Annals of Botany 87: 789ą794, 2001
doi:10.1006/anbo.2001.1407, available online at http://www.idealibrary.com on
Seasonal Dimorphism in the Mediterranean Cistus incanus L. subsp. incanus
GIOVANNA ARONNE* and VERONICA DE MICCO
Laboratorio di Ecologia Riproduttiva, Dipartimento di Arboricoltura, Botanica e Patologia Vegetale (Sezione
Botanica), Universita� degli Studi di Napoli `Federico II', via Universita� 100, 80055 Portici (Napoli), Italy
Received: 20 November 2000 Returned for revision: 5 January 2001 Accepted: 23 February 2001
Mediterranean perennial species are described as being sclerophyllous, or summer deciduous, or seasonally
dimorphic. Field observation in the coastal maquis of Castelvolturno Nature Reserve, southern Italy, showed that
Cistus incanus L. subsp. incanus is a seasonally dimorphic species as it develops brachyblasts with small leaves in
summer, and dolichoblasts with large leaves in winter. Field biometric data con�rmed that winter shoots were 14-
times longer than those developed in summer and had many more leaves. The area of single winter leaves was �ve-
times that of summer leaves. Anatomical leaf structure also changed with the season: winter leaves were Żat while
summer leaves had a crimped lamina which was partially rolled to form crypts in the lower surface. Leaves were
covered by considerably more trichomes in summer than in winter. Stomata were uniformly distributed along the
lower epidermis of winter leaves but were only present in the crypts of summer leaves. In summer leaves, a palisade
layer was often found on both sides of the lamina, the mesophyll cells were generally smaller and the intercellular
spaces were reduced. Winter leaves had a dorsiventral structure and larger intercellular spaces. Seasonal dimorphism
is generally reported to be an adaptation to summer drought. However, the morphology and anatomy of C. incanus
L. subsp. incanus showed that the subspecies has not only developed a strategy to survive summer drought, but has
evolved two di�erent habits, one more xerophytic than the other, to optimize adaptation to the seasonal climatic
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changes occurring in Mediterranean environments. 2001 Annals of Botany Company
Key words: Cistus, Cistus incanus L. subsp. incanus, climatic changes, leaf anatomy, leaf dimorphism, Mediterranean
shrubs, phenology, seasonal dimorphism.
INTRODUCTION 1987; Stephanou and Manetas, 1997; Gratani and
Bombelli, 1999). However, to date, no investigation has
The Mediterranean-type climate is characterized by hot, dry
de�ned the biometrical and leaf anatomical di�erences
summers alternating with cool, wet winters (Daget, 1977;
between summer and winter habits of Cistus plants. In the
Nahal, 1981). The seasonal Żuctuations in soil moisture are
present work, phenology and seasonal changes in shoot
considered a limiting factor for growth and productivity of
biometry, leaf morphology and anatomy were studied in
Mediterranean perennial species (Mitrakos, 1980; Specht,
Cistus incanus L. subsp. incanus. The nomenclature for
1987). According to the severity of the summer drought,
C. incanus L. subsp. incanus follows Warburg (1968).
Mediterranean ecosystems can be distributed along a
gradient which has maquis with evergreen sclerophylls at
the wet end, and garigue with seasonally dimorphic species
MATERIALS AND METHODS
at the dry end (Margaris, 1981). Evergreen sclerophylls are
Plant material was collected at Castelvolturno Nature
characterized by small, thick, leathery, long-lived leaves
Reserve on the Tyrrhenian coast, north of the Bay of
(Margaris, 1981). Seasonally dimorphic species are charac-
Naples (southern Italy). The site is situated on stabilized
terized by a seasonal reduction in their transpiring surface
sand dunes and has a typical Mediterranean climate
which is achieved by shedding the larger winter and spring
(Daget, 1977; Nahal, 1981) with an annual rainfall of
leaves growing on dolichoblasts and developing smaller
about 1000 mm, but with precipitation concentrated in
summer leaves on new brachyblasts (Orshan, 1964, 1972).
autumn and winter, followed by a dry summer. The
Species which exhibit seasonal dimorphism are reported
vegetation, which is subject to �re, varies from 0.5 to 3 m
in di�erent Mediterranean-type ecosystems (Orshan, 1964,
in height and is characterized by a patchwork mosaic of
1972; Margaris, 1981). As regards the Mediterranean
shrub species and restricted gap areas colonized by
region, this habit was described for species from the
therophytes. The co-dominant species are Phillyrea latifolia
Greek phrygana (Margaris, 1975, 1977; Margaris and
L., Pistacia lentiscus L., Rhamnus alaternus L., Myrtus
Vokou, 1982; Christodoulakis, 1989; Christodoulakis
communis L., Rosmarinus o�cinalis L., Cistus salvifolius L.
et al., 1990; Kyparissis and Manetas, 1993a, b).
and Cistus incanus L. subsp. incanus.
