Photoprotective Responses to Winter Stress in Evergreen Mediterranean Ecosystems

Abstract: The role of antioxidants and regulation of photosynthesis as photoprotective adaptations of Mediterranean vegetation to winter stress have been studied. These mechanisms are influenced by the degree of environmental stress (studied at different altitudes) and the taxonomic origin of each species. Thus, antioxidant composition was species-dependent, but not apparently affected by altitude; while the reductions in photochemical efficiency, associated with the presence of zeaxanthin and a lower chlorophyll content, were common among species with increasing altitude. Three different strategies to cope with winter stress were observed in Mediterranean evergreens. First, in Buxus sempervirens antioxidant concentration was very high and the photochemical efficiency was much reduced, with a large accumulation of zeaxanthin. Second, in other Mediterranean sclerophylls, reversible reductions of PSII efficiency related to activity of the xanthophyll cycle allowed day to day adaptation of photosynthetic rates. Third, the summer semideciduous Cistus species maintained a high photochemical efficiency and accumulated little antioxidant, and this strategy could be justified by the occurrence two leaf populations with different physiological tolerances to environmental stress.     

Stimulated growth rate by restriction of P availability at moderate salinity but insensitive to P availability at high salinity in Crithmum maritimum

The halophyte Crithmum maritimum thrives in cracks of calcareous rocks or cliffs at seashores, a situation which associates limited phosphorus availability and high salinity. In order to understand the common patterns of colonization and zonation of this species, seedlings were cultivated for 34 d in inert sandy soil irrigated with a nutrient solution containing or not phosphorus at moderate (50 mM) or high (250 mM) NaCl level. Net assimilation rate and consequently relative growth rate increased in response to P deprivation at moderate saline level, but not at high salinity level. Parallelly, CO2 fixation rate, rubisco capacity, transpiration rate and stomatal conductance were diminished by P deprivation at moderate NaCl level. Intercellular CO2 concentration was therefore not affected. Chlororophyll fluorescence analysis revealed that photosynthetic systems were insensitive to change in P availability at moderate salinity level: neither pigment content, nor effective and maximum quantum yield, photochemical and non photochemical quenching, and electron transport rate were affected by P deprivation. On the contrary, at high salinity level when net photosynthesis, rubisco capacity and the quantum yields of PS2 were severely affected, P deprivation strongly augmented electron transport rate. Stomatal aperture and more modest increase in net photosynthesis, rubisco capacity, photosystem II effective quantum yield and photochemical quenching accompanied this response. This study shows the tolerance of C. maritimum to the phosphorus deprivation combined to moderate or to high saline level which may explain the common patterns of colonization and zonation of this species.     

Photosynthetic acclimation to solar UV radiation of marine red algae from the warm-temperate coast of southern Spain: A review

A review is presented of the physiological mechanisms developed bybenthic macroalgae to cope with deleterious wavelengths, particularly UVradiation. Photoinhibition of photosynthesis, is a photoprotectivemechanism in various species studied in southern Spain. Incubations inoutdoor systems and transplantation experiments under natural radiationallowed to led to understanding of some the photoprotective strategies usedby red algae. Under conditions of enhanced UV-B radiation, algae inshallow sites show marked photoinhibition and rapid recovery ofphotosynthesis (dynamic photoinhibition), whereas algae from deeperlocations can suffer photodamage (chronic photoinhibition). Theexpression of this photoprotective strategy by intertidal species representsan efficient physiological adaptation to tolerate deleterious irradiance, whenlow tides coincide with the onset of solar radiation. Subtidal species canbe also exposed to high doses of UV radiation. This is particularly evidentin clear, Mediterranean waters, where light (including UV-B) can reach to10 m depth. The implications of photoacclimation processes formacroalgal ecology in warm-temperate littorals and the possibleconsequences for outdoor cultivation are outlined in terms of environmentalUV variability.     

