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Phytolith types and type-frequencies in
subalpine-alpine plant species of the
European Alps
Article in Review of Palaeobotany and Palynology · January 2004
DOI: 10.1016/j.revpalbo.2003.11.002 · Source: OAI
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Review of Palaeobotany and Palynology 129 (2004) 39 – 65
www.elsevier.com/locate/revpalbo
Phytolith types and type-frequencies in subalpine–alpine plant
species of the European Alps
Adriana L. Carnelli a,*, Jean-Paul Theurillat b, M. Madella c
a
Institut of Plant Science, University of Bern, Altenbergrain 21, CH-3013 Bern, Switzerland
Centre Alpien de Phytogéographie, Fondation J.-M. Aubert, CH-1938 Champex, Switzerland and Laboratoire de Biogéographie,
Département de Botanique et de Biologie végétale, University of Geneva, 1 ch. de l’Impératrice, CH-1292 Chambésy, Switzerland
c
The Cambridge Phytolith Project, The McDonald Institute for Archeological Research,
University of Cambridge, Downing Street, Cambridge CB2 3ER, UK
b
Received 28 May 2002; accepted 11 November 2003
Abstract
Biogenic silica extracted from 21 species commonly occurring in subalpine and alpine plant communities in the central
Swiss Alps were examined using light and SEM microscopes; 19 species being screened here for the first time. An inventory of
phytolith types is provided and type-frequencies are assessed. Light microscope photographs and SEM micrographs provided
illustrations of the types described. The monocotyledons analysed belonged to the genera Calamagrostis, Festuca, Nardus, Poa
and Carex. Monocotyledons yielded mainly types of epidermal origin (short cells, rods, cork cells, silicified stomata and
trichomes).
Dicotyledons analysed were from five genera of the Ericaceae family (Arctostaphylos, Calluna, Loiseleuria, Rhododendron,
Vaccinium) and from one genus of the Betulaceae (Alnus). In dicotyledons, silicified epidermal jigsaw cells, stomata complexes
and vessels were recovered.
Conifer species of the genera Abies, Juniperus, Picea, Pinus and Larix were studied. Distinctive conifer cells were mainly
silicified endodermids and transfusion tissues. Phytolith taxonomic diagnostic potential was tested by cluster analysis and
principal component analysis (PCA). It was shown that grass and sedge species could be easily differentiated on the basis of
phytolith types. In general, Ericaceae and conifers could also be distinguished on the basis of phytoliths; however, some species
yielding mainly redundant types were not unequivocally identifiable.
The aim of the present work is to provide a framework for phytolith-based plaeoecological studies at the treeline in the
European Alps.
D 2004 Elsevier B.V. All rights reserved.
Keywords: biogenic silica; conifers; Cyperaceae; Ericaceae; Gramineae; phytolith
1. Introduction
* Corresponding author. Tel.: +41-31-6314923.
E-mail address: adriana.carnelli@ips.unibe.ch (A.L. Carnelli).
0034-6667/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.revpalbo.2003.11.002
Opal-A is deposited in the tissues of many vascular plants. These deposits can be cast from the
cells, from the infilling of the cell lumen or by
40
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
silicification of the cell walls (their shape resembling
the outline of the original cell). The silicification can
also be found as intercellular deposits in the interstitial spaces (Carnelli et al., 2001). The term phytoliths is commonly employed to describe silicified
cells, either isolated or in tissues. The initial interest
in phytolith type was focused on their diagnostic
potential in plant taxonomy and phytoliths were
observed in situ (Metcalfe, 1960). More recently,
attention has been given to their applications in
archeological and palaeoecological studies. Phytoliths released in soils, in sediments or in archeological sites, can be preserved and, eventually, analysed
for palaeoecological reconstructions.
The morphology of phytoliths occurring in several
crop species has been more extensively described
because of its interest for archeological studies
(Blackman, 1969; Whang et al., 1998; Rapp and
Mulholland, 1992; Ball et al., 1999). In general,
grasses were the plants usually chosen for study
(Twiss et al., 1969; Blackman, 1971; Palmer, 1976),
and only a few non-grass species naturally occurring
in a temperate climate have been investigated. Extensive works for American and Japanese species are
available (Geis, 1973; Wilding and Drees, 1973; Klein
and Geis, 1978; Kondo and Peason, 1981; Bozarth,
1993). For a more comprehensive list of phytolith
studies in non-grass plants, see also Mulholland et al.
(1992).
Any attempt to interpret soil-borne phytolith
assemblages should be based on a documented inventory relevant for the study area (Bozarth, 1993;
Piperno, 1988). Data on species of the European
Alps are not available, and we are aware of only one
study of a mountain ecosystem, in the Caucasus
(Blinnikov, 1994). This paper is the third of a series
describing the scanning of a set of 21 species
occurring in the subalpine – alpine belts of the European Alps. In this paper, the morphology of phytoliths is described. The content of biogenic silica
has been already assessed from the same plant
material (Carnelli et al., 2001) and the diagnostic
potential of aluminium presence in biogenic opal
has been tested (Carnelli et al., 2002). The aim of
the present work is to supply an inventory of
phytoliths of dominant alpine species on siliceous
bedrock to provide a framework for phytolith-based
palaeoecological studies at the treeline in the Euro-
pean Alps. Therefore, light microscopy and scanning
electron micrographs are supplied for phytolith identification. In addition, we used cluster analysis and
principal components analysis (PCA) to test the
hypothesis that taxonomic groups can be distinguished on the basis of phytolith types. The physiological role of silicon in vascular plants is still an
open subject and ecological conditions may play a
strong role in determining the degree of silicification
of plant individuals and populations, therefore the
present data should be validated with a larger data
set of plant populations from different ecological
settings.
2. Methods
2.1. Laboratory procedures and samples
Phytoliths present in the above-ground tissues of
21 species commonly occurring on siliceous bedrocks in the subalpine and alpine vegetation belts
in the Central Alps were analysed (Table 1). Plant
material was collected in Val d’Arpette and at
Furka Pass (Central Alps, Valais region, CH). A
composite sample was collected from the aboveground tissues of several randomly selected plants
from each species, from sites with rather homogeneous environmental conditions. Site locations,
sampling and extraction procedures have been described elsewhere (Carnelli et al., 2001). The leaves
and branches of woody species were analysed
separately. Among the plants previously analysed
for biogenic silica (Carnelli et al., 2001), species
with very low biogenic silica content and rare
identifiable phytoliths were not taken into account
[i.e., leaf material from Alchemilla pentaphylla L.
(Rosaceae), Geum montanum L. (Rosaceae), Leontodon helveticus Merat (Asteraceae), Salix herbacea
Vill. (Salicaceae), Veronica bellidioides L. (Scrophulariaceae), and leaf and wood from Empetrum
nigrum subsp. hermaphroditum (Hagerup) Böcher
(Ericaceae)].
Silica bodies were observed and identified using
a petrographic microscope equipped with phase
contrast optic and polarised illumination at a magnification of 504 and 800 (oil immersion).
Permanent microscope slides were mounted in
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Table 1
List of species and plant tissues from which biogenic silica was extracted (L = leaves, C = culms, N = needles, W = woody branches).
Plant samples were collected in Central Swiss Alps, if not specified
in Val d’Arpette, otherwise:
Species
Plant
tissue
Sampling
sites altitude
(m a.s.l.)
MONOCOTYLEDONS
Gramineae
Calamagrostis villosa (Chaix.) Gmelin.
Festuca halleri All.
Festuca melanopsis Foggi, Rossi and
Signori [ = F. puccinellii auct.]
Festuca scabriculmis (Hackel.) Richter
Nardus stricta L.
Poa alpina L.a
L, C
L, C
L, C
1900
2730
2090
L, C
L
L
2300
2300
2795
Cyperaceae
Carex curvula All.
Carex sempervirens Vill.
L, C
L, C
2470
2300
Ericaceae
Arctostaphylos uva-ursi Spreng.
Calluna vulgaris L.
Loiseleuria procumbens Desf.
Rhododendron ferrugineum Linn.
Vaccinium myrtillus L.
Vaccinium vitis-idaea L.
L,
L,
L,
L,
L,
L,
W
W
W
W
W
W
2420
2420
2370
2050
2180
1980
Betulaceae
Alnus viridis (Chaix) DC
L, W
2000
DICOTYLEDONS
CONIFERS
Pinaceae
Abies alba Miller
Juniperus nana Willd.
Larix decidua Miller
Picea abies (L.) Karsten
Pinus cembra L.