The morphology, physiology and leaf anatomy of Cistus
In spring 1996, �ve plants of Cistus incanus L. subsp.
species are reported in several studies (e.g. Harley et al.,
incanus were randomly selected in the �eld and branches
were tagged to follow shoot development. On each plant,
* For correspondence. Fax �39 081 7755114, e-mail aronne@unina.
it ten shoots were sampled for biometric measurements both
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0305-7364/01/060789+06 $35.00/00 2001 Annals of Botany Company
790 Aronne and De Micco�Seasonal Dimorphism in Cistus incanus L.
at the end of April, before Żowering and the dry period, and re-grow and develops a stem with long internodes and large
in September, before the autumn rains. Winter and summer leaves (dolichoblast). This growth ceases in late spring when
shoot elongation and the area of each leaf on the shoot were
the terminal bud becomes an inŻorescence (Fig. 1B).
measured, and the number of leaves that formed during the
Subsequently, the large leaves are shed and new brachyblasts
two seasons was also counted. Leaf area was measured by
develop from the axillary buds (Fig. 1C). This cyclic process
digitizing leaf images and analysing them with `Plant
determines the round shape of such bushes (Fig. 1D).
Meter', a software program specially devised for measure-
Another di�erence between the two habits regards lamina
ment of lines and areas.
inclination which is horizontal in winter leaves and almost
In both seasons, three leaves per plant were also sampled
vertical in summer leaves.
for subsequent anatomical observation. The leaves were
Field observations were corroborated by biometric
�xed in a mixture of 40 % formaldehyde : glacial acetic
measurements (Table 1). Winter shoots were on average
acid : 50 % ethanol (5 : 5 : 90 by volume) for several days, cut
14-times longer than those developed in summer and had
into pieces of approx. 5 5 mm, dehydrated in an ethanol
about four-times the number of leaves. However, leaf
series and embedded in JB41 wax (Polysciences, Warring-
density, i.e. the ratio between leaf number and shoot length,
ton, PA, USA). Leaf sections (5ą8 mm) were stained with
was almost four-fold lower in winter than in summer
0.5 % toluidine blue in water (Jensen, 1962) and observed
shoots. As regards leaf area, winter leaves were �ve-times
under a transmitted light microscope (BX60, Olympus,
larger than those developed in summer. Therefore, summer
Hamburg, Germany). A digital micrograph of one section
shoots are shorter with fewer, more densely packed, small
per leaf from the area of the maximum leaf width was
leaves while winter shoots have long stems with many larger
obtained with a digital camera (Olympus, CAMEDIA
leaves.
C2000). The 30 images (one section three leaves �ve
plants two seasons) were analysed using the image Interestingly, no interplant variability was found in any
analysis system, `Plant Meter'. Hair density (n mm 1) and parameter measured on summer samples, while very signi-
stomatal density (n mm 1) were calculated by counting,
respectively, the number of stalks and stomata present
along the section on both abaxial and adaxial sides, and
TABLE 1. Biometric data from �ve plants of Cistus incanus
measuring the length of the section analysed. Similarly, for
randomly selected in the �eld and measured at the end of the
each image, the thickness of the palisade layer as well as the
summer and winter growth periods respectively
minimum and maximum distance between the upper and
lower epidermises (thickness) of the lamina were measured.
Summer Winter
growth growth t
RESULTS
Shoot length (cm) 0.8 11.2 P 5 0.001
Number of leaves per shoot 3 11 P 5 0.001
In C. incanus L. subsp. incanus, each axillary bud grows out
Number of leaves per shoot/shoot 3.8 1.0 P 5 0.001
in summer, producing a shoot with short internodes
length (n cm 1)
(brachyblast), small leaves and a leaf terminal bud
Leaf area (mm2) 67 339 P 5 0.001
(Fig. 1A). At the end of the summer, after the �rst autumn
rains, summer leaves are shed. The terminal bud begins to Mean values and signi�cance of Student's t-test.
FIG. 1. Schematic view of C. incanus growth: summer brachyblasts (A); brachyblasts and dolichoblasts (B); development of new brachyblasts after
shedding of winter leaves (C); development of new dolichoblasts (D).
