ISSN 10674136, Russian Journal of Ecology, 2014, Vol. 45, No. 3, pp. 215–222. © Pleiades Publishing, Ltd., 2014. Seasonal Ecophysiology of an Endangered Coastal Species, the Yellowhorned Poppy (Glaucium flavum Crantz)1 J. Cambrollé, S. RedondoGómez, E. MateosNaranjo, T. Luque, and M. E. Figueroa Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, Apartado 1095, 41080 Sevilla, España email: [email protected] Received August 10, 2011 Abstract—Glaucium flavum Crantz. is a shortlived perennial herb distributed in coastal zones from the Black Sea to southern, western and northwestern Europe. Despite its diminishing area of distribution and potential pharmacological value, little is known about the ecophysiological features of this coastal species. We investi gated the photosynthetic performance of G. flavum by measuring gas exchange, chlorophyll fluorescence, photosynthetic pigment concentration and leaf water content over the space of a year in a coastal habitat of SW Spain. We also measured the variation in total concentrations of nitrogen, phosphorus, sulphur, potas sium, calcium and magnesium, in the leaves and soil, throughout the study period. G. flavum showed a high resistance to summer drought conditions which appeared to be due to the high degree of stomatal control. The potential photochemical efficiency of photosystem II showed minimum values during the winter, indi cating that low temperatures can produce negative effects within the photosynthetic apparatus. However, the marked decline in net photosynthesis during the winter seems to be mainly related to a loss of metabolic activ ity. Although leaf nutrient concentrations were, in general, within the normal ranges, phosphorus availability seems to be limited by the high calcium concentrations detected in the soil of the study site. Our study points out the efficiency of the different physiological adaptations of this rare and endangered coastal species in cop ing with the strong seasonal variability of the Mediterranean climate. Keywords: ecophysiology, coastal flora, Glaucium flavum, photosynthesis, nutrients DOI: 10.1134/S1067413614030023 INTRODUCTION In most of its distribution area, G. flavum is subject The yellow horned poppy, Glaucium flavum to the strong seasonal effects of the Mediterranean cli Crantz., is a shortlived latexbearing perennial herb. mate. This climate offers contrasting challenges for It is found mainly in calcareous soils on sand dunes, plant growth that oscillate between hot, arid summers cliffs and shingle beaches from the Black Sea through with high irradiance and cool winters with irregular southern and western to northwestern Europe (Scott, rainfall and episodic frosts (Figueroa et al., 1997). The 1963). Like many other plants of the family Papaver flora of coastal dunes, shingle and rocky beaches are aceae, G. flavum contains benzylisoquinoline alka also exposed to other adverse physical conditions, loids, some of which have therapeutic properties (Kint such as the influence of saltspray, lack of fresh water surashvili and Vachnadze, 2000). At present, G. flavum and/or nutrient scarcity (Packham and Willis, 1997). is included in various IUCN categories in certain parts Although recent studies under greenhouse conditions of its distribution area (e.g. ‘Critically Endangered’ in have indicated the high tolerance of G. flavum to certain Norway and ‘Endangered’ in Romania), and several potential stress factors (Cambrollé et al., 2011a, b), little authors have reported the retreat of its populations in is known about the ecophysiology of this coastal spe many parts of Europe (e.g. Rappé, 1984; Prieto et al., cies in its natural habitat. The clear lack of information 2007; Solås et al., 2007). about the effects of environmental conditions on the performance of G. flavum and the cited reduction of its 1 The article is published in the original. distribution area highlight the need to expand the Abbreviations: A, net photosynthetic rate; Chl a+b, chlorophyll a knowledge about this Mediterranean coastal species. and chlorophyll b; Ci, intercellular CO concentration; Cx+c, 2 The aim of this work was to describe the ecophysi carotenoids; F0, minimal fluorescence level in the darkadapted state; Fm, maximal fluorescence level in the darkadapted state; ological features of G. flavum under natural condi Fs, steady state fluorescence yield; Fv, variable fluorescence level tions. For this purpose, levels of gaseous exchange, in the darkadapted state; Fv/Fm, maximum quantum efficiency chlorophyll fluorescence, photosynthetic pigments, of PSII photochemistry; ΦPSII, quantum efficiency of PSII; Gs, stomatal conductance; LWC, leaf water content; NPQ, nonpho leaf water content, and both foliar and soil concentra tochemical quenching; RGR, relative growth rate. tions of nitrogen, phosphorus, sulphur, potassium, 215 216 CAMBROLLÉ et al. Physicochemical properties of soil at the study site. Values from June to July, when practically no rain fell and represent mean ±SE, n = 5 mean monthly temperatures reached maximum val ues. Winter was relatively wet, and the lowest temper Parameter Soil atures were reached in this period. Ecophysiological measurements were always car Gravel, % 38 ± 6 ried out on the same plants selected from the study Medium and coarse sand, % 62 ± 8 site, and were taken on young rosette leaves of the same orientation relative to the light, to avoid effects Fine sand, silt and clay, % 4 ± 2 of microclimatic variation. Measurements were taken from January to December 2007 with twelve sampling pH 8.4 ± 0.03 dates, one in the middle of each month, in order to –1 study the photosynthetic performance and nutrient Conductivity, mS cm 0.16 ± 0.02 status of the plant in response to the strong seasonal variability of the Mediterranean climate. calcium and magnesium were assessed monthly over the course of a year in a typical coastal habitat of SW Gas Exchange Spain. Gas exchange measurements were taken monthly from the fully developed leaves of 10 plants randomly chosen in the field (n = 20, two measurements per MATERIAL AND METHODS plant), using an infrared gas analyzer in an open sys Study Area and Sampling Procedures tem (LI–6400, LI–COR Inc., Neb., USA). All mea surements were taken at the same time of day, between The study was conducted in the joint estuary of the 10 a.m. and 11 a.m., to eliminate any possible diurnal Odiel and Tinto rivers in Huelva, on the Atlantic coast variation. Net photosynthetic rate (A), intercellular of SW Spain (37°15′ N, 6°58′ W). The study site is a CO2 concentration (Ci) and stomatal conductance of sand dune spit with gravel and calcareous shell deposits, CO2 (Gs) were determined at ambient CO2 concentra which was selected as it supports one of the few existing tion of 365 μmol mol–1, temperature of 20/25°C, populations of Glaucium flavum in southwestern Spain. 50 ± 5% relative humidity and photon flux density of –2 –1 The physicochemical properties of the soil are given in 1000 μmol m s A, Ci and Gs were calculated using Table 1. The climate is Mediterranean with an Atlantic the standard formulae of Von Caemmerer and Farqu influence (Marine Mediterranean Climate). Data for har (1981). monthly rainfall and mean monthly temperature were obtained from the Huelva (Ronda Este) Meteorologi cal Station located next to the study site (Fig. 1). Dur Leaf Water Content ing the experimental period, the climatic conditions Leaf water content (LWC) of fully expanded rosette were typical of the region: a summer drought occurred leaves from each plant (n = 20, two leaves per plant) was calculated every month as: LWC = (FW – DW)/FW × 100, 50 100 where FW is the fresh mass of the leaves, and DW is the dry mass after ovendrying at 80°C for 48 h (Medrano 40 80 and Flexas, 2004). Leaves were collected in the field, at the same time as gaseous exchange measurements 30 60 were taken, and immediately transferred to the labora tory, where samples were processed. 20 40 Rainfall, mm Chlorophyll Fluorescence and Photosynthetic Pigments Temperature, °C 10 20 Chlorophyll fluorescence was measured monthly 0 0 in the field in the same 10 plants, in randomly chosen, fully expanded leaves (n = 20, two measurements per July May June plant) using a portable modulated fluorimeter (FMS2, April March August Hansatech Instrument Ltd., England). Light and January October February darkadapted fluorescence parameters were measured December November September μ –2 –1 Time, month at dawn (stable, 50 mol m s ambient light) and at midday (1600 μmol m–2 s–1) according to the method Fig. 1. Monthly rainfall (mm) (᭿) and mean monthly tem ology used by Cambrollé et al. (2011a). The following perature (°C) (᭹) at the Huelva (Ronda Este) Meteorolog parameters were calculated: maximum quantum effi ical Station from January to December 2007. ciency of PSII photochemistry (Fv/Fm), quantum effi RUSSIAN JOURNAL OF ECOLOGY Vol. 45 No. 3 2014 SEASONAL ECOPHYSIOLOGY OF AN ENDANGERED COASTAL SPECIES 217 Φ ciency of PSII ( PSII), and nonphotochemical 20 (a) quenching (NPQ). In each season of the year, fully expanded rosette –1 leaves from each plant (n = 20, two leaves per plant) s 15 –2 were excised and immersed in liquid N2 for transfer to the laboratory. Photosynthetic pigments were 10 mol m extracted according to the methodology used by Cam μ brollé et al. (2011a). Concentrations of pigments A, 5 (chlorophyll a, Chl a; chlorophyll b, Chl b; and caro tenoid, Cx + c) were obtained by calculation, using the method of Lichtenthaler (1987). 0 0.8 (b) Nutrient Analysis –1 s 0.6 Rosette leaf samples, randomly chosen from the –2 population, were collected every two months from January to November 2007 and taken to the laboratory 0.4 (n = 5). In addition, samples from the uppermost 20 cm of soil (corresponding to an average rooting Gs, mol m 0.2 depth of G. flavum) were taken in areas where vegeta tion was absent (n = 5). Leaves were carefully washed 0 with distilled water before any further processing or 350 (c) analysis.