VISCOSI et al., 2009a)
Hfr Trn Bll Sfl Teh Hmd Err Akf Bbr Hza Gra Mch
Trn 0.04
Bll 0.09 0.07
Sfl 0.06 0.06 0.08
Teh 0.06 0.07 0.12 0.06
Hmd 0.03 0.04 0.08 0.05 0.05
Err 0.09 0.10 0.11 0.05 0.07 0.07
Akf 0.12 0.11 0.07 0.10 0.15 0.12 0.14
Bbr 0.10 0.09 0.04 0.08 0.12 0.09 0.10 0.05
Hza 0.08 0.07 0.08 0.05 0.07 0.06 0.07 0.09 0.06
Gra 0.09 0.07 0.06 0.06 0.10 0.07 0.08 0.08 0.04 0.05
Mch 0.15 0.14 0.11 0.13 0.16 0.14 0.15 0.07 0.09 0.11 0.09
Chl 0.05 0.03 0.07 0.06 0.08 0.04 0.10 0.10 0.08 0.06 0.06 0.12
Table 3. Procrustes distances within-group matrices from canonical variate analysis (CVA) of leaf shape of 13 stands of Q.
canariensis and Q. faginea (9 and 4 stands, respectively)
trees (20 leaves per tree) that were found on 13 stands (same
sample localities from the morphological and micromorpho-
logical study by AISSI et al., 2021) with different environmental
conditions (Table 1) (AISSI et al., 2021). The data revealed that
both leaf species exhibits dissimilar distributions (cf. Fig. 1). Q.
canariensis covers a large area and forms large stands stretch-
ing across the far eastern and central parts of Algeria (MAIRE,
1961; AISSI et al., 2021), with a smaller population found in
the far West along the Tlemcen Mountains (Hafi r and Zarifet
forests). Q. faginea appears in isolated stands alongside other
species in four separate locations. Aside from the close distri-
bution found in Tlemcen region, the two species stands do not
share the same biogeographical distribution (AISSI et al., 2021).
As per the prior source, the type of indumentum on the leaves
was used to identify the two species and appropriately allo-
cate the population samples, with Q. canariensis leaves hav-
ing a deciduous indumentum and Q. faginea leaves having a
persistent indumentum.
Further assortment of the leaves helped to eliminate
those bearing morphological abnormalities, thus obtaining
10 leavers per tree. The remaining leaves were scanned and
saved on a tps (.tps) fi le using tpsUtil software v1.67 (Tps
Software series). Using tpsDig2 v.2.26, 11 landmarks were
digitized (VISCOSI and CARDINI, 2012) (Table 2). For further
description of these landmarks, see VISCOSI et al. (2009a).
Before adopting these procedures, several combinations
were tested to determine the best represented morphometry
of the two analyzed species (VISCOSI et al., 2009a; 2009b
and further combinations). At the end of the digitization,
a fi le (.tps) was created containing all the geometric in-
formation (raw coordinates) of the leaves. An approxima-
tion of the Procrustes space was created by using tpsSmall
software v1.33. A full Procrustes fi t (DRYDEN and MARDIA,
1998) via MorphoJ software v1.06d (KLINGENBERG, 2011)
was achieved to eliminate any non-form variations and thus
identify shape components. Using Mahalanobis distance, a
fi nal check was made to detect and eliminate specimens that
were well beyond average or that contained any anomalies
(repetition and mispositioning of the landmarks) created
during digitization (Klingenberg and Monteiro, 2005).
Statistical analyses
With the use of MorphoJ software, a principal component anal-
ysis (PCA) was performed to inspect trends in the stand shape
and determine any variability between the two taxa and stands.
To resolve the issue with intra-tree morphological variability
(JENSEN, 1990), the leaves of each tree were further processed
to create a mean leaf confi guration (VISCOSI et al., 2009a). In
this new confi guration, the number of leaves was reduced to
130 (one leaf per tree). Based on this confi guration, a second
PCA was performed. In addition, canonical variate analysis
(CVA) was used to compare the two taxa and shape variations
of the leaves in the stands. Discriminate analysis (DA) through
cross-validation function was also used to test the signifi cant
differences of the leaf shapes between the two taxa.
178
Fig. 2. Principal component analysis (PCA) (axes 1 and 2) plot performed on all leaves, showing the leaf shape of 13 stands of
Q. canariensis and Q. faginea (9 and 4 stands, respectively), with 95% confi dence ellipses for stands means (a) and taxa means
(b). The conformation graphs (Wireframe Graph) show the morphological features of the leaves along both axes.
Fig. 3. Principal component analysis (PCA) (axes 1 and 2) plot performed based on the mean leaf confi guration (130 leaves),
showing the leaf shape of 13 stands of Q. canariensis and Q. faginea (9 and 4 stands, respectively), with 95% confi dence el-
lipses for stands means (a) and taxa means (b). The conformation graphs (Wireframe Graph) show the morphological features
of the leaves along both axes.
