8 Northeastern Naturalist Vol. 16, Special Issue 5 Geobotany and Biogeochemistry of Serpentine Soils of Neyriz, Iran Seyed Majid Ghaderian1,*, Houshang Fattahi1, Ahmad Reza Khosravi2, and Mousa Noghreian3 Abstract - In this study, soils and plants of ultramafic areas of Neyriz, in the south of Iran, were collected, identified, and analyzed for “serpentine” metals. Soil analysis of total element concentrations indicated that maximum total concentrations (μg g-1) of Ni = 1250, Cr = 200, Co = 295, Mn = 1850, Fe = 105,300, Mg = 73,000, and Ca = 2800. The maximum concentration of exchangeable Ni in these soils was of 4.7 μg g-1. During this study, 116 plant species belonging to 30 families were collected and a few species were endemic to ultramafic soils of these areas. Analysis of the plant leaves did not reveal any hyperaccumulators of Ni or any other “serpentine” metals. The highest concentrations of Ni (140 μg g-1) and Co (47 μg g-1) were found in Rheum ribes. The highest concentration of Cr (76 μg g-1) was measured in Nepeta glomerulosa. Introduction Ultramafic (serpentine) soils, are widely distributed in different parts of the world (Brooks 1987). These soils contain high concentrations of Mg and Fe, and relatively high concentrations of total Ni and Cr ranging from 500– 5000 μg g-1 and Co ranging from 110–500 μg g-1 (Reeves and Baker 2000, Reeves et al. 1996). Manganese levels are often a little higher than for many other soil types. Concentrations of N, P, and K are usually low, and the Mg/Ca ratio is high (Proctor 1999). Due to these environmental stresses, the growth forms and physiognomy of some of the plant species growing in these soils can be different from those of plant species in non-serpentine areas. Serpentine soils of the world support some plants that are endemic and restricted to these substrates. Among all morphological changes produced in vegetation by substrates, those found in serpentine floras are probably the most extreme (Brooks 1998); thus, serpentine soils can act as agents of ecotypic selection (Reddy et al. 2001). Serpentine vegetation is often distinctive in physiognomy and includes unusual species and races. However, generalizations about serpentine vegetation are difficult to make due to variability. The number of endemic species in some tropical and subtropical regions, like New Caledonia and Cuba are high (Jaffré 1992, Reeves et al. 1999), while in other regions, such as some parts of Europe and New Zealand, they are lower (Brooks 1998, Reeves 1992a). Endemic plants on serpentine soils 1Department of Biology, Faculty of Sciences, University of Isfahan, Isfahan, Iran. 2Department of Biology, Faculty of Sciences, University of Shiraz, Shiraz, Iran. 3Department of Geology, Faculty of Sciences, University of Isfahan, Isfahan, Iran. *Corresponding author - ghaderian@sci.ui.ac.ir. Soil and Biota of Serpentine: A World View 2009 Northeastern Naturalist 16(Special Issue 5):8–20 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 9 can be important, not only for studies of physiological adaptation and plant speciation, but also for mineral prospecting, as they are indicators of ultramafic rocks and related geologies. Regarding uptake of heavy metals, plants that grow on ultramafic substrates can be divided into “normal” plants and metal hyperaccumulators (Reeves 1992b). Most plants of ultramafic soils are of the former type and show only slightly elevated heavy metal concentrations in shoot dry matter in comparison to those from other soil types. Total concentrations of Ni, Cr, and Co in normal serpentine plants range from 10–100, 5–50, and 2–20 μg g-1, respectively. While most serpentine plants grow on these soils without excess uptake of elements, hyperaccumulators take up more than 1000 μg g-1 Ni, Cr, or Co into their leaf dry matter (Baker and Brooks 1989). To date, about 350 hyperaccumulators of Ni have been identified from serpentine soils, mostly collected from tropical and subtropical countries, with those from Mediterranean areas belonging mainly to the Brassicaceae (Brooks 1998). One case appears to have been recorded of Co hyperaccumulation on serpentine soils (Reeves 2005). In the Cu and Co mineralized soils of