Plant species coexistence in cliff habitats

An ecological analysis of the ledge and crevice vegetation of cliffs in north-east Ireland was carried out using a sampling programme based on multivariate land classification. The composition of the vegetation was shown to be determined primarily by distance from the sea, elevation and rock type. The chemical composition and physical structure of the cliffs, together with environmental gradients associated with aspect, elevation and nearness to the sea provide a wide range of habitats in which plants coexist. Certain types of cliff vegetation contained associations of species with a contrasting ecology, such as arctic–montane, maritime, woodland, calcicole and calcifuge plants. The positions of these species in ordination space were found to be unique but overlapping. A model is described to account for these observations. It proposes that species dominance in cliff habitats is prevented by factors such as physical disturbance and that plants are able to coexist in cliff habitats which meet their common environmental tolerances and preferences. The model predicts that cliff habitats with the greatest diversity of species are likely to be subject to less extremes of environmental variability. These habitats include inland sites with nutrient enrichment by sea spray, north-facing sites, seepage sites, base-rich sites, low elevation sites and sites with a heterogeneous physical structure.     

Patterns of spatio-temporal distribution of winter chronic photoinhibition in leaves of three evergreen Mediterranean species with contrasting acclimation responses

High irradiance and relatively low temperature, which characterize Mediterranean winters, cause chilling stress in plants. Downregulation of photosynthetic efficiency is a mechanism that allows plants to survive these conditions. This study aims to address whether this process shows a regular spatial pattern across leaf surface or not. Three species (Buxus sempervirens, Cistus albidus and Arctostaphylos uva-ursi) with contrasting responses to winter stress were studied. During 7 days, macro and micro Fv/Fm spatial patterns were monitored by the use of chlorophyll fluorescence imaging techniques. In the field, the strongest photoinhibition was found in B. sempervirens, while there was almost no chronic photoinhibition in C. albidus. In leaves of the first species, Fv/Fm decreased from base to tip while in C. albidus it was uniform over the leaf lamina. An intermediate behavior is shown by A. uva-ursi leaves. Spatial heterogeneity distribution of Fv/Fm was found inside the leaves, resulting in greater Fv/Fm values in the inner layers than in the outer ones. Neither xanthophyll-linked downregulation of Fv/Fm nor protein remobilization were the reasons for such spatial patterns since pigment composition and nitrogen content did not reveal tip-base differences. During recovery from winter, photoinhibition changes occurred in Fv/Fm, pigments and chloroplast ultrastructure. This work shows for the first time that irrespective of physiological mechanisms responsible for development of winter photoinhibition, there is an acclimation response with strong spatio-temporal variability at leaf level in some species. This observation should be taken into account when modeling or scaling up photosynthetic responses.     

Clustering of halophytic species from Cyprus based on ionic contents

This paper presents the work conducted on the chemical constituents of some common and widely distributed halophyte taxa from Cyprus with the aim that these studies will help in the evaluation of halophytes for different economical purposes. The plant species of Crithmum maritimum L., Limbarda crithmoides (L.) Dumort, Atriplex portulacoides L., Salsola kali L., Atriplex halimus L., Limonium oleifolium Mill., L. meyeri (Boiss.) Kuntze; and Tetraena alba (L.f.) Beier & Thulin were collected in the middle of July. The shoot tissue and leaf samples were collected from the natural habitats and left for drying under air circulation followed by placing them in oven at 60 °C for 96 hours. The material was crushed using mortar and pestle and subjected to an analysis of macro- and micro-nutrients and biochemical compounds. K⁺/Na⁺ in the leaf tissues of the dicot species showed relatively high values depicting their behavior as Na+ includes but very low Cl- levels were recorded. Out of the species investigated here in 4 TFAA content was rather high. Values ranging from 0.5% to 1% dry weight were exhibited in one species. However, only 3 species showed very low TFAA values. Later may be due to low nitrogen availability in their environment. The phenetic analyses of eight halophyte species performed on the data matrix using Ntsys-pc program version 2.1 revealed that, cluster analysis of the overall results obtained here leads to 2 clusters. This discrimination appears to be as a result of their different abilities to accumulate either proline or glycine betaine.     

Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought

The adaptive strategies to high radiation and water stress of the drought tolerant evergreen sclerophylls Quercus coccifera and Arbutus unedo are compared to those of the semi-deciduous Cistus spp. (C. albidus and C. monspeliensis). Cistus spp. partially avoided drought by a marked reduction of their transpirational surface through leaf abscission during summer, when predawn water potential declined below -5.5 MPa. Chlorophyll fluorescence measurements revealed a reversible diurnal decrease of maximum photochemical efficiency of PSII (F_v/F_m), which became more accentuated during summer drought in all species. An important strategy to avoid damage by excessive radiation levels in Cistus spp. was the structural regulation of light interception through leaf angle changes, from a more horizontal orientation in spring (< 35°) to a more vertical orientation in summer (> 70°). Horizontal orientated leaves were highly susceptible to photoinhibition, and excessive radiation often resulted in irreversible photodamage followed by leaf abscission during summer, whereas vertical leaf orientation appeared to protect the leaf from severe photoinhibition. Still, these mechanisms were not fully successful in avoiding chronic photoinhibition, and predawn F_v/F_m values remained low in Cistus spp. during summer (only exhibiting a partial overnight recovery). Evergreen sclerophylls were less susceptible to photoinhibition, and the diurnal decline in F_v/F_m remained fully reversible during drought. Structural regulation of light interception was not found to be an important strategy in these species, and only small, though significant changes in leaf angle occurred. The ecological importance of the adaptive strategies of each functional group is discussed.     

Seasonal Patterns of Photosystem 2 Photochemical Efficiency in Evergreen Sclerophylls and Drought Semi-Deciduous Shrubs under Mediterranean Field Conditions

Photochemical efficiency of photosystem 2 (PS2), assessed from in situ chlorophyll (Chl) fluorescence measurements, was seasonally monitored in five evergreen sclerophyll and five malacophyllous drought semi-deciduous species, co-occurring in the same Mediterranean field site. In evergreen sclerophylls, a considerable drop in the variable (F_v) to maximum (F_m) Chl fluorescence ratio coincided with the lowest winter temperatures, indicating low PS2 efficiency during this period. Summer drought caused a comparatively slight decrease in F_v/F_m and only in three of the five evergreen sclerophyll species tested. In drought semi-deciduous shrubs, the winter drop in F_v/F_m was much less conspicuous. During the summer, and in spite of the severe and prolonged desiccation of their malacophyllous leaves, F_v/F_m was maintained high and only in one species the PS2 efficiency was transiently suppressed, when the leaf relative water content became lower than 30 %. Thus evergreen sclerophylls are more prone to photoinhibition by low winter temperatures, while the sensitivity of drought semi-deciduals depends on the extent and duration of summer drought. This revised version was published online in September 2006 with corrections to the Cover Date.     

Full light and soil drought constrain plant growth in Mediterranean cliffs: the case of Primula palinuri Petagna

In any biogeographical region, cliffs shelter a larger number of relict species than do the surrounding areas. To develop effective conservation strategies, experimental studies are needed. We focused on Mediterranean coastal cliffs and on Primula palinuri Petagna, an endangered narrow-endemic plant, included in the IUCN Red List and chosen as a key species. The hypothesis was that light intensity and soil water availability could affect survival and growth of juvenile plants. To avoid the bias of other cliff environmental factors and to overcome problems of cliff site inaccessibility, we performed an ex-situ experiment. The effect of two light regimes and two soil water availability conditions on survival and morpho-functional traits were analysed. Plants grown under reduced light intensity and wet soil showed no reduction in survival and performed very well in terms of growth and storage accumulation. By contrast, full light and dry soil proved to be detrimental conditions. Overall results suggested that cliff environmental conditions play an important role in conservation of narrow-endemic species. The decreasing trend of the already severely fragmented populations of P. palinuri and the ongoing increasing aridity is likely to contribute to a further reduction of the already narrow distribution this cliff relict species.     