Results
Multivariate analysis
Figures 2 and 3 show, respectively, the results of the fi rst
two components of the PCA performed for each leaf, on both
stands and taxa levels (axes one and two) showing variations
of 36.60% and 28.95% for the fi rst PCA (a), and of 37.36%
and 28.42% for the second PCA (b), as well as the fi rst two
components of the PCA performed and based on the mean
leaf confi guration. Axes one and two showing a variation of
26.40% and 15.24% for the fi rst PCA, (a), and 46.16% and
25.33% for the second PCA (b). In all four diagrams, the dot
cluster trend shows strong correlations between the different
examined stands. In fact, the leaves of the stands pre-classi-
fi ed as Q. faginea completely overlap those of Q. canarien-
sis. This similarity is also indicated by conformation graphs
(Wireframe Graph) which show no morphological shape
differentiation among the different populations and species
(Fig. 2 and 3). Similarly, confi dence ellipses of the mean
179
Fig. 4. Discriminate analysis (DA) (a) and canonical variate analysis (CVA) (axes 1 and 2) (b) of the leaf shape of 13 stands
of Q. canariensis and Q. faginea (9 and 4 stands, respectively), with 95% confidence ellipses for stands means (b).
Fig. 4. Discriminate analysis (DA) (a) and canonical variate analysis (CVA) (axes 1 and 2) (b) of the leaf shape of 13 stands of
Q. canariensis and Q. faginea (9 and 4 stands, respectively), with 95% confi dence ellipses for stands means (b).
of each stand widely overlap and therefore do not provide
a suffi ciently clear distinction among and between the two
oaks (Fig. 2 and 3).
The DA between the means of the two oaks turned out
to be signifi cant (Fig. 4a, T2 = 143.70, p = > 0.0001). However,
a cross-validation test revealed that 68.58% of Q. canariensis
individuals and 67.78% of Q. faginea individuals were correct-
ly classifi ed. This indicates that unambiguously identifying a
given leaf (regardless of other morphological traits) seems un-
feasible. Moreover, the results of the CVA computed with Ma-
halanobis distance (sequential Benferroni signifi cance) demon-
strated insignifi cant inter-population differences (Table 3, Fig.
4a). The confi dence ellipses of the mean of each stand similarly
implies a scarce differentiation based on leaf shape that does
not allow for a clear distinction between Q. canariensis and Q.
faginea (Fig. 4b).
Discussion
The approximation of our data in the tangent space shows that
the gradient of the regression line is practically equal to one
(r2 = 0.999996 with a correlation of 1.000000). In previous
studies, several authors have stated that the distance between
the Procrustes and tangent space is generally small (ROHLF,
1999). Although the regression line for the data approxima-
tion is close to 1 (DEAN et al., 2004), checking the variation
between the two spaces is essential and ensures that the ap-
proximation of the tangent space can be used (VISCOSI and
CARDINI, 2012).
Contrary to previous morphometric studies, the afore-
mentioned results showed no clear morphological distinction
between the two analyzed species. It is important to note the
frequency in previous studies to compare the differences be-
tween different species of red oak in North America (JENSEN et
al., 1993), white oak in Europe (VISCOSI et al., 2009a; 2009b;
VISCOSI et al., 2010; VISCOSI 2015), several types of oak in
Mexico (ALBARRÁN-LARA et al., 2010; PEÑALOZA-RAMÍREZ
et al., 2010), two sympatric oak found in China (LIU et al.,
2018), and four sympatric Mediterranean oaks and hybrids in
Algeria (AKLI et al., 2022). However, the results of the anal-
yses highlighted a strong correlation between the two species
and drew attention to a strong morphological similarity of leaf
shape between Q. faginea and Q. canariensis. This would ex-
plain why botanists previously encountered diffi culties when
designating the taxonomy of Q. faginea Lam. complex (cf.
AISSI et al., 2021). Our results thus confl ict with those ob-
tained by VISCOSI et al. (2009b), showing that the implemen-
tation of the mean leaf confi guration can provide a solution
for the lack of signifi cant differences within and between the
analyzed species.
By acknowledging the effi cient combination of land-
marks that were chosen, the morphological variability be-
tween the stands of the two species is mainly due to a variation
in the size of their leaves. In fact, these stands show a gradual
reduction in leaf size, which is a characteristic trend from east
to west and from north to south. Environmental and climatic
variations are most likely the main causes of this phenomenon
(TRABUT, 1892; AISSI et al., 2021). Drought is also commonly
known to cause a reduction in the leaf size of several plants
(SCHIMPER, 1903), and it would be no different for the leaves of
the Quercus species. The results from CORCUERA et al. (2002)
found that oaks in the Mediterranean have leaves with a small-
er leaf surface area compared to those found in nemoral and
temperate zones. In addition, intense solar radiation and high
temperatures appears to affect the leaf size, by producing either
small-sized or widely-lobed leaves (MCDONALD et al., 2003).