Pinus mugo Turra
a
N,
N
N,
N,
N,
N,
W
W
W
W
W
2050
1930
2050
2050
2050
2050
Furka Pass.
EUKITT (mounting medium with refractive index
of 1.5 at 20 jC). A count of 500 identifiable
phytoliths per slide was carried out whenever possible. Few large fragments of silicified tissues
(skeletons) were extracted from heavy silicified
monocotyledons (e.g., Calamagrostis villosa): they
were not considered in the count, this should not
affect the representativeness of the samples since
they were present in negligible quantities. For very
poor samples, a standardised scanning of 3 h was
41
performed. The number of phytoliths counted was
on average 300. Non-idioblastic silica particles, such
as intercellular deposits or fragments, were not
included in the count. Whenever possible the types
were described quoting the botanical terminology
for the plant cells from which they originated (Fahn,
1974), or employing the terminology commonly
used in phytoliths studies, and referring to their
shape. In this study, the phytoliths are identified
by an acronym and an outline sketch (Table 2, Fig.
1). Since several trichome types are present, they
are identified, for simplicity, as ‘‘TRI’’ followed by
a number (Fig. 1).
Light microscope photographs were taken using
Kodak T MAX 400 asa professional film.
A fraction of the same extract used for light
microscopy was spread with the help of a paint-brush
on double sided tape, mounted on aluminium stub,
coated with gold and examined in a JEOL JSM 6400
scanning electron microscope operating at 15 kV, at a
working distance of 15 mm and live time of 50 s.
SEM photographs were taken with Agfa Pan APX
100 asa professional film.
2.2. Cluster analysis and principal components
analysis
Cluster analysis and PCA analysis were employed
to test if taxonomically related species could be
identified and grouped on the basis of the presence
and frequency of types (STATISTICA 4.5 F for
Windows). In woody species, the percentages of
types were counted separately in leaf and wood
tissues: for the analysis, wood and leaf type percentages were added together and the new sum normalised to 100%.
For cluster analysis (Fig. 2), Ward’s method was
applied (where the criterion of choice of linkage is the
least increase in the sum of squared deviations from
cluster means), and the algorithm of the Euclidean
distance was used on normalised data (i.e. chord
distance). However, in cluster analysis, the ordination
can be biased by the arbitrary choice of data transformation and linkage algorithms. To test the strength of
the ordination obtained, additional tests were also run
with square root transformed data and presence/absence data. For comparison, PCA was also performed
(Fig. 3) on square root transformed data. Finally, to
42
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Table 2
Morphotype acronyms and description, anatomical origin (if known) and available literature
Acronym
Description
Occurrence in plant taxa
BLOCK RIDGED
BULL
CALL L CELL
Block with a ridge in the middle, endoderm cells
Bulliform cells (Parry and Smithson, 1958b)
Long cells with sinuous edge
CONE 1, CONE 2, CONE 3,
CONE M
P. abies, P. mugo
M.
C. vulgaris, V. myrtillus,
V. vitis-idaea, R. ferrugineum
C. curvula, C. sempervirens
RECT PITTED
Cones smooth or with sculpturing, distinctive
of sedges (Ollendorf et al., 1987; Metcalfe, 1971).
Isolated or in skeletons of 2, 3 or more
Cork cells
M.
Jigsaw epidermal cells
D, C
Epidermal long cells
M, D, C
Epidermal long cells with grainy surface
D, C
Irregular waved blocky, mesophyll cells
L. decidua
Mesophyll cells
L. decidua
Mesophyll cells
M, D, C
Undulated hypodermal cells (Klein and Geis, 1978; Bozarth, 1993) P. abies
Mesophyll palysade cells
A. viridis
Microhairs
D, C
Irregular rectangular with few pits
M, D, C
Polyhedral cells
M, D, C
A. alba, P. abies, P. cembra,
Blocky polyhedrons transfusion cells often pitted
(Klein and Geis, 1978; Bozarth, 1993)
P. mugo
Rectangular with many pits in rows
D, C
Rods:
ROD BR
ROD CW
ROD FW
ROD LS
ROD LTS
ROD MS
Branched Rod cells (Parry and Smithson, 1958a)
Rods long coarse wavy
Rods long smooth fine wavy
Rods long smooth (‘‘long cells’’ in Metcalfe, 1960)
Rods long thin smooth
Rods medium smooth
N. stricta
M, P. abies
M, D
M
M, D, C
M, D, C
SPHE R
SPHE S
STO CYP; STO ERIC 1; STO ERIC 2;
STO GRAM; STO CON; STO DIC
TRACH
Spherical rugose
Spherical smooth
Stomata complexes, respectively: Cyperaceae,
Ericaceae, Gramineae, conifer and, dicotyledon type
Tracheids
D, C
M, D, C
Trichomas
TRI 1/18
THREAD
Trichomas, see Fig. 1 for variants
Monocellular thread-like, non-segmented trichomas
See Tables 3 – 5
M, C, D
Trapezoids (short cell)
TRA
TRA CR
TRA L
TRA LOB
TRA LTH
TRA O
TRA SB
TRA V
VES
VES SP
WAVY
Trapezoids (‘‘short cells’’ in Metcalfe, 1960)
Crenated based trapezoids
Long trapezoids
Lobated based trapezoids
Long thin trapezoids
Ornamented trapezoids
Sinuous based trapezoids
Narrow, chimney-like trapezoids
Vessels
Vessels with spiral thickening
Ridge-like invaginations of the mesophyll
Gramineae
Gramineae
Gramineae
P. alpina, F. melanopsis
Gramineae
Gramineae
Gramineae
Gramineae
A. viridis
M, D, C
L. decidua, P. abies
CORK
JGS
L CELL
L CELL GRAINY
LARIX BLOCKY W
LARIX SPIKY CELL
MESO
UND
PALISADE
PAPILLAE
PLAT PERF
POLY
POLY CONIF
D, C
Occurrence in plants from this data set is summarised as: M (monocotyledons), D (dicotyledons) and C (conifers). For diagnostic morphotypes,
the species or genus are listed. Outline drawings are in Fig. 1.
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Fig. 1. Outline sketches of phytolith morphotypes.
43
44
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Fig. 2. Dendrogram resulted from the clustering analysis (Ward’s method, Euclidean distance, normalized data). The species are clustered on the
basis of phytolith frequency. For the analysis, leaf and woody phytoliths were added. Two clusters are individuated: monocotyledons and
dicotyledons with conifers. The latter consists of two clusters: Ericaceae and conifers with Alnus viridis.
verify the robustness of the ordination, both cluster
analysis and principal component analysis were run
after adding similar types from all categories [respectively, all trapezoids (TRA), all rod-like cells (ROD),
all Cyperaceae conical types (CONE), all trichomes
(TRI)].
3. Type descriptions and frequencies
Line drawings of the types are displayed in Fig. 1
and an explanation of the acronyms in the text is given
in Table 2. Percentage presence of the types and SEM
micrographs and light microscope photos are given in
Table 3 and Plates I– III for monocotyledons, in Table
4 and Plates IV – V for dicotyledons, and in Table 5
and Plates VI – IX for conifers.
Descriptions of species types are divided into three
sections: monocotyledons, dicotyledons (i.e., mainly
Ericaceae) and conifers.
3.1. Monocotyledons (Table 3, Plates I –III)
The species examined belong to Gramineae and
Cyperaceae.
Bulliform cells (BULL) occurred regularly in
monocotyledons but were observed in very low
percentages in the population here examined. Rods
were common in grasses but not unique to this
family, excepting ROD BR that was unique to
Nardus stricta (Plate I, 5 –6). Trapezoidal types were
unique to Gramineae (TRA, TRA L, TRA LOB,
TRA O, TRA SB, TRA V, TRA CR; e.g., Plate I,
2 – 4); other taxonomically significant types were
some trichome types (TRI 2, TRI 5, TRI 7; e.g.,
Plate II, 1 and 11 and stomata complexes (STO GRA;
Plate I, 10).
Unique to Cyperaceae types were cones (CONE 1,
CONE 2, etc.; Plate III, 13 and 16), stomata complexes (STO CYP; Plate III, 13) and the trichome type
TRI 18.