Leaf traits and water relations of 12 evergreen species in Costa Rican wet and dry forests: patterns of intra-specific variation across forests and seasons

This study examined variation in leaf traits and water relations in 12 evergreen and semideciduous woody species that occur in both seasonal wet and dry forests in Costa Rica and compared intra-specific leaf–trait correlations to those found in inter-specific global studies. The following traits were measured in both forests across seasons for 2 years: leaf nitrogen (N), leaf carbon (C), specific leaf area (SLA), toughness, cuticle thickness, leaf thickness, and leaf lifespan (LLS). Leaf water potential (LWP) and water content (LWC) were measured as indices of plant available water. Canopy openness, soil moisture, and herbivory were also measured to compare environmental variation across sites. Although species contributed the greatest amount to variation in traits, season, forest, and their interaction had a large influence on patterns of intra-specific leaf–trait variation. Leaf traits that contributed most to variation across sites were C, LWP, leaf thickness, and SLA. Traits that contributed most to variation across seasons were leaf toughness, LWP, and LWC. Furthermore, leaf traits were more correlated (i.e., number and strength of correlations) in the dry than in the wet forest. In contrast to results from global literature syntheses, there was no correlation between LLS and N, or LLS and SLA. Both light and water availability vary seasonally and may be causing variation in a number of leaf traits, specifically those that relate to water relations and leaf economics. Strong seasonality may cause leaf–trait relationships at the local scale to differ from those documented in continental and global-scale studies.     

Chemical intra-Mediterranean variation and insecticidal activity of Crithmum maritimum

The chemical composition of the volatile metabolites of Crithmum maritimum harvested from several geographic localities along the Mediterranean coasts was studied by GC and GC-MSD. The major oil constituents were found to be dillapiole, gamma-terpinene, sabinene, limonene and beta-phellandrene. The Western populations were richer in dillapiole, whereas the Southern collections were characterized by increased amounts of thymol methyl ether and gamma-terpinene. The Italian chemical profiles differentiated by the significant contributions of carvacrol methyl ether and isoterpinolene. The essential oils were also investigated for their insecticidal activity and their repellency against Pheidole pallidula (Nylander) ants and found to possess significant activity.     

Patterns of nitrate reductase activity vary according to the plant functional group in a Mediterranean maquis

Since little is known about how the Mediterranean Basin ecosystems are affected by nitrogen deposition, we aimed to understand the use of nitrogen by distinct plant functional groups (PFG: summer semi-deciduous and evergreen sclerophylls) present in the Mediterranean maquis in order to assess which may be more affected by changes in nitrogen availability. The availability of soil inorganic nitrogen, leaf nitrate concentrations and nitrate reductase activity (in vivo and in vitro) were measured during the year in three plant species from each PFG. The patterns of in vitro NRA along the shoot and through the day were also determined. Although summer semi deciduous species occupied soil patches richer in nitrate, their leaf NRA were significantly lower than that of evergreen sclerophylls species. The pattern of nitrate and ammonium availabilities along the year also distinguished the PFG. Results show that each PFG is composed of a number of physiologically similar species. Patterns of NRA varied according to the PFG, which may represent distinct specializations of co-occurring species to access nitrogen. Therefore, the NRA can be used as an indicator of the nitrate availability taking into consideration the time of the year, the plant species and its PFG.     

Multi-scale comparisons of cliff vegetation in Colorado

We developed a nested vegetation sampling protocol to sample the plant diversity on south-facing cliffs and cliff bases in Jefferson County, Colorado. The multi-scale plots included three nested spatial scales, 1 m², 20 m², and 40 m². We compared plant species richness and species diversity among large cliffs, medium cliffs, small cliffs, and non-cliff sites using Hill's diversity numbers (N ₀, N ₁, and N ₂) for the 1-m² quadrats. Species richness (N ₀) was calculated for the 20-m² and 40-m² plots. Our results indicate that plant species diversity on the cliff faces did not increase with increasing cliff area. This pattern was consistent at all three sampling scales. A model selection was run to determine if plant species diversity values on the cliff faces were associated with cliff variables. None of the cliff variables measured were good predictors of diversity at the 1-m² scale. However, at the 20-m² scale, canyon differences and a positive relationship with increasing cliff surface roughness explained 70% of the variability in species richness. Although most plant species sampled on the cliff faces were also found in the base plots, 13 species were sampled only on the cliff faces. Additionally, dry south facing cliffs support a mix of xeric and mesic plants indicating that cliffs may provide unique microenvironments for plant establishment. This revised version was published online in August 2006 with corrections to the Cover Date.     

