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Annals of Botany 87: 789±794, 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 G IOVA N N A A RO N N E* and V E RO NI CA DE M IC CO Laboratorio di Ecologia Riproduttiva, Dipartimento di Arboricoltura, Botanica e Patologia Vegetale (Sezione Botanica), UniversitaÁ degli Studi di Napoli `Federico II', via UniversitaÁ 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 14times longer than those developed in summer and had many more leaves. The area of single winter leaves was ®vetimes that of summer leaves. Anatomical leaf structure also changed with the season: winter leaves were ¯at 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 dierent habits, one more xerophytic than the other, to optimize adaptation to the seasonal climatic # 2001 Annals of Botany Company changes occurring in Mediterranean environments. Key words: Cistus, Cistus incanus L. subsp. incanus, climatic changes, leaf anatomy, leaf dimorphism, Mediterranean shrubs, phenology, seasonal dimorphism.
I N T RO D U C T I O N The Mediterranean-type climate is characterized by hot, dry summers alternating with cool, wet winters (Daget, 1977; Nahal, 1981). The seasonal ¯uctuations in soil moisture are considered a limiting factor for growth and productivity of Mediterranean perennial species (Mitrakos, 1980; Specht, 1987). According to the severity of the summer drought, Mediterranean ecosystems can be distributed along a gradient which has maquis with evergreen sclerophylls at the wet end, and garigue with seasonally dimorphic species at the dry end (Margaris, 1981). Evergreen sclerophylls are characterized by small, thick, leathery, long-lived leaves (Margaris, 1981). Seasonally dimorphic species are characterized by a seasonal reduction in their transpiring surface which is achieved by shedding the larger winter and spring leaves growing on dolichoblasts and developing smaller summer leaves on new brachyblasts (Orshan, 1964, 1972). Species which exhibit seasonal dimorphism are reported in dierent Mediterranean-type ecosystems (Orshan, 1964, 1972; Margaris, 1981). As regards the Mediterranean region, this habit was described for species from the Greek phrygana (Margaris, 1975, 1977; Margaris and Vokou, 1982; Christodoulakis, 1989; Christodoulakis et al., 1990; Kyparissis and Manetas, 1993a, b). The morphology, physiology and leaf anatomy of Cistus species are reported in several studies (e.g. Harley et al., it
* For correspondence. Fax 39 081 7755114, e-mail aronne@unina.
0305-7364/01/060789+06 $35.00/00
1987; Stephanou and Manetas, 1997; Gratani and Bombelli, 1999). However, to date, no investigation has de®ned the biometrical and leaf anatomical dierences between summer and winter habits of Cistus plants. In the present work, phenology and seasonal changes in shoot biometry, leaf morphology and anatomy were studied in Cistus incanus L. subsp. incanus. The nomenclature for C. incanus L. subsp. incanus follows Warburg (1968). M AT E R I A L S A N D M E T H O D S Plant material was collected at Castelvolturno Nature Reserve on the Tyrrhenian coast, north of the Bay of Naples (southern Italy). The site is situated on stabilized sand dunes and has a typical Mediterranean climate (Daget, 1977; Nahal, 1981) with an annual rainfall of about 1000 mm, but with precipitation concentrated in autumn and winter, followed by a dry summer. The vegetation, which is subject to ®re, varies from 0.5 to 3 m in height and is characterized by a patchwork mosaic of shrub species and restricted gap areas colonized by therophytes. The co-dominant species are Phillyrea latifolia L., Pistacia lentiscus L., Rhamnus alaternus L., Myrtus communis L., Rosmarinus ocinalis L., Cistus salvifolius L. and Cistus incanus L. subsp. incanus. In spring 1996, ®ve plants of Cistus incanus L. subsp. incanus were randomly selected in the ®eld and branches were tagged to follow shoot development. On each plant, ten shoots were sampled for biometric measurements both # 2001 Annals of Botany Company