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
45
Fig. 3. Scatter plot resulted from the PCA. Species are grouped on the basis of phytolith frequency. For the analysis, leaf and woody phytoliths
percentage were added. Two groups are individuated: monocotyledons and conifers with dicotyledons; Carex species are isolated. Factor 1
explains 45% of variability of the data; factor 2 explains 17%. PCA loadings are given in Table 6. Variables V11, V12 and V15 are grouped with
V9; variables V14, V16, V17, V20 and V21 are grouped with V10 and V19. Symbols: V1: Calamagrostis villosa, V2: Festuca melanopsis, V3:
Festuca halleri, V4: Festuca scabriculmis, V5: Nardus stricta, V6: Poa alpina, V7: Carex sempervirens, V8: Care curvula, V9: Calluna
vulgaris, V10: Vaccinium myrtillus, V11: Rhododendron ferrugineum, V12: Larix decidua, V13: Pinus mugo, V14: Pinus cembra, V15: Picea
excelsa, V16: Abies alba, V17: Arctostaphylos uva-ursi, V18: Vaccinium vitis-idaea, V19: Juniperus nana, V20: Alnus viridis, V21: Loiseleuria
procumbens.
3.2. Gramineae (Plates I– II)
In Gramineae, epidermal cells, mesophyll cells,
stomata complexes and trichomes were silicified.
3.2.1. Epidermal cells
Elements of silicified epidermis were common in
above-ground tissues of grasses (Plates I, 8, 13 – 14
and III, 3 –7). The most common types were ‘‘short
cells’’ (Metcalfe, 1960), in the species examined here
their general outline was trapezoidal (TRA), but
several variants occurred (Fig. 1). The length of
trapezoids was about 15 A for short trapezoids and
about 30 A for long trapezoids, and width was about
10 A. Trapezoids (TRA) diagnostic of grasses, were
idiomorphic and well silicified (Plates I, 2 –4, 7, 11
and II, 2, 4 –6, 13, 18). Short cells were among the
first silica bodies to be described (Metcalfe, 1960),
they were also defined as ‘‘hats’’ and ‘‘wavy – edged
coastal rods’’ (Parry and Smithson, 1964), and as
‘‘nodular coastal rods’’ (Geis, 1978). Among the
species examined here, trapezoids with a lobed base
(TRA LOB; Plate I, 2 – 3) were dominant in Poa
alpina (51%). Sinuous-based trapezoids (TRA SB)
were common in Festuca melanopsis (Plate II, 18),
Calamagrostis villosa and P. alpina (Plate I, 11),
respectively, 50.4%, 27.4% and 23.9%.
Rod-like long cells (ROD) were sub-epidermal
columnar or rectangular cells. They were recovered
isolated or in skeletons in all grass species, with
percentages from 0.2% to 11%. Rods with narrow
terminations were present (e.g., Plates I, 11 and II,
10). Rods were erratically filled with silica; the
silicification may be complete or restricted to the
cell walls. Rods varied in length (20 – 50 A), in
width (5– 10 A) and in the extent to which the
margins were sinuous (e.g., smooth, fine wavy,
coarse wavy; see Fig. 1). Silicified projections
may occur (Plate II, 8 – 9) (Hayward and Parry,
1975). Occasionally, rods presented concave ends
46
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Table 3
Monocotyledon species: morphotypes counting as percentages and total number counted
Calamagrostis
villosa
Morphotypes unique of monocotyledons
BULL
1.2
CORK
11.4
STO GRAM
4.9
TRA
14
TRI 2
1.4
TRA LTH
0.6
ROD LS
4.7
TRA SB
27.4
TRA O
–
TRA L
–
TRI 7
5.5
TRI 5
0.4
TRA LOB
–
TRA V
–
CONE 1
–
CONE 2
–
CONE 3
–
CONE M
–
STO CYP
–
TRA CR
2.4
ROD BR
–
TRI 18
–
Festuca
melanopsis
0.4
0.2
4
7.8
0.2
2
1.4
50.4
0.2
4.2
2.4
0.2
0.5
–
–
–
–
–
–
–
–
–
Morphotypes occurring in monocotyledons and dicotyledons
ROD FW
–
1.4
TRI 1
0.4
2.2
TRI 3
6.7
0.7
TRI 4
–
0.2
TRI 16
–
4.7
TRI 15
0.2
0.9
TRI 6
–
0.9
TRI 17
–
–
TRI 12
–
–
TRI 8
–
0.2
TRI 13
–
–
TRI 9
–
–
TRI 10
–
–
Morphotypes occurring in monocotyledons and conifers
ROD CW
5.3
7.4
Festuca
halleri
Festuca
scabriculmis
Nardus
stricta
0.4
16.9
29.4
18.1
0.4
0.2
–
–
2.8
–
–
–
–
–
–
–
–
2.2
–
–
–
–
–
–
–
–
2.1
1.9
–
3.6
0.2
0.2
4.4
–
–
–
0.2
2.5
0.2
–
–
–
–
0.4
–
–
0.2
–
–
–
–
0.6
0.6
0.4
–
–
–
–
–
–
–
–
0.7
0.2
0.2
0.2
0.7
0.2
–
0.2
0.6
9.8
–
–
–
–
–
–
–
–
–
–
–
4
–
0.9
6.6
0.9
3.8
–
Carex
sempervirens
0.2
17.2
0.2
46.9
0.2
0.9
0.2
2.1
1.9
3.5
1.2
–
–
9.1
0.2
–
–
–
0.4
33.1
0.4
31.6
0.6
–
Poa
alpina
3.4
0.2
23.9
–
0.2
–
–
51
–
–
–
–
–
–
–
–
–
0.9
1.7
0.6
–
0.4
–
0.2
–
0.2
0.4
–
–
–
–
–
–
–
–
–
–
–
–
1.5
–
–
–
–
–
–
–
–
–
–
–
–
–
15.5
36.9
13.5
14.9
1.6
–
–
–
8.9
25.9
2.7
9.7
13.9
–
–
3.6
–
1.2
–
–
0.5
–
–
4.6
–
–
0.4
0.2
–
–
–
–
9.0
9.5
11.0
1.3
7.0
0.2
–
–
–
–
–
–
–
–
3.2
0.4
0.6
–
–
–
1.5
1.3
0.8
0.2
–
–
–
–
–
0.2
2.8
1.4
–
Morphotypes occurring in monocotyledons, dicotyledons and conifers
ROD MS
0.8
0.2
1.9
L CELL
2.2
6.9
0.2
POLY
–
–
3.7
ROD LTS
9.1
0.2
0.2
MESO
1.4
0.4
0.7
THREAD
–
–
0.2
PLAT PERF
–
–
–
SPHE R
–
–
–
VES SP
–
–
–
Tot. %
100
100
100
N. counted
507
552
431
100
497
0.2
–
–
100
471
100
469
Carex
curvula
0.2
–
–
0.2
–
100
502
0.4
0.4
0.8
0.8
–
–
–
0.8
–
0.8
0.4
1.9
–
5
24.7
–
–
–
–
–
0.4
100
259
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
47
Plate I. Gramineae. SEM micrographs of silicified tissues from plant leaves; *light microscope photographs. Scale bar = 10 Am. (1) Poa alpina,
trichoma.* (2) P. alpina, TRA LOB.* (3) P. alpina, TRA, TRA LOB.* (4) P. alpina, TRA V, VESS.* (5) Nardus stricta, ROD BR. (6) N. stricta,
ROD BR.* (7) N. stricta, TRA.* (8) N. stricta, skeleton ROD CW, STO GRAM.* (9) N. stricta, TRI 2.* (10) Calamagrostis villosa, STO
GRAM.* (11) C. villosa, TRA CW, ROD MS.* (12) C. villosa, EL CELL.* (13) C. villosa, ROD FW. (14) C. villosa, ROD CW. (15) C. villosa,
ROD FW.