southwest Africa, 28 hyperaccumulators of Co were reported (Reeves and Baker 2000). There are a few reports in the literature of plants that have hyperaccumulated Cr (Reeves and Baker 2000, Zhang et al. 2007). The flora of Iran comprises about 8000 plant species, belonging to 150 flowering plant families. Approximately 22% of these species are endemic to the country (Jalili and Jamzad 1999). A very large number of species are found in two phytogeographical regions, the Irano-Turanian region (western to eastern parts of Iran); and the Saharo-Sindian region (the southern part of Iran), where most of Iranian serpentine soils are located. Serpentine soils cover substantial areas of Iran at many locations. These areas are located in the northwest, west, center, northeast, southeast, and south of the country (Fig. 1). Whereas the ultramafic floras in most parts of the world have been described, there is little information available regarding the ultramafics of Iran. Ghaderian and Baker (2007), in a geobotany and biogeochemistry reconnaissance study, described the ultramafics of central Iran. There are scattered and relatively large areas of ultramafics in Neyriz, in the south of Iran, located between the Irano-Turanian and Saharo-Sindian phytogeographical regions. The aim of this study was to document the plants growing on the ultramafic soils of the Neyriz area and to initiate a geobotanical and biogeochemical study to reveal serpentine endemics and metal accumulator plants in these major ultramafic areas in Iran. Field-site Description Neyriz is a town in Fars Province, in the south of Iran, 160 km east of Shiraz. There are several serpentine outcrops in this site located in a 60- km2 area, at 1600–2600 m above sea level, between 29º48′ to 29º54′N, and 53º45′ to 53º55′E (Fig. 1). The climate of Neyriz is semi-dry, with average 10 Northeastern Naturalist Vol. 16, Special Issue 5 Figure 1. Ophiolitic occurrences in Iran (left), and serpentine areas of Neyriz in blue (right). 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 11 annual rainfall about 270 mm, mostly falling in winter and to some extent in autumn and early spring. The daily maximum temperature of this area in late spring and summer reaches 45 ºC,and the daily minimum reaches -5 ºC in late autumn and winter. Mean annual temperature is about 17–18 ºC. Methods Plant collection and analysis During April 2004 to July 2005, plants growing on the Neyriz serpentines were collected for identification and preservation of reference specimens. Taxonomic determinations were based on Rechinger (1963–1997).To determine any Ni hyperaccumulator in the field, leaf fragments from all plant species were screened for Ni accumulation by a semi-quantitative test using filter paper impregnated with dimethylglyoxime (1% solution in ethanol). A negative result generally indicates a Ni concentration of <1000 μg g-1 (Reeves et al. 1999). For the analysis of plant dry matter, leaf materials were washed with double-distilled water and dried at 70 ºC for 48 h. About 300 mg of dry leaf sample was added to a 25-ml beaker and ashed in a muffle furnace for 12 h at 480 ºC. The ash was taken up in 5 ml 10% HNO3, and the digest was finally made up to 10 ml in 10% HNO3. The solutions were analyzed for elemental composition by atomic absorption spectrophotometry (AAS Philips model PU 9100). Soil collection and analysis More than 50 soil samples from 0–15 cm depth near roots of some plants in the serpentine study area were collected for analysis. Soil samples were air-dried and sieved to 2 mm. Sub-samples of 4 g were ground to pass through a 215-μm sieve and oven dried at 70 ºC. A further sub-sample of 0.5 g was transferred to a Kjeldahl digestion tube for extraction with 10 ml of a 3:1 HCl/HNO3 mixture. Tubes were left at room temperature overnight and were then placed in a heating block. Each was covered with an air condenser and refluxed gently at 80 °C for 2 hours. After cooling, the digests were filtered through a moistened Whatman No. 40 filter paper into a 50-ml volumetric flask. Flasks were then made up to volume with distilled water. Analyses for Ni, Cr, Co, Mn, Fe, Mg, and Ca were performed by atomic absorption