The phytosociology of British sea-cliff vegetation with special reference to the ecophysiology of some maritime cliff plants

The major factors thought to control the distribution of associations on the sea cliffs in Britain are discussed in relation to the zonation of cliff vegetation, and some experiments to investigate the effects of these factors are described.The seeds of the maritime cliff species are able to germinate in higher salinities than those of closely related inland species.Relative growth rates of maritime cliff species indicate stimulation at low salinities over non-saline conditions, and less reduction in growth at higher salinities than those of closely related inland species.Increasing salinity reduces both photosynthesis and dark respiration in Lavatera arborea. Mesophyll and stomatal resistances are increased while transpiration is reduced.The distribution of ions within Lavatera arborea grown at different salinities indicates differential accumulation between young leaves, old leaves and roots.Nomenclature follows Clapham, Tutin & Warburg (1962).     

Comparative protective strategies of Cistus albidus and Quercus ilex facing photoinhibitory winter conditions

The role of structural photoprotection under photoinhibitory winter conditions was evaluated in two Mediterranean woody species: Cistus albidus (semideciduous) and Quercus ilex (evergreen). Shoots were manipulated in order to modify the light load naturally received by the leaves throughout the cold season, and monitored for changes in maximum photochemical efficiency of PSII, phenology, and leaf morphology. Naturally steep leaves of C. albidus were restrained to a horizontal position, and compared with control leaves (naturally horizontal, or steeply inclined). Fully exposed leaves of Q. ilex were artificially protected through partial shading, and compared with control leaves (not shaded). During the cold season, the most exposed (either naturally or artificially) leaves were always more photoinhibited (had lower maximal photochemical efficiency of PSII) than the photoprotected ones. The differences disappeared at the beginning of spring. Winter photoinhibition was not more pronounced in older than in younger leaves of C. albidus, indicating that inclination rather than age affected their photochemical efficiency. Leaf chlorophyll contents were not significantly affected by the manipulations. Leaf thickness decreased slightly in the least exposed shoots of the evergreen species, but no changes were detected in leaf morphological traits of the semideciduous one. The increased photoinhibitory pressure led only to slight and non-significant changes in phenology and growth.     

树锦鸡儿、柠条锦鸡儿、小叶锦鸡儿和鹰嘴豆干旱适应能力比较

对1年生豆科作物鹰嘴豆Rupali品种和Almaz品种以及多年生植物树锦鸡儿、柠条锦鸡儿和小叶锦鸡儿叶相对含水量和叶水势对逐渐干旱胁迫的响应进行了分析,比较了两类植物的干旱适应能力。结果表明鹰嘴豆叶相对含水量随叶水势的下降线性下降,树锦鸡儿、柠条锦鸡儿和小叶锦鸡儿叶相对含水量在叶水势分别下降到-2.4MPa、-2.5MPa和-1.5 MPa之前没有下降,之后随水势的下降线性下降。树锦鸡儿、柠条锦鸡儿和小叶锦鸡儿这种叶相对含水量下降的滞后性表明该类植物叶具有较硬而弹性较差的细胞壁,使得植物在干旱胁迫下叶具有良好的保水能力。鹰嘴豆叶具有的最低水势为-4.5MPa,对应的土壤相对含水量为14％,锦鸡儿植物叶具有的最低水势可达-6.7MPa,对应的土壤相对含水量为6％,说明锦鸡儿植物比鹰嘴豆具有更好的干旱适应能力,这种能力可能取决于锦鸡儿植物体内大量渗透调节物质的累积。     

Are Sclerophylls and Malacophylls Hydraulically Different?