48
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Table 4
Dicotyledon species: morphotypes counting as percentages and total number counted; L from leaves, W from wood
Arctostaphylos
uva-ursi
Calluna
vulgaris
L
L
W
Morphotypes unique of dicotyledons
STO ERIC 1
8
15.7
STO ERIC 2
–
–
CALL L CELL
–
–
TRI 11
–
–
TRI 14
–
–
STO DIC
–
–
PALISADE
–
–
VES
–
–
W
27.4
–
–
–
1.1
–
–
–
Loiseleuria
procumbens
Vaccinium
myrtillus
Vaccinium
vitis-idaea
Rhododendron
ferrugineum
Alnus
viridis
L
L
L
L
L
–
–
12.3
–
–
–
–
–
W
W
W
W
0.8
–
–
1.3
–
–
–
–
0.4
–
–
–
–
–
–
–
–
32.7
2.8
–
0.2
–
–
–
–
1.6
–
–
–
–
–
–
–
28.8
4.7
0.3
–
–
–
–
–
17.6
–
–
–
–
–
–
2.9
–
12.8
–
–
–
–
–
23.5
–
–
–
–
–
–
–
–
–
–
–
–
3.9
2.4
0.3
0.3
0.8
1.1
0.3
0.3
0.3
–
–
0.8
0.3
–
0.5
–
–
–
–
–
–
–
–
–
–
–
–
–
–
0.2
0.4
0.2
1.2
0.4
–
0.4
–
0.6
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
4.1
0.9
0.3
0.3
0.3
0.3
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
0.7
2.2
0.5
3.9
2.9
1.2
2
1.2
3.2
–
1
–
0.5
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
56.2
–
–
–
–
–
1.3
–
–
–
–
0.4
28.8
–
–
0.2
–
–
–
–
–
–
–
–
45.6
–
–
3.8
–
–
28.6
–
–
–
–
–
8.6
–
–
1.2
–
–
20.6
–
–
–
–
–
3.6
8.0
3.3
1.2
–
–
Morphotypes occurring in monocotyledons, dicotyledons and conifers
POLY
85.3
69.4
9.5
82.6
35
97.9
VES SP
0.8
–
–
0.3
1.6
–
MESO
–
–
0.7
–
0.5
–
PLAT PERF
–
–
–
0.3
–
–
TREAD
–
–
26.7
–
–
–
L CELL
–
–
–
–
–
–
ROD MS
–
–
–
–
–
–
SPHE R
–
–
–
–
–
–
ROD LTS
0.3
–
–
–
–
–
Tot. %
100
100
100
100
100
100
N. counted
400
121
453
310
377
235
29
1.8
–
–
–
0.8
0.2
0.2
–
100
507
96.7
–
–
1.7
–
–
–
–
–
100
120
6.6
1.6
0.3
0.3
–
–
–
–
–
100
320
52.7
–
–
1.1
–
–
–
–
–
100
91
33.2
20.6
1.2
–
–
–
–
–
–
100
407
55.9
–
–
–
–
–
–
–
–
100
34
72.3
–
2.4
–
–
1.5
0.3
0.3
–
100
336
Morphotypes occurring in monocotyledons and dicotyledons
TRI 9
0.5
–
–
–
TRI 8
1.3
–
–
–
TRI 16
–
–
0.2
–
TRI 4
–
–
–
–
TRI 3
–
–
–
–
TRI 1
–
–
0.9
–
TRI 12
0.3
–
2.6
–
TRI 13
–
–
–
–
TRI 15
–
–
1.5
–
ROD FW
0.3
–
–
–
TRI 6
0.3
–
–
–
TRI 10
0.3
–
–
–
TRI 17
–
–
8.2
–
Morphotypes occurring
JGS
L CELL GRAINY
PAPILLAE
SPHE S
RECT PITTED
TRACH
in dicotyledons and conifers
2.8
14.0
21.2
–
–
–
–
–
–
0.3
–
–
–
0.8
–
–
–
–
4.5
–
–
–
–
–
in proximity of stomata (Plate I, 11). Branched rods
(ROD BR; Plate I, 5– 6; about 50 A length) were
unique to Nardus stricta (Parry and Smithson,
1958a), a small percentage (4%) was extracted either
intact or fragmented. Cork cells are epidermal cells,
crescent- or U-shaped (CORK; Plate II, 17; about
10 A). They were completely silicified and ubiquitous in the different grass species (0.2 – 33.1%); in
49
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Table 5
Conifer species: morphotypes counting as percentages and total number counted; N from needles, W from wood
Abies alba
Larix decidua
Picea abies
Pinus cembra
Pinus mugo
Juniperus nana
N
N
N
N
N
N
Morphotypes unique of conifers
POLY CONIF
34.4
STO CON
5.4
WAVY
–
BLOCK RIDGED
–
UND
–
LARIX SPIKY CELL
–
LARIX BLOCKY W
–
W
0.4
–
–
–
–
–
–
W
W
W
–
–
–
–
–
–
–
12.3
9.2
12.6
18.0
33
–
–
–
–
–
–
–
–
–
0.2
9.1
–
–
–
–
–
–
–
–
–
–
–
–
71.1
–
–
1.0
–
–
–
0.8
–
–
–
–
–
–
–
11.9
–
–
–
–
–
Morphotypes occurring in monocotyledons and conifers
ROD CW
–
–
–
–
0.8
–
–
–
–
–
–
Morphotypes occurring in dicotyledons and conifers
RECT PITTED
1.1
0.4
–
L CELL GRAINY
3.2
–
–
TRACH
11.8
–
4.8
PAPILLAE
6.5
–
–
SPHE S
1.1
–
–
JGS
–
–
1.6
–
0.8
–
2.7
–
–
1.1
–
–
–
–
–
1.4
33.5
4.4
3.0
–
–
0.3
–
–
–
–
–
–
18.6
3.2
–
0.2
–
0.4
–
–
–
–
–
–
–
–
–
–
–
dicotyledons and conifers
10.6
91.7
8.4
–
4.6
–
6.8
–
2.3
7.7
–
–
1.3
–
–
2.6
–
–
–
–
–
–
–
–
–
–
–
100
100
100
311
108
261
94.9
0.6
–
–
–
–
–
–
–
100
178
47.6
0.8
–
–
–
–
–
–
–
100
496
99.7
–
–
–
–
–
–
–
–
100
320
4.4
–
0.2
–
–
0.4
0.4
0.2
0.2
100
495
98.8
–
–
–
–
–
–
–
–
100
250
Morphotypes occurring in monocotyledons,
POLY
36.6
99.2
PLAT PERF
–
–
THREAD
–
–
L CELL
–
–
MESO
–
–
ROD MS
–
–
SPHE R
–
–
ROD LTS
–
–
VES SP
–
–
Tot. %
100
100
N. counted
93
256
–
0.3
20.9
–
–
31.8
11.6
W
–
–
–
–
–
–
Festuca halleri cork cells had crenate outline due to
tiny projections.
Fan-shaped bulliform cells (BULL) occurred in the
adaxial surface of the leaf blade, they were silicified
mainly in old leaves (Parry and Smithson, 1958b);
BULL were rare in the species examined (0.2 – 1.2%).
3.2.2. Mesophyll cells
Sponge-like mesophyll cells (MESO) were only
occasionally silicified (0.2 – 1.4%).
3.2.3. Stomata
Silicified stomata complexes (STO GRAM) were
present in all grasses as epidermal fragments (silica
87.2
–
–
–
–
–
–
–
–
100
109
skeletons) as well as isolated elements (25 A). They
were characterised by the presence of guard-cells
having their lumen more constricted in the middle.
Stomata in Calamagrostis villosa (4.9%; Plate I, 10)
and Festuca melanopsis (4%; Plate II, 15) had subsidiary cells with spiky edges. In Festuca scabriculmis stomata constituted 29.4% of the total phytoliths
extracted (Plate II, 14).
3.2.4. Trichomes
Trichomes having their lumen partially or totally
infilled with silica were commonly recovered in
grasses (Plates I, 1, 9 and II, 1, 11– 12). Tree trichome
types were unique to grass species in this data set (TRI
50
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
2: Calamagrostis villosa, 1.4%; Festuca melanopsis,
0.2%; Festuca halleri, 0.4%; Nardus stricta, 0.6%;
TRI 5: C. villosa, 0.4%; F. melanopsis, 0.2%; and TRI
7: C. villosa, 5.5%; F. melanopsis, 2.4%; F. halleri,
1.5%) (Table 3).
3.3. Cyperaceae (Plate III)
In Cyperaceae, silicified cells were mainly epidermal cells and stomata complexes.
3.3.1. Epidermal cells
The majority of phytoliths identified in sedges
were conical (CONE; Plate III, 2– 5, 7– 8, 10– 13).