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at the end of April, before ¯owering and the dry period, and in September, before the autumn rains. Winter and summer shoot elongation and the area of each leaf on the shoot were measured, and the number of leaves that formed during the two seasons was also counted. Leaf area was measured by digitizing leaf images and analysing them with `Plant Meter', a software program specially devised for measurement of lines and areas. In both seasons, three leaves per plant were also sampled for subsequent anatomical observation. The leaves were ®xed in a mixture of 40 % formaldehyde : glacial acetic acid : 50 % ethanol (5 : 5 : 90 by volume) for several days, cut into pieces of approx. 5 5 mm, dehydrated in an ethanol series and embedded in JB41 wax (Polysciences, Warrington, PA, USA). Leaf sections (5±8 mm) were stained with 0.5 % toluidine blue in water (Jensen, 1962) and observed under a transmitted light microscope (BX60, Olympus, Hamburg, Germany). A digital micrograph of one section per leaf from the area of the maximum leaf width was obtained with a digital camera (Olympus, CAMEDIA C2000). The 30 images (one section three leaves ®ve plants two seasons) were analysed using the image analysis system, `Plant Meter'. Hair density (n mm ÿ1) and stomatal density (n mm ÿ1) were calculated by counting, respectively, the number of stalks and stomata present along the section on both abaxial and adaxial sides, and measuring the length of the section analysed. Similarly, for each image, the thickness of the palisade layer as well as the minimum and maximum distance between the upper and lower epidermises (thickness) of the lamina were measured. R E S U LT S In C. incanus L. subsp. incanus, each axillary bud grows out in summer, producing a shoot with short internodes (brachyblast), small leaves and a leaf terminal bud (Fig. 1A). At the end of the summer, after the ®rst autumn rains, summer leaves are shed. The terminal bud begins to
re-grow and develops a stem with long internodes and large leaves (dolichoblast). This growth ceases in late spring when the terminal bud becomes an in¯orescence (Fig. 1B). Subsequently, the large leaves are shed and new brachyblasts develop from the axillary buds (Fig. 1C). This cyclic process determines the round shape of such bushes (Fig. 1D). Another dierence between the two habits regards lamina inclination which is horizontal in winter leaves and almost vertical in summer leaves. Field observations were corroborated by biometric measurements (Table 1). Winter shoots were on average 14-times longer than those developed in summer and had about four-times the number of leaves. However, leaf density, i.e. the ratio between leaf number and shoot length, was almost four-fold lower in winter than in summer shoots. As regards leaf area, winter leaves were ®ve-times larger than those developed in summer. Therefore, summer shoots are shorter with fewer, more densely packed, small leaves while winter shoots have long stems with many larger leaves. Interestingly, no interplant variability was found in any parameter measured on summer samples, while very signi-
T A B L E 1. Biometric data from ®ve plants of Cistus incanus randomly selected in the ®eld and measured at the end of the summer and winter growth periods respectively
Shoot length (cm) Number of leaves per shoot Number of leaves per shoot/shoot length (n cm ÿ1) Leaf area (mm2)
Summer growth
Winter growth
t
0.8 3 3.8
11.2 11 1.0
P 5 0.001 P 5 0.001 P 5 0.001
67
339
P 5 0.001
Mean values and signi®cance of Student's t-test.
F I G . 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 MiccoÐSeasonal Dimorphism in Cistus incanus L. T A B L E 2. Interplant variability of biometric measurement in summer and winter among the ®ve marked plants of Cistus incanus at Castelvolturno Summer growth
Winter growth
0.376 0.922 0.561
0.002 0.011 0.019
0.059
0.000
Shoot length (cm) Number of leaves per shoot Number of leaves per shoot/shoot length (n cmÿ1) Leaf area (mm2) Signi®cance (P-values) of ANOVA.