However, MAHEBI BIJARPASI et al. (2019) noted that Fagus ori-
entalis Lipksy morphological and physiological traits could be
affected differently along elevation gradients, refl ecting a spe-
cifi c adaptation to local conditions. A comparative study be-
tween three oak species (Q. robur L., Q. pyrenaica Willd. and
Q. faginea) revealed a correlation between reduced leaf size
and shape. This included lobed margins on one side and leaf
temperature on the other, thus suggesting that these morpholog-
ical traits contribute to a lower leaf temperature (GIL-PELEGRÍN
et al., 2017). The reduction in leaf size is associated with a
decrease in surface area, which should increase the specifi c
hydraulic conductivity and make the species more resistant
to Mediterranean climate conditions (PEGUERO-PINA et al.,
180
2016; GIL-PELEGRÍN et al., 2017).
The qualitative characteristics of the leaves are
known for their numerous functions in several species of
the genus Quercus (TSCHAN and DENK, 2012; GIL-PELEGRÍN
et al., 2017), especially the indumentum. This includes in-
terspecifi c separation (BRUSCHI et al., 2000; KREMER et al.,
2002) and the role of the indumentum on the abaxial side of
the leaf in xeric environmental conditions (HE et al., 2014).
The results found in GIL-PELEGRÍN et al. (2017) demonstrat-
ed that the pubescence of the abaxial side of the leaves of the
Quercus genus is related to the climatic conditions of their hab-
itats, especially during drought. This signifi es that pubescent
leaves characterize the species that thrive in extremely dry con-
ditions. This study also found that evergreen oaks from arid and
Mediterranean areas tend to have the thickest pubescence on
the abaxial side of their leaves. HARDIN in (1979) made a link
between environmental conditions and leaf pubescence, noting
that the density of leaf pubescence increases at the intraspecifi c
level as a result of drought. In fact, the reduced size and dura-
bility of the leaf indumentum of Q. faginea, among other traits,
may be a mean of adapting themselves to xeric environmental
conditions (AISSI et al., 2021). In contrast, TSCHAN and DENK
(2012) suggest that the deciduous appearance of the indumen-
tum of Q. canariensis leaves is likely related to the fact that this
species has developed under mesic conditions. Larger leaves
with deciduous indumentum appear to be linked to the ecolog-
ical conditions of the stands in Algeria, especially the higher
average rainfall and preferential growth of Q. canariensis on
more developed soils and on sandstone, schist and siliceous
substrates. On the contrary, Q. faginea thrives within specifi c
habitat parameters and thus generally grows in less developed
soils (AISSI et al., 2021).
Considering the results, Q. faginea and Q. canarien-
sis appears to share most of the same biometric character-
istics, excluding their size. The climatic and environmental
changes in Algeria may have caused a divergent morpholog-
ical evolution. Furthermore, the genetic diversity studied at
sequenced microsatellites of 11 Algerian Q. faginea and Q.
canariensis stands exhibited a continuous pattern of genetic
differentiation between the two main genetic clusters repre-
senting the two species. This pattern was also found with the
eight specifi c clusters that have been identifi ed, and therefore
does not unambiguously defi ne any limits between the two
species (LEPAIS et al., 2022). The intermediate and genetic
characteristics of the populations—especially the smallest
and most isolated (LEPAIS et al., 2022)—and the morpholog-
ical similarities among stands and species may be supported
by maintaining ancestral polymorphism or ancient hybrid-
ization. These makes a signifi cant contribution to the overall
genetic diversity of Q. faginea (s.l), thus creating an urgency
to take action and preserve its vulnerable status, and more
specifi cally that of Q. faginea (s.s) (cf. LEPAIS et al., 2022).
Conclusion
The landmark-based geometric morphometrics analysis of the
stands reveal no clear distinction between the two species in
terms of form. The analysis thus demonstrated a strong mor-
phological similarity between the different stands examined.
These fi ndings strongly support that the morphological evolu-
tion of both species could be attributed to climatic change and
stand conditions. Q. faginea is likely the result of an adapta-
tion to the xeric conditions of the Mediterranean climate. Fur-
ther genetic analyses is ongoing to study the potential links
between genetics and size variation of the leaves found on
stands across species distribution ranges and to better under-
stand their evolutionary history.
Acknowledgements
The authors would like to acknowledge S. Zekak, R. Ferroud-
ji, H. Cherir, and H. Benaissa for their fi eldwork assistance,
and would also like to thank James Cairns, Olivier Lepais and
Tabatha Melendez for their input, comments, and review.
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Received January 10, 2022
Accepted June 5, 2022