CONE types mainly occurred in the epidermal cells
that overlay the sclerenchyma occurring with the
vascular bundles of the veins (Metcalfe, 1971;
Ollendorf, 1992). From the top, a CONE appeared
as a circle within a larger one, positioned on a
pentagonal or hexagonal cell. From the side it was
conical. They were recovered as single elements
(CONE 1) or arranged in groups of two (CONE 2)
or three (CONE 3) or more (CONE m) on one
epidermal cell. These cells were counted as single
elements, no matter the number of cones that they
yielded (Table 3). Cells with several cones were very
common in Carex sempervirens (65.3%). Carex
sempervirens and Carex curvula presented both
CONEs with psilate (smooth) surfaces (Plate III,
11), and with sculpturing (Plate III, 4, 13). The
presence of surface ornamentation consisted of small
subsidiary cones (satellites), scattered or clustered on
the apex or periphery of the CONE. The ornamentation did not seem to be diagnostic at the species
level in the population observed; however, more
investigations are needed. In C. curvula, CONE
types were about 5 Am in diameter. C. sempervirens
tissues were more extensively silicified, and CONEs
were generally bigger (about 10 Am) with more
marked ornamentation. From the side, the psilate
CONE could be confused with a conical trichome
(TRI 9). CONEs were largely dominant in sedges;
51
the different types totalling 47.2% for C. curvula and
80.8% for C. sempervirens.
Other epidermal cells were present in small percentages (ROD FW, ROD CW; Plate III, 12). The sum
of ROD types was 10.8% and 3.1%, for Carex
curvula and Carex sempervirens, respectively. Rodshaped phytoliths were reported for various species of
Cyperaceae (Ollendorf et al., 1987).
3.3.2. Stomata
In Cyperaceae, paracytic silicified stomata complexes (STO CYP; Plate III, 6, 14, 17) had clearly
defined elongated dome-shaped subsidiary cells lying
parallel to the stomata pore. Silicified stomata (measuring about 45 A in length) were present in both
species, although more frequently in Carex curvula
(13.9%), than in Carex sempervirens (1.6%).
3.3.3. Other cells
Rare silicified mesophyll cells (MESO) (about 10
A) were present only in Carex sempervirens (0.2%);
trichomes were also rare, in all up to 4%). Polyhedrons (POLY; Plate III, 2, 5) represented up to 24.7%
of the phytolith production observed in Carex curvula, and were similar to the polyhedrons found in
conifers, although they were generally smaller (about
30 A) and never yield bordered pits.
3.4. Dicotyledons (Table 4, Plates IV– V)
The dicotyledons described here belong to the
Ericaceae family, with the exception of Alnus viridis
(Betulaceae). Studies of wild dicotyledons are scanty
(Bozarth, 1992; Runge, 1996; Runge and Runge,
1997), and in particular the phytolith type of Ericaceae has never been investigated. Phytoliths extracted
from leaves and wood were examined separately.
Stomata complexes were characteristic in the Ericaceae (STO ERIC 1, STO ERIC 2; (Plates IV, 5 –6, 14,
17 and V, 5, 10). TRI 11 was present only in
Loiseleuria procumbens and Vaccinium vitis-idaea
(1.3% and 0.3% respectively) and TRI 14 occurred
Plate II. Gramineae. SEM micrographs of silicified tissues from plant leaves; *light microscope photographs. Scale bar = 10 Am. (1) Festuca
halleri, TRI 7. (2) F. halleri, ROD LS, TRA SB. (3) F. halleri, ROD CW, STO GRAM. (4) F. halleri, ROD FW, TRA. (5) F. halleri, ROD CW.
TRA. (6) F. halleri, ROD CW, TRA.* (7) F. halleri, skeleton. (8) F. halleri, ROD FW with spiny projections.* (9) F. halleri, ROD FW. (10) F.
halleri, ROD FW. (11) F. halleri, TRI 4. (12) Festuca scabriculmis, TRI 2.* (13) F. scabriculmis, STO GRAM.* (14) F. scabriculmis, STO
GRAM. (15) Festuca melanopsis, STO GRAM. (16) F. melanopsis, ROD CW.* (17) F. melanopsis, CORK. (18) F. melanopsis, TRA SB.*
52
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
only in Calluna vulgaris and Vaccinium myrtillus
(1.1% and 0.2%, respectively). The types most commonly occurring in leaves and wood were jigsaw
epidermal cells (JGS; Plates IV, 13 and V, 7) these
types are very common in dicotyledons in general.
Silicified vessels and vessels with spiral thickening
(VES, VES SP; Plates IV, 12, 15 –16 and V, 2) were
also often recovered from leaf tissues, mainly in Rhododendron ferrugineum leaves (VESS SP, 20.6%),
these types are not distinctive.
3.4.1. Epidermal cells
Epidermal cells presented a wide morphometric
variability. Two main groups were recognisable: cells
with a sinuous outline (JGS and CALL L CELL) and
cells with a polygonal outline (POLY). Silicified
jigsaw epidermal cells were frequent (JGS; Plates
IV, 13 and V, 7) and typical of dicotyledon cells. This
type is described as anticlinal by Piperno (1988). Cells
with a similar shape, however, occurred in a very low
percentage in other groups (e.g., conifers; Plate VII,
10). They were usually recovered as silica skeletons.
The highest percentages were recorded in Loiseleuria
procumbens and Vaccinium vitis-idaea leaves (56.2%
and 45.6%).
Elongated and sinuous cells, probably of epidermal origin (CALL L CELL; Plate V, 8) were present
in Calluna vulgaris wood (12.3%; Plate IV, 8),
Vaccinium myrtillus leaves (2.8%), Vaccinium vitisidaea leaves (4.7%) and Rhododendron ferrugineum
leaves (12.8%). Polyhedral cells (POLY) do not
present distinctive morphological features; they are
formed by fragments of silicified tissues of various
histological origin. POLY are common in leaves
(6.6 – 85.3%) and form most of the phytoliths in
wood (from 52.7% to 97.9%). These types were
dominant in Alnus viridis leaves and wood (55.9%
and 72.3%).
3.4.2. Mesophyll cells
Mesophyll cells (MESO) were only occasionally
silicified in Ericaceae leaves (0.5 –0.7%; Plates IV, 2,
53
9 and V, 6, 12). In Alnus viridis, palisade mesophyll
cells (PALISADE; 2.4%) were present.
3.4.3. Stomata
Each stomata type (STO ERIC 1, STO ERIC 2;
(Plates IV, 5 –6, 14, 17 and V, 4 –5, 10) may constitute
up to 32.7% of phytoliths in leaves of the Ericaceae,
and added together up to 65.4% in the leaves of
Vaccinium myrtillus. They were also present in woody
branches of most of the Ericaceae examined (0.4 –
23.5%). Calluna vulgaris and Rhododendron ferrugineum had similar stomata complexes consisting of
many neighbouring cells which had no distinctive
shape (STO ERIC 1) (this type also occurred in other
Ericaceae species). The stomata complex may be
covered by silicified cuticle. In R. ferrugineum, stomata were generally bigger (30 Am) than in C.
vulgaris (20 Am). In the genus Vaccinium, the stomata
apparatus consisted of a pair of guard cells with single
subsidiary cells on each side placed parallel to the
pore. In Vaccinium myrtillus, the stomatal edge had a
double polar T-piece (STO ERIC 2; Plate IV, 14).
3.4.4. Trichomes
In the species examined, several trichome types
(TRI, Table 4) were regularly present in leaves although each usually showed low frequency (less than
2%). Only in Calluna vulgaris (total sum 14.5%) and
Rhododendron ferrugineum (total sum 19.3%) trichomes were more abundant, while in the remaining
heaths trichomes were less common (total from 2.7%
to 6.5%). Trichomes typical of Ericaceae were TRI 11
and TRI 14. In C. vulgaris, surface hairs were simple
uniseriate silicified hairs (THREAD, 26.7%; Plate
V(11)). Arrow tip-like hairs (TRI 14) were present in
this species (1.1%) and in Vaccinium myrtillus (0.2%).
TRI 11 was present with low frequency in Loiseleuria
procumbens (1.3%) and Vaccinium vitis-idaea (0.3%).
3.4.5. Vascular elements
Vascular elements (VES, VES SP) were present in
Ericaceae leaves (Plate IV, 3, 4, 15, 16) and wood
Plate III. Cyperaceae. SEM micrographs of silicified tissues from plant leaves; *light microscope photographs. Scale bar = 10 Am. (1) Carex
curvula, ROD CW. (2) C. curvula, CONE M. (3) C. curvula, CONE M. (4) C. curvula, CONE 2. (5) C. curvula, ROD LS. (6) C. curvula, STO
CYP. (7) C. curvula, CONE M, side view.* (8) C. curvula, CONE M, top view.* (9) C. curvula, STO CYP.* (10) Carex sempervirens, ROD
CW. (11) C. sempervirens, CONE 2, CONE 3. (12) C. sempervirens, ROD FW. (13) C. sempervirens, CONE 2. (14) C. sempervirens, STO
CYP. (15) C. sempervirens, CONE 3.* (16) C. sempervirens, CONE 2.* (17) C. sempervirens, STO CYP.*
54
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
(Plate IV, 7– 8, 11– 12). VES SP were frequent in
Rhododendron ferrugineum leaves (20.6%), but seldom in the leaves of the other Ericaceae studied (up to
1.8%).