®cant dierences were reported when the same parameters were measured in winter (Table 2). Transverse sections of winter and summer leaves also showed dierences in their anatomy. Winter leaves were ¯at, while summer leaves had a crimped lamina which was partially rolled to form several crypts in the lower surface (Fig. 2A, C). Lamina thickness was not uniform either in summer or winter leaves (Figs 2 and 3): signi®cant dierences were found between the minimum and maximum distance between the upper and lower epidermis of each section in both kinds of leaves. Within each leaf, the variation in thickness (ratio between maximum and minimum widths) was signi®cantly greater in summer than in winter leaves. Therefore, the variation in the lamina thickness of a single leaf was greater in summer leaves. Upper epidermal cells were much larger in winter than in summer leaves (Fig. 2B). The palisade parenchyma was signi®cantly thicker in winter (84 mm) than in summer leaves (53 mm). However, in summer leaves the palisade tissue was often present on both sides of the lamina (Fig. 2E) and the mesophyll cells were generally smaller with reduced intercellular spaces. As a result, the whole structure was more compact. Moreover, in summer leaves, single palisade cells often had undulating walls forming inward and outward folds alternately (Fig. 2E). Both leaf surfaces were covered by a thick layer of white trichomesÐstellate hairs consisting of a stalk and eight-18 long branches. In both kinds of leaves there were signi®cantly more trichomes on the lower than on the upper surface (Fig. 4). However, trichome density was much higher in summer than in winter leaves. In both kinds of leaves, stomata were present only on the lower surface (Fig. 2), being uniformly distributed along the lower epidermis of winter leaves but found almost exclusively in the crypts of summer leaves (Figs 2F and 5).
DISCUSSION Xerophytes are dry habitat plants with transpiration decreasing to a minimum under conditions of water de®cit (Maximov, 1931). Certain tissues of xerophytes, particularly leaf tissues, become altered structurally in relation to the environment, and plant survival depends upon the ability to withstand desiccation without permanent injury (Shields, 1950).
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Seasonal dimorphism has been reported to be an adaptive strategy to the seasonal climatic changes occurring in Mediterranean habitats (Orshan, 1964, 1972; Christodoulakis, 1989; Christodoulakis et al., 1990; Kyparissis and Manetas, 1993b; Kyparissis et al., 1997). We have described this habit for C. incanus at Castelvolturno, suggesting that the species is well adapted to the rhythmic ¯uctuation of the Mediterranean climate. Development of brachyblasts in summer and dolichoblasts in winter is reported for other Cistus species (Floret et al., 1989). In C. incanus, most of the growth in terms of shoot length, number of leaves and leaf 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 factors aect plant growth and biometric parameters dier signi®cantly among individuals. Steep leaf inclination has been described for many species in dierent environments and interpreted as a strategy to reduce the amount of direct solar radiation, resulting in lower leaf temperature and transpiration rates, and avoidance of damage to the photosynthetic apparatus (Miller, 1967; Mooney et al., 1977; Comstock and Mahall, 1985; He et al., 1996; Gratani and Bombelli, 1999; Werner et al., 1999). Erect summer leaves of C. incanus maximize light interception in the early morning and late afternoon, keeping noon interception to a minimum. This allows the species to tolerate very hot environments by physically evading the midday sun. By contrast, during autumn, winter and spring, when drought is not a limiting environmental factor, horizontal leaves optimize direct solar radiation. Dierent leaf inclination in summer and winter was also reported for C. incanus by Gratani and Bombelli (1999). We suggest that the occurrence of vertical leaves in summer and horizontal leaves in winter is a strategy that evolved in C. incanus to obtain the best advantage from solar radiation in both seasons. This dual adaptation is also corroborated by leaf anatomy: summer leaves frequently have a palisade layer under both epidermises while winter leaves have a typical dorsiventral structure. The presence of a palisade layer on both leaf surfaces, together with a mesophyll composed of smaller cells and reduced intercellular spaces, is reported to be characteristic of xerophytic species (Shields, 1950). These traits are found in summer leaves of C. incanus but not in winter ones which show longer palisade cells only under the upper epidermis, together with wider intercellular spaces. The occurrence of anatomical dierences between summer and winter leaves is in agreement with reports for other seasonal dimorphic species (Christodoulakis, 1989; Christodoulakis et al., 1990; Kyparissis and Manetas, 1993a). Moreover, a lower mesophyll cell density and larger intercellular spaces compared to the sclerophyllous Phillyrea latifolia and Quercus ilex were reported for leaves of C. incanus sampled in October (Gratani and Bombelli, 1999). In summer leaves of C. incanus, we observed palisade cells with involuted walls. This anatomical feature is well known in some evergreen conifers and is reported in Caesalpinioid legumes (Curtis et al., 1996). Although their real function has not yet been ascertained, it has been
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Aronne and De MiccoÐSeasonal Dimorphism in Cistus incanus L.