This work tests the hypothesis that sclerophylls (i.e. hard-leaved species) would be less efficient than malacophylls (i.e. soft-leaved species) in terms of water transport through the stem as well as within the leaf blade. Mean leaf surface area (A_L), leaf specific mass (LSM) as well as shoot (K_WL), stem (K_SL) and leaf (K_LL) hydraulic conductances were measured in eight Mediterranean evergreen sclerophylls and eight temperate deciduous malacophylls. No difference was observed between the two groups in terms of K_LL and of the contribution of leaves to the overall shoot hydraulic resistance. Leaves represented in all cases 48 to 90 % of the shoot hydraulic resistance, suggesting that the sclerophyllous habitus does not per se lead to low efficiency in water transport within the leaf blade. A weak negative relationship (r² = 0.252) appeared to exist between K_SL and LSM. This might provide an explanation for the lower growth rates of sclerophylls with respect to malacophylls.     

喜光榕树和耐荫榕树光适应机制的差异

100%和36%光强下生长的喜光的斜叶榕的光合能力高于耐荫的假斜叶榕,而热耗散能力与之相似,说明强光下斜叶榕主要通过光合作用利用光能和热耗散、假斜叶榕主要通过热耗散防御光破坏.100%光强下生长的两种榕树的日间光抑制程度相似,但叶表光强相同情况下各光强下生长的假斜叶榕的光抑制均比斜叶榕严重.100%光强下假斜叶榕叶片悬挂角大于斜叶榕,导致日间叶表光强低于斜叶榕,这可能是两种榕树日间光抑制程度相似的原因,表明叶片悬挂角的适应变化对假斜叶榕有重要的意义.     

A New Coastal Species of Limonium (Plumbaginaceae) from Southeastern Spain

A new species, Limonium scopulorum (Plumbaginaceae), is described from the maritime cliffs of Alicante province, Spain (southeastern part of the Iberian Peninsula). This new taxon belongs to the group of Limonium delicatulum, which is highly diversified in the Mediterranean territories of the Iberian Peninsula. It is related to the Balearic species L. biflorum, though several leaf, floral and chromosomal features warrant its easy recognition. Molecular divergence, shown in previous studies, also supports its separate treatment. Major affinities and differences with other related taxa are discussed. Moreover, morphological, ecological, chorological, biogeographic features of the new taxon are discussed, and its conservation status is reported. An identification key is provided for Spanish taxa of the Limonium delicatulum group.     

Environmental factors affecting patterns of distribution and co‐occurrence of two competing raptor species

Habitat selection is a complex process, that is affected by several factors, including habitat characteristics, environmental conditions, and both intra‐ and interspecific interactions. We analysed habitat preferences of two top avian predators, Peregrine Falcon Falco peregrinus, a medium‐sized diurnal raptor, and Eagle Owl Bubo bubo, a large nocturnal raptor. These two species are known to compete for preferred nest‐sites, and proximity to cliffs with Eagle Owls may reduce Peregrine breeding output through predation of young Falcons. We investigated the environmental factors affecting occurrence and coexistence of the two species and the potential role of habitat suitability in favouring co‐occurrence in 3519 km² of the central pre‐Alps of Italy, where the two species breed on cliffs and sometimes co‐occur on the same cliff. Peregrines settled on long, steep and favourably orientated cliffs in woodland landscapes close to urban areas. Eagle Owls settled on topographically similar cliffs, but in lower rainfall areas compared with cliffs occupied by Peregrines and cliffs unoccupied by either species. Sites where the two species co‐occurred were characterized by more horizontally extended cliffs compared with sites of exclusive occurrence of each species. An analysis of relative habitat suitability revealed that sites where the two species co‐occurred had the highest predicted probability of occupancy for both species, suggesting that those sites should be regarded as high‐quality sites. Breeding productivity of Eagle Owls was negatively affected by the co‐occurrence of Peregrines, whereas the effect of Eagle Owl proximity on Peregrine productivity varied according to cliff suitability for the Peregrines. Habitat selection had fitness consequences for Eagle Owls because breeding productivity increased with cliff length. Environmental conditions, particularly climatic factors, could allow the widespread coexistence of these competing raptors at the landscape scale, whereas at the local scale co‐occurrence could take place only on larger cliffs. These were preferred sites for both species, presumably because breeding at such sites offsets the costs of settling close to the competitor species.