3.4.6. Wood
The most common types occurring in wood of
Ericaceae were not idioblastic. Indeed, POLY were
always more than 50%; other common types were
JGS (in Arctostaphylos uva-ursi, 14%; Vaccinium
vitis-idaea, 28.6%; Rhododendron ferrugineum,
20.6%) and stomata (STO) (A. uva-ursi, 15.7%; V.
vitis-idaea, 17.6%; R. ferrugineum, 23.5%).
3.5. Conifers (Table 5, Plates VI –IX)
Needle and wood phytoliths were examined separately. The types most frequently recovered were not
idioblastic; they had a polygonal outline and were of
variable size (POLY; e.g., Plate VI, 10 – 12). It must
be stressed that this type although not distinctive of
conifers was, however, the dominant type produced.
Indeed, POLY were common in needles (4.4 – 87.2%)
and dominant in wood (91.7 – 99.7%). In woody
tissues, distinctive types were rare; nevertheless, the
abundance of POLY types is itself characteristic of
wood. Distinctive types in conifers were recovered
mainly from needles. Silicified transfusion cells
(POLY CONIF) were common in Pinus mugo needles (71.1%; Plate VI, 1– 2, 5, 9) and present in
needles of Abies alba, Picea abies and Pinus cembra
(34.4%, 12.3% and 0.2%, respectively). Silicified
endodermal cells (BLOCK RIDGED) occurring in
needles were diagnostic of P. abies (18%) and P.
mugo (1%). Larix decidua could be distinguished on
the basis of mesophyll tissues (LARIX BLOCKY W,
11.6%; Plate IX, 4 –6 and LARIX SPIKY CELL,
31.8%; Plate IX, 11). WAVY type (Plate IX, 1– 2)
was present only in needles of P. abies and L.
decidua (12.6% and 20.9%). Conifer stomata (STO
CON; Plate VII, 6) were present with low frequency
55
(0.3 – 11.9%) in all species excepting P. mugo. UND
type (hypodermal cells) was typical of P. abies (33%
in needles).
3.5.1. Epidermal cells
In conifers, cells in the inter-stomata files were
elongated with smooth edges, similar to grass epidermal cells, albeit generally bigger in size. These cells,
once fragmented, were likely to produce fragments
with a polygonal outline (POLY) (Plate IX, 7 –9).
Juniperus nana needles contained abundant POLY
(Plate VIII, 7 – 11), probably in part also of epidermal
origin. In this species, POLY had a grainy aspect
when observed under a light microscope and, when
observed at SEM, the surface appeared covered by
many small spheres that could be either attached to the
external surface or loose (Plate VIII, 6, 11).
3.5.2. Hypodermal cells
Picea abies needles yielded characteristic hypodermal cells, with rectangular outline and with mineralised cell walls undulated on the long side and straight
on the short side (UND; Plate VII, 3, 7– 9), finger-like
projections may also occur.
3.5.3. Mesophyll cells
Distinctive types were present in Larix decidua
and Picea abies (WAVY; Plate IX, 1 –2). These types
were probably ridge-like invaginations of the mesophyll, which have been described elsewhere as ‘‘suspended bridge-like’’ (Blinnikov, pers. comm.) or
‘‘square netting-like fragments’’ (Rovner, 1971).
WAVY type was also recovered in Pinus sylvestris
(Klein and Geis, 1978), Pinus banksiana and Picea
glauca (Bozarth, 1993). LARIX BLOCKY W types
probably also originated from silicified mesophyll
cells (Plate IX, 4– 6). These cells were completely
silicified; they had an undulating outline, grainy
aspect and evident three-dimensional relief. LARIX
SPIKY cells may be silicified mesophyll cells (31.8%
in L. decidua needles).
Plate IV. Ericaceae. SEM micrographs of silicified tissues from plant leaves (L = leaves, W = wood); *light microscope photographs. Scale
bar = 10 Am. (1) Rhododendron ferrugineum (L), unknown. (2) R. ferrugineum (L), MESO, VESS SP. (3) R. ferrugineum (L), TRACH. (4) R.
ferrugineum (L), VESS SP. (5) R. ferrugineum (L), STO ERIC 1.* (6) R. ferrugineum (L), STO ERIC 1. (7) R. ferrugineum (W), POLY. (8) R.
ferrugineum (W), POLY. (9) R. ferrugineum (W), MESO. (10) Vaccinium vitis-idaea (W), POLY. (11) V. vitis-idaea (W), POLY. (12) V. vitisidaea (W), VESS.* (13) Vaccinium myrtillus (L), JGS.* (14) V. myrtillus (L), STO ERIC 2.* (15) V. myrtillus (L), VESS,* (16) Arctostaphylos
uva-ursi (L), VESS. (17) A. uva-ursi (L), unknown. (18) A. uva-ursi (L), unknown.
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Plate V. Ericaceae. SEM micrographs of silicified tissues from plant leaves (L = leaves, W = wood); *light microscope photographs. Scale bar = 10
Am. (1) Loiseleuria procumbens (L.), RECT PITTED. (2) L. procumbens (L), VESS. (3) L. procumbens (L), TRACH. (4) Calluna vulgaris (L),
STO ERIC 1, MESO. (5) C. vulgaris (L), STO ERIC 1. (6) C. vulgaris (L), MESO. (7) C. vulgaris (L), JGS. (8) C. vulgaris (W), CALL L CELL.
(9) C. vulgaris (W), papillated ROD. (10) C. vulgaris (L), STO ERIC 1.* (11) C. vulgaris (L), TRHEAD.* (12) C. vulgaris (L), MESO.*
3.5.4. Endodermal cells and vascular elements
Ridged silicified endodermal cells were present in
Picea abies (BLOCK RIDGED, 18%). Conifers produced cubic to polyhedral blocky elements, consisting
of well-silicified transfusion elements, scattered or in
pairs, often with bordered pits (POLY CONIF). Isolated or in skeletons, they were extremely abundant in
Pinus mugo (71%; Plate VI(1– 2, 5, 9), less frequent
in P. abies (Plate VII(11)), Abies alba, Pinus cembra
and absent in Larix decidua.
Silicified rectangular platelets with pits (RECT
PITTED; Plate IX(3, 10) were rare (up to 1.4% in
Pinus cembra needles). They originate from transfusion cells and tracheary systems. RECT PITTED were
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57
Plate VI. Conifers. SEM micrographs of silicified tissues from plant tissues (N = needles, W = wood); *light microscope photographs. Scale
bar = 10 Am. (1) Pinus mugo (N), POLY CONIF. (2) P. mugo (N), POLY CONIF. (3) P. mugo (N), unknown. (4) P. mugo (N), unknown. (5) P.
mugo (N), POLY CONIF. (6) P. mugo (N), unknown. (7) P. mugo (N), TRACH.* (8) P. mugo (N), TRACH.* (9) P. mugo (N), POLY CONIF.*
(10) P. mugo (W), POLY. (11) P. mugo (W), POLY. (12) P. mugo (W), POLY.
identified in all conifer wood and needle samples
except for Larix decidua and Juniperus nana. These
types are also present in dicotyledons.
differentiate between species. Detailed descriptions of
conifer stomata morphology are available elsewhere
(Trautmann, 1953; Hansen, 1995).
3.5.5. Stomata
Silicified stomata (STO CON) were detected occasionally in needles. In Picea abies (Plate VII, 6),
Pinus cembra and Juniperus nana, stomata made up
about 10% of total types. No attempt was made to
3.5.6. Wood
Silicified cells in conifer wood were mainly nonidioblastic polyhedrons (POLY; Plates VI, 10 – 12,
VIII, 2– 4 and IX, 12. Other types occurring in wood
were POLY CONIF, RECT PITT and PLAT PERF.