Aronne and De Micco�Seasonal Dimorphism in Cistus incanus L. 791
TABLE 2. Interplant variability of biometric measurement in Seasonal dimorphism has been reported to be an
summer and winter among the �ve marked plants of Cistus adaptive strategy to the seasonal climatic changes occurring
incanus at Castelvolturno in Mediterranean habitats (Orshan, 1964, 1972; Christo-
doulakis, 1989; Christodoulakis et al., 1990; Kyparissis and
Summer growth Winter growth Manetas, 1993b; Kyparissis et al., 1997). We have described
this habit for C. incanus at Castelvolturno, suggesting that
Shoot length (cm) 0.376 0.002
the species is well adapted to the rhythmic Żuctuation of the
Number of leaves per shoot 0.922 0.011
Mediterranean climate. Development of brachyblasts in
Number of leaves per shoot/shoot 0.561 0.019
summer and dolichoblasts in winter is reported for other
length (n cm 1)
Cistus species (Floret et al., 1989). In C. incanus, most of the
Leaf area (mm2)0.059 0.000
growth in terms of shoot length, number of leaves and leaf
Signi�cance (P-values) of ANOVA. area occurs in winter. During summer, growth is similar in
the whole population because it is limited by drought to the
minimal values for survival, while in winter no limiting
�cant di�erences were reported when the same parameters
factors a�ect plant growth and biometric parameters di�er
were measured in winter (Table 2).
signi�cantly among individuals.
Transverse sections of winter and summer leaves also
Steep leaf inclination has been described for many species
showed di�erences in their anatomy. Winter leaves were
in di�erent environments and interpreted as a strategy to
Żat, while summer leaves had a crimped lamina which was
reduce the amount of direct solar radiation, resulting in
partially rolled to form several crypts in the lower surface
lower leaf temperature and transpiration rates, and avoid-
(Fig. 2A, C).
ance of damage to the photosynthetic apparatus (Miller,
Lamina thickness was not uniform either in summer or
1967; Mooney et al., 1977; Comstock and Mahall, 1985; He
winter leaves (Figs 2 and 3): signi�cant di�erences were
et al., 1996; Gratani and Bombelli, 1999; Werner et al.,
found between the minimum and maximum distance
1999). Erect summer leaves of C. incanus maximize light
between the upper and lower epidermis of each section in
interception in the early morning and late afternoon,
both kinds of leaves. Within each leaf, the variation in
keeping noon interception to a minimum. This allows the
thickness (ratio between maximum and minimum widths)
species to tolerate very hot environments by physically
was signi�cantly greater in summer than in winter leaves.
evading the midday sun. By contrast, during autumn, winter
Therefore, the variation in the lamina thickness of a single
and spring, when drought is not a limiting environmental
leaf was greater in summer leaves.
factor, horizontal leaves optimize direct solar radiation.
Upper epidermal cells were much larger in winter than in
Di�erent leaf inclination in summer and winter was also
summer leaves (Fig. 2B). The palisade parenchyma was
reported for C. incanus by Gratani and Bombelli (1999). We
signi�cantly thicker in winter (84 mm) than in summer
suggest that the occurrence of vertical leaves in summer and
leaves (53 mm). However, in summer leaves the palisade
horizontal leaves in winter is a strategy that evolved in
tissue was often present on both sides of the lamina
C. incanus to obtain the best advantage from solar radiation
(Fig. 2E) and the mesophyll cells were generally smaller
in both seasons.
with reduced intercellular spaces. As a result, the whole
This dual adaptation is also corroborated by leaf
structure was more compact. Moreover, in summer leaves,
anatomy: summer leaves frequently have a palisade layer
single palisade cells often had undulating walls forming
under both epidermises while winter leaves have a typical
inward and outward folds alternately (Fig. 2E).
dorsiventral structure. The presence of a palisade layer on
Both leaf surfaces were covered by a thick layer of white
both leaf surfaces, together with a mesophyll composed of
trichomes�stellate hairs consisting of a stalk and eight-18
smaller cells and reduced intercellular spaces, is reported to
long branches. In both kinds of leaves there were
be characteristic of xerophytic species (Shields, 1950). These
signi�cantly more trichomes on the lower than on the
traits are found in summer leaves of C. incanus but not in
upper surface (Fig. 4). However, trichome density was
winter ones which show longer palisade cells only under the
much higher in summer than in winter leaves.
upper epidermis, together with wider intercellular spaces.
In both kinds of leaves, stomata were present only on the
The occurrence of anatomical di�erences between summer
lower surface (Fig. 2), being uniformly distributed along the
and winter leaves is in agreement with reports for other
lower epidermis of winter leaves but found almost
seasonal dimorphic species (Christodoulakis, 1989; Christo-
exclusively in the crypts of summer leaves (Figs 2F and 5).
doulakis et al., 1990; Kyparissis and Manetas, 1993a).
Moreover, a lower mesophyll cell density and larger inter-
cellular spaces compared to the sclerophyllous Phillyrea
DISCUSSION
latifolia and Quercus ilex were reported for leaves of
Xerophytes are dry habitat plants with transpiration C. incanus sampled in October (Gratani and Bombelli,
decreasing to a minimum under conditions of water de�cit 1999).