F I G . 2. Light microscope view of cross-sections of C. incanus winter leaves (A, B), and summer leaves (C±F). E, Large epidermal cells; t, fragments of the numerous trichomes; c, crypt; s, stomata (s). Bars 100 mm.
Aronne and De MiccoÐSeasonal Dimorphism in Cistus incanus L.
Lamina thickness (µm)
300 250 200 150 100 50 0 SL
WL
F I G . 3. Mean values and s.d. of minimum (F) and maximum (h) thickness of the lamina in summer (SL) and winter (WL) leaves of C. incanus.
Trichomes (n mm1)
12 10 8 6 4 2 0 SL
WL
F I G . 4. Number of trichomes found along leaf sections of both lower (F) and upper (h) surfaces. Mean values and s.d. are reported for summer (SL) and winter (WL) leaves.
Stomata (n mmÐ1)
10
8
6
4
2
0 WL
SL-out
SL-in
F I G . 5. Mean number and s.d. of stomata found along leaf sections of winter leaves (WL) and summer leaves outside the crypt (SL-out) and inside the crypt (SL-in).
speculated that they are an important anatomical adaptation to periodic drought. Under water stress these cells should lose water and shrink, reducing the thickness of the entire leaf. When water becomes available again, they might quickly enlarge, causing the leaf to expand in thickness (Curtis et al., 1996). Light intensity is also decreased by the hairy covering of leaves, which is thicker during the season of greatest solar
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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 favourable 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 than in winter leaves, suggesting the occurrence of two levels of leaf xeromorphism. 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 ¯at structure of the lamina is characteristic of mesomorphic 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 (Ehleringer and Comstock, 1987; Kyparissis and Manetas, 1993a; Gratani and Bombelli, 1999). We have shown that C. incanus develops ¯at leaves in winter and folded leaves, with wider variation in lamina thickness, in summer. Therefore, leaf structure is optimized according to seasonal environmental changes occurring in the Mediterranean. Stomatal distribution is dierent between the two leaf types. Stomata are uniformly distributed on the lower surface of the ¯at winter leaves, whereas they are concentrated in the crypts of summer leaves to reduce evapotranspiration, 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 Mediterranean species Nerium oleander L. and Rosmarinus ocinalis L. (Strasburger et al., 1982). In C. incanus, large epidermal cells of winter leaves would support the populations during occasional periods of winter drought. In Mediterranean environments, perennial species are either sclerophyllous, summer deciduous, or seasonally dimorphic (Margaris, 1981). According to Orshan (1964, 1972), the latter is an adaptation to summer drought. Christodoulakis et al. (1990) described seasonal dimorphism for Sarcopoterium spinosum as a major strategy which produces `seasonally dierent plants' from the same individual, that can successfully stand the variety of unfavourable Mediterranean conditions. The overall consideration of phenology, morphology and leaf anatomy of C. incanus is in agreement with the conclusion by Christodoulakis et al. (1990). We suggest that C. incanus has evolved two dierent
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forms, one more mesophytic, the other more xerophytic, to optimize adaptation to the seasonal ¯uctuation of environmental conditions throughout the year.
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