58
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Plate VII. Conifers. SEM micrographs of silicified tissues from plant tissues (N = needles, W = wood); *light microscope photographs. Scale
bar = 10 Am. (1) Picea abies (N), UND. (2) P. abies (N), silica skeletons. (3) P. abies (N), UND. (4) P. abies (N), silica skeletons. (5) P. abies
(N), TRACH. (6) P. abies (N), STO CONIF.* (7) P. abies (N), UND.* (8) P. abies (N), UND.* (9) P. abies (N), UND.* (10) P. abies (N), JGS.*
(11) P. abies (N), POLY CONIF.*
3.6. Clustering analysis and PCA
In the dendrogram shown in Fig. 2 (Wards’ method, Euclidean distance, normalized data), species are
classified into two main clusters on the basis of
phytolith frequency: the first cluster groups monocotyledons (grasses and sedges), and the second cluster
groups dicotyledons and conifers. In the monocotyledon cluster, grasses were separated on the basis of
short cells (TRA), bulliform cells (BULL) and stomata (STO GRAM). Among grasses, Poa alpina and
Festuca scabriculmis were distinguished from other
grasses because of the high frequency of TRA LOB,
and STO GRAM, respectively. Within the monocotyledon cluster, Carex species were easily differentiated on the basis of CONE and STO CYP presence.
Dicotyledons and conifers were assigned to the
same cluster, mainly because of redundant polyhe-
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
59
Plate VIII. Conifers. SEM micrographs of silicified tissues from plant tissues (N = needles, W = wood); *light microscope photographs. Scale
bar = 10 Am. (1) Pinus cembra (N), silica skeleton. (2) P. cembra (W), POLY. (3) P. cembra (W), POLY with perforations scalariform. (4) P.
cembra (W), POLY. (5) P. cembra (W), POLY. (6) Juniperus nana (N), SPHE S. (7) J. nana (N), POLY. (8) J. nana (N), POLY. (9) J. nana (N),
POLY. (10) J. nana (N), POLY. (11) J. nana (N), POLY. (12) J. nana (N), TRACH.*
dral types (POLY). However, two groups were
differentiated: the first consisted of Ericaceae and
the second of conifers and Alnus viridis. Ericaceae
species were distinguished on the basis of the
presence of the types STO ERIC 1, STO ERIC 2
and JGS. Conifers were grouped by distinctive types
such as POLY CONIF. Alnus viridis was grouped
with conifers rather than with Ericaceae because of
the presence of epidermal long cells (L CELL
GRAINY) and microhairs (PAPILLAE); types absent
in the Ericaceae. It should be noted that Larix
decidua yielded diagnostic types (LARIX BLOCKY
W, LARIX SPIKY CELL) and that Pinus mugo was
negatively differentiated from all conifers by the
absence of silicified stomata (STO CON), and was
characterised by the abundance of POLY CONIF.
Thus, they were assigned to distinct branches of the
cluster. The robustness of this classification was
tested by using different data transformations (not
transformed percentage data, root transformed data
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A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
Plate IX. Conifers. SEM micrographs of silicified tissues from plant tissues (N = needles, W = wood); *light microscope photographs. Scale
bar = 10 Am. (1) Larix decidua (N), WAVY.* (2) L. decidua (N), WAVY. (3) L. decidua (N), TRACH.* (4) L. decidua (N), LARIX BLOCKY
W.* (5) L. decidua (N), LARIX BLOCKY W. (6) L. decidua (N), LARIX BLOCKY W. (7) L. decidua (N), L CELL. (8) L. decidua (N), L
CELL. (9) L. decidua (N), TRACH.* (10) L. decidua (N), LARIX SPIKY CELL. (11) L. decidua (W), POLY.*
and, finally, with groups of similar types summed in
one category, e.g., all trapezoids, not shown). No
matter which transformation was applied, the two
main clusters were maintained (monocotyledons,
dicotyledons– conifers) and the classification of the
monocotyledon cluster was unchanged. However,
according to the transformation chosen, some species
(Juniperus nana, A. viridis and Pinus cembra) were
attributed differently within the second cluster. Discrepancies were as follows. Normalised (Fig. 2) and
root-transformed data (not shown) gave the same
results. If the analysis was run with non-transformed
percentages, results were unchanged but the cluster
grouping P. cembra, A. viridis and J. nana showed a
weak affinity with the Ericaceae. With presence/
absence data, A. viridis and J. nana were not well
classified within a cluster, and showed only a weak
affinity with conifer and Ericaceae groups, respectively. Finally, when data of similar types were
combined in categories (non-transformed percentage
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
data; when several variants of a type were present in
a species, they were added together: i.e., all trapezoids,
rods, cones, trichomes and polygonal) P. cembra, A.
viridis and J. nana were attributed to the Ericaceae
cluster.
In addition, when a test was run, keeping leaf and
wood data separate (percentage data non-transformed,
Euclidean distance; not shown), the classification was
similar but a further cluster, grouping all wood samples, was present. This cluster showed an affinity
between wood samples and samples from conifers
needles of Juniperus nana and Ericaceae leaves of
Arctostaphylos uva-ursi and Alnus viridis.
PCA classification is a multivariate ordination
technique, employed here to examine the degree of
correspondence between types and taxa (Fig. 3, Table
6). The first axis of the principal components analysis
explains the majority of the variability (45%). Such a
high percentage can be explained by the strong
diagnostic power of short cells that are unique and
largely dominant in grass species.
PCA run on square root transformed data confirmed the classification proposed by the cluster
analysis: the species were divided into two main
groups (monocotyledons and dicotyledons with coni-
Table 6
PCA loadings for each species, labels are explained in Fig. 3
Species
Factor 1
Factor 2
V1
V2
V3
V4
V5
V6
V7
V8
V9
V10
V11
V12
V13
V14
V15
V16
V17
V18
V19
V20
V21
0.2017522
0.1863757
0.0175233
0.1660261
0.0787601
0.0646531
0.0423945
0.4103878
0.8037481
0.9190497
0.8196555
0.7163232
0.7541657
0.8580057
0.7323243
0.8447424
0.9508866
0.7586679
0.8886325
0.8681059
0.9083434
0.7932636
0.6935168
0.8875576
0.7194143
0.8286935
0.6046596
0.0108916
0.0587367
0.0046828
0.0571643
0.0135351
0.0108368
0.0350921
0.0717067
0.0067158
0.0479644
0.0863568
0.0133594
0.1289849
0.0714046
0.0823253
61
fers). Carex species were separate. If the PCA was run
with similar types added together in categories (as was
done for cluster analysis) the classification did not
vary, but points were less scattered (not shown).
4. Discussion
In this study, biogenic silica extracted from 21
species either dominant or abundant at the subalpine – alpine ecocline were examined to obtain an
inventory of phytolith types. Of the 21 species, 19
were studied for the first time for phytoliths.
4.1. Monocotyledons
It is known that grasses and sedges yield typical
phytoliths (e.g., Twiss et al., 1969; Mulholland and
Rapp, 1992; Ollendorf, 1992). A morphological
classification for short cells related to grass taxonomy has been proposed (Twiss et al., 1969). This
classification is based on the fact that short cell
morphology is in general distinctive in three of the
five subfamilies occurring in the world: Festucoideaea, Panicoideae and Clorideae, the other two are
Arundinoideae and Bambusoideae). All grasses examined here belonged to the Festucoideae and
produced only short cells of trapezoidal shape
(TRA sensu lato). Present data confirmed that the
genera of this subfamily could not be distinguished
on the basis of short cell morphology. In this set of
grass species, the only types that were characteristic
at species level were branched rods (ROD BR) that
were unique to Nardus stricta (Parry and Smithson,
1958a). However, it should be noted that lobate
trapezoids (TRA LOB), although not diagnostic,
were largely dominant in Poa alpina. CONES were
characteristic of the Cyperaceae family. However, a
study on modern phytolith assemblages of subalpine – alpine grasslands showed that CONES are
poorly preserved in soil (Carnelli, 2002; Runge,
personal communication). Gramineae and Cyperaceae are known to produce a significant percentage
of silicified above-ground tissues; in a previous
study, it was shown that subalpine and alpine
grasses and sedges from the Central Alps produced
between 0.6% and 5.6% of silicification of dry plant
mass.
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4.2. Dicotyledons
Phytolith studies often neglect wild dicotyledon
species. The dicotyledons examined here belonged
mainly to the Ericaceae. Species of this family are
often dominant at the treeline, where they can form
extensive heaths. We are aware of only one study
mentioning the Ericaceae; it covers East African
plants and discusses the species Vaccinium stanley
(Runge, 1999). Subalpine –alpine heath species produced silicified cells mainly from the epidermis
(JGS). These types are, however, commonly recovered in all dicotyledons. Distinctive stomata complexes (STO ERIC 1, STO ERIC 2) were present.