(Maximov, 1931). Certain tissues of xerophytes, particu- In summer leaves of C. incanus, we observed palisade
larly leaf tissues, become altered structurally in relation to cells with involuted walls. This anatomical feature is well
the environment, and plant survival depends upon the known in some evergreen conifers and is reported in
ability to withstand desiccation without permanent injury Caesalpinioid legumes (Curtis et al., 1996). Although their
(Shields, 1950). real function has not yet been ascertained, it has been
792 Aronne and De Micco�Seasonal Dimorphism in Cistus incanus L.
FIG. 2. Light microscope view of cross-sections of C. incanus winter leaves (A, B), and summer leaves (CąF). E, Large epidermal cells; t,
fragments of the numerous trichomes; c, crypt; s, stomata (s). Bars � 100 mm.
Aronne and De Micco�Seasonal Dimorphism in Cistus incanus L. 793
radiation. Trichomes are reported to be inferior to the
cutinous coat in reducing transpiration (Yapp, 1912),
except in strong sunlight where the cuticle has less
protective value (Wiegand, 1910). Leaf pubescence is
reported to be an adaptation to the Mediterranean
environment by reducing transpiration, increasing the
probability of water uptake by leaves, maintaining favour-
able leaf temperature, and protecting against UV-B
radiation responsible for photosynthetic inhibition (Save�
et al., 2000). Where a single species exists in a mesophytic
and xerophytic form, Shields (1950) found the latter to be
more hairy. Therefore, in the more hairy summer leaves of
C. incanus, light intensity and transpiration should be lower
FIG. 3. Mean values and s.d. of minimum (F) and maximum (h) than in winter leaves, suggesting the occurrence of two
thickness of the lamina in summer (SL) and winter (WL) leaves of
levels of leaf xeromorphism.
C. incanus.
Plants with small leaves are more common in dry habitats
(Fahn, 1964). A very common characteristic of xeromorphic
leaves is a reduced external area and a lower surface area to
volume ratio (McDougall and Penfound, 1928). A signi�-
cant reduction in the leaf area occurs in C. incanus during
the drier season, and this, together with the modi�cations in
internal leaf structure, allows the species to optimize
environmental seasonal conditions.
The Żat structure of the lamina is characteristic of meso-
morphic leaves, but a crimped lamina, folded to form crypts
in which stomata are concentrated, is reported to be an
adaptive strategy to drought (Strasburger et al., 1982). Leaf
rolling is described for summer leaves of seasonal dimorphic
Mediterranean species to reduce light interception (Ehler-
inger and Comstock, 1987; Kyparissis and Manetas, 1993a;
Gratani and Bombelli, 1999). We have shown that C. incanus
FIG. 4. Number of trichomes found along leaf sections of both lower
develops Żat leaves in winter and folded leaves, with wider
(F) and upper (h) surfaces. Mean values and s.d. are reported for
variation in lamina thickness, in summer. Therefore, leaf
summer (SL) and winter (WL) leaves.
structure is optimized according to seasonal environmental
changes occurring in the Mediterranean.
Stomatal distribution is di�erent between the two leaf
types. Stomata are uniformly distributed on the lower
surface of the Żat winter leaves, whereas they are concen-
trated in the crypts of summer leaves to reduce evapo-
transpiration, as reported for other Mediterranean species
such as Nerium oleander L. (Strasburger et al., 1982).
Large epidermal cells, as well as a strati�ed epidermis, are
described as water storage structures characteristic of
xerophytes and are also present in the evergreen Mediterra-
nean species Nerium oleander L. and Rosmarinus o�cinalis
L. (Strasburger et al., 1982). In C. incanus, large epidermal
cells of winter leaves would support the populations during
occasional periods of winter drought.
FIG. 5. Mean number and s.d. of stomata found along leaf sections of In Mediterranean environments, perennial species are
winter leaves (WL) and summer leaves outside the crypt (SL-out) and
either sclerophyllous, summer deciduous, or seasonally di-
inside the crypt (SL-in).
morphic (Margaris, 1981). According to Orshan (1964,
1972), the latter is an adaptation to summer drought.
speculated that they are an important anatomical adap- Christodoulakis et al. (1990) described seasonal dimorphism
tation to periodic drought. Under water stress these cells for Sarcopoterium spinosum as a major strategy which pro-
should lose water and shrink, reducing the thickness of the duces `seasonally di�erent plants' from the same individual,
entire leaf. When water becomes available again, they might that can successfully stand the variety of unfavourable
quickly enlarge, causing the leaf to expand in thickness Mediterranean conditions. The overall consideration of
(Curtis et al., 1996). phenology, morphology and leaf anatomy of C. incanus is in
Light intensity is also decreased by the hairy covering of agreement with the conclusion by Christodoulakis et al.
leaves, which is thicker during the season of greatest solar (1990). We suggest that C. incanus has evolved two di�erent
�
794 Aronne and De Micco�Seasonal Dimorphism in Cistus incanus L.
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