The species studied accumulated low percentages of
biogenic silica in leaves and wood, with a maximum
value for Calluna vulgaris, in which silicified tissues
were 0.68% of leaves’ dry mass (Carnelli et al., 2001).
4.3. Conifers
Conifers are dominant in the subalpine forest and
their contribution to phytolith assemblages cannot be
neglected when investigating biogenic silica in plants
at the treeline. A few species of conifers, mainly
American, have been investigated (Klein and Geis,
1978), but data on European species are lacking:
Picea abies, Abies alba, Juniperus nana, Pinus cembra and Pinus mugo were examined here for the first
time.
In conifers, silicification was detected both in
needles and in wood. Larch epidermal phytoliths,
varying greatly in size and shape but very thin and
fragile, were earlier described for Larix laricina (Du
Roi) K. Koch and Larix decidua Mill. (Klein and
Geis, 1978). Klein and Geis (1978) after examining
15 taxa of Pinaceae stated that the identification of
conifers was possible on the basis of tracheary elements, blocky polyhedrons and epidermal cells. However, on the basis of the present result, epidermal cells
should not be taken as diagnostic, because they are
similar to the long cells occurring in grass species, and
fragmentation after deposition in the soil will make
distinction impossible (Plate IX(7 –8)).
Conifer-specific phytoliths (POLY CONIF), produced in tranfusion tracheids and endodermal cells,
were very frequent in Pinus mugo. This type was also
mentioned by Klein and Geis (1978) although fre-
quency was not assessed. The same types were
extracted from conifer needles (Abies balsamea, Picea
glauca and Pinus banksiana) and topsoils in boreal
forest (Bozarth, 1993). Non-idioblastic polyhedral
phytoliths (POLY) were dominant in woody tissues.
However, being highly redundant, they did not add
any relevant taxonomic information and they should
not be used for palaeoecological reconstructions.
Among conifers, Larix decidua and Picea abies
contained the highest proportion of biogenic silica
(1.09% and 0.85% of dry mass, respectively) (Carnelli et al., 2001) and needles were extensively
silicified, including epidermal tissues. In the remaining conifers, silicification was less extensive (about
0.01% of dry mass) and mainly endodermal cells
were biomineralised.
4.4. Cluster analysis and PCA
Cluster analysis and PCA results only partially
supported the hypothesis that taxonomically related
species can be identified on the basis of type presence
and frequency. Indeed, while monocotyledon plants
could be clearly identified, dicotyledons and conifers
were less clearly separated. Both classification and
ordination methods evidenced that the taxonomical
power of phytoliths described here was limited for
species yielding mainly redundant types such as
Juniperus nana, Alnus viridis and Pinus cembra.
These could not be unequivocally identified on the
basis of phytoliths. In contrast, idioblastic types from
key species may be diagnostic at family, genus or
even at species level (e.g., Cyperaceae, Pinus mugo,
Larix decidua and Calluna vulgaris). However, it is
important to stress that, in general, herbaceous and
woody species could be identified, the former yielding
diagnostic types, the latter being defined by some
specific types. This finding is relevant when applied
to the study of assemblages of fossil phytoliths, e.g.,
in soils.
4.5. Potential relevance of phytoliths when studying
the subalpine treeline
The subalpine –alpine ecocline is a transition zone
of heathland, stunted trees and meadows that occurs
above the timberline (i.e., the limit of rather closed
forest with trees 6– 8 m or taller). The present tim-
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
berline in the Central Swiss Alps is located between
2000 and 2300 m a.s.l. However, its present elevation
is largely anthropogenically determined (e.g., Theurillat et al., 1998; Tinner and Theurillat, 2003; Carnelli
et al., in press). Land use since the Neolithic period
has resulted in an artificial extension downward of
alpine meadows, both for grazing and timber exploitation. Therefore, the uppermost limits attained by the
forest during the Holocene, and even the natural
occurrence of alpine meadows and heathlands are
debated issues. The history and dynamic of vegetation
at the treeline was investigated mainly by means of
pollen, plant macrorest and soil charcoal analysis
(e.g., Burga, 1991, 1995; Tinner et al., 1996; Wick
and Tinner, 1997; Talon et al., 1998; Carcaillet and
Brun, 2000; Carnelli et al., in press; Tinner and
Theurillat, 2003). The analysis of soil-borne phytoliths may supply a new perspective in the reconstruction of the history of vegetation at the subalpine –
alpine ecocline by enhancing the possibility of detecting taxa, such as monocotyledons, that are usually
under-represented in palaeobotanical records.
However, soil-borne phytolith assemblages were of
limited use for palaeoecological reconstruction. (1)
The diagnostic power of phytoliths was limited by the
fact that similar types could, in some cases, be
produced by plants of unrelated taxa. (2) The occurrence of a given type in plant tissues did not guarantee
that it would be found in soil assemblages, since a
differential preservation of phytoliths may occur in
soil (Carnelli, 2002; Bartoli and Wilding, 1980). (3)
Yet the combination of qualitative (i.e., the inventory
of type frequencies) and quantitative (biogenic silica
production) analysis may be a promising tool (Carnelli, 2002). It was shown in a previous study (Carnelli et al., 2001) that the heavily silicified aboveground tissues of grasses and sedges produce an
annual biogenic silica input of 1.9 – 10.3 g m 2 in
the subalpine and alpine meadows in the Central Alps.
In comparison, the estimated annual production of
biogenic silica from subalpine heaths would be between 0.19 and 1.13 g m 2, i.e., about one order of
magnitude smaller than the predicted input of meadows, as well as the annual input of biogenic silica of a
Larix decidua subalpine forest (2.4 g m 2 year 1) or
of a Picea excelsa forest (0.7 g m 2 year 1). Thus,
the combination of quantitative analysis of biogenic
silica production and the inventory of type frequencies
63
may provide an estimate of the potential frequency of
types in soil assemblages (Carnelli et al., 2001) and
the comparison with findings in soil should help
towards a better understanding of the taphonomical
processes phytoliths undergo.
In addition, the chemical composition of opal
could be a valuable tool to source phytoliths lacking
distinctive morphology: indeed, it was shown that the
presence of aluminium in the reticule of biogenic
silica was very frequent in woody species phytoliths
but negligible in grass and sedge species (Bartoli and
Wilding, 1980; Carnelli et al., 2002).
It should be noted that, although conifers and
dwarf shrubs produced low amounts of silica, phytoliths contained in persistent needles or leaves and in
woody tissue persisted in the plant for several years.
Therefore, they were less hydrated and often accumulated aluminium (Bartoli, 1985; Carnelli et al., 2002).
For these reasons, once released in soil, they were
likely to be better preserved than the more soluble
phytoliths from yearly abscised Larix needles or grass
leaves.
5. Conclusions
In this paper, descriptions of species and related
types were grouped under three taxa: conifers, dicotyledons (mainly Ericaceae) and monocotyledons. Interestingly, this framework reflected the three main
physiognomical units of vegetation at the subalpine –
alpine ecocline: coniferous forests, alpine heathlands
(dominated by woody dicotyledons) and alpine meadows (dominated by monocotyledons). Our results
showed that it was possible identify these three groups
by using phytolith morphology to differentiate them
and that there was a rationale for the utilisation of
phytolith soil fossils in order to study past interactions
between these plant communities. Indeed, quantitative
and qualitative analysis of biogenic silica in subalpine –alpine soils may give a record of past altitudinal
fluctuations of woody versus herbaceous vegetation
during the Holocene, triggered by variations of climate and/or by the impact of human activities. This is
now a subject of general concern in view of the
predicted climate modification which is very likely
to have an enormous influence on high alpine ecosystems (Theurillat et al., 1998; Theurillat and Guisan,
64
A.L. Carnelli et al. / Review of Palaeobotany and Palynology 129 (2004) 39–65
2001). Information about past ecosystem fluctuations
is essential in order to understand patterns of vegetation resistance and resilience and thus be able to
forecast future ecosystem responses.
Acknowledgements
This work was supported by the Swiss National
Science Foundation (project FNRS 31-52911.97 to J.P. Theurillat). We thank Prof. Walter Wildi and Prof.
Brigitta Ammann for logistic support and discussion;
Rossana Martini, Philippe Clerc, Dario Zürcher and
Luca Malgeri for help at SEM, light microscopy and
with photographs, respectively. The English language
was kindly revised by Julie Warrillow. The paper was
improved, thanks to the revision of Freya Runge and
Irwin Rovner.
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