spectrophotometry (AAS, Philipps model PU 9100). For determination of exchangeable elements, 20 g of air-dry soil sieved to <2 mm were placed in a 100-ml screw-cap polythene bottle, 50 ml of 1M NH4NO3 solution was added, and the suspension shaken for 2 hours at 20 °C in an end-over-end shaker. After shaking, the soil suspensions were left to stand for 5 min, and then filtered (Whatman No. 42 filter paper) into a clean bottle. The filtrate was then acidified to 0.2% HNO3 for analysis of the above elements by AAS. The pH of the soil was determined using a glass electrode after 10 g of soil had been stirred well in 30 ml distilled water in a beaker and allowed to stand for about 30 min. 12 Northeastern Naturalist Vol. 16, Special Issue 5 Results Concentrations of total and exchangeable Ni, Cr, Co, Mn, Fe, Mg, and Ca in representative serpentine soils of Neyriz are shown in Table 1. The maximum concentrations of total metals in the soils were 1250 μg g-1 Ni, 200 μg g-1 Cr, 295 μg g-1 Co, 1850 μg g-1 Mn, 10.53% Fe, and 7.3% Mg. The Mg/Ca quotients were very high with a maximum of 44. The Fe concentrations were high, but the levels of Ni and Co were slightly below the average of the typical ranges, as much higher concentrations have been found elsewhere (Reeves and Baker 2000). Total Ca in the soils was low (<0.28%), as is usual in serpentines. The exchangeable fractions of Ni, Cr, Co, and Mn were low, and their maximum concentrations were 4.7, 0.5, 0.6, and 0.8 μg g-1 , respectively, while the maximum value for Fe was relatively higher (25 μg g-1). Exchangeable proportions of both Ca and Mg in the soils were very high, particularly for Ca. The pH of these soils was circum-neutral to slightly basic, ranging between 6.8–7.7 (Table 1). During the course of our study, 116 species and subspecies of vascular plants were collected from serpentine soils of Neyriz (Appendix 1). The species belong to 86 genera and 30 families. Major plant families represented are Asteraceae (17 species), Lamiaceae (13), Fabaceae (11), Apiaceae (10), Brassicaceae (7), Boraginaceae (6), Caryophyllaceae (6), and Polygonaceae (5). Most plants (97.5%) are herbaceous annuals (therophytes) and perennials (hemicryptophytes or chamaephytes), with 3 tree and shrub species (phanerophytes). Most of the plant species (87%) belonged to the Irano-Turanian phytogeographical region, but there were some (13%) Saharo-sindian and Nubo-Sindian species in this area. The number of Iranian endemic species collected from these serpentine areas is high (40 species). Elemental analysis of leaf dry matter of all the species collected did not reveal any metal hyperaccumulators at these serpentine areas. Appendix 1 shows the concentration of Ni, Cr, Co, Mn, Fe, Mg, and Ca in the collected plant species. Concentrations of Ni in these plants were in the range for non-hyperaccumulators from serpentines (Reeves 1992b). Highest concentrations of Ni in plants were found in Rheum ribes (140 μg g-1), Ferula sp. (89 μg g-1), Colchicum persicum (78 μg g-1), and Polygonum thymifolium Table 1. Means (n = 15) and ranges (in bracket) of total and exchangeable element concentrations (μg g-1), Mg/Ca quotient and pH in serpentine soils of Neyriz, Iran. Element measured Total Exchangeable Ni 1050 (810–1250) 3.8 (2.5–4.7) Cr 145 (90–200) 0.42 (0.3–0.5) Co 230 (165–295) 0.53 (0.4–0.6) Mn 1500 (1125–1850) 0.7 (0.5–0.8) Fe 78,500 (50,700–105,300) 22.3 (18–25) Mg 57,250 (51,100–73,000) 1080 (970–1130) Ca 1850 (1160–2800) 1450 (750–2150) Mg/Ca 31 (23–44) 1.27 (0.52–1.5) pH 7.2 (6.8–7.6) 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 13 (70 μg g-1). In all other plants, Ni was less than 67 μg g-1. Cheilanthes fragrans and Amygdalus scoparia contained the lowest amounts of Ni (6 and 7 μg g-1, respectively). The highest Cr concentrations were in Nepeta glomerulosa (76 μg g-1) and Sinapis arvensis (55 μg g-1). Chromium concentrations were <10 μg g-1 in plants of most species. For Co, Rheum ribes (47 μg g-1) and Centaurea microlonchoides (37 μg g-1) had the highest concentrations, compared to <10 μg g-1 in most other plants. The highest concentration of foliar Mn was in Arnebia decumbens (142 μg g-1). The lowest value recorded was 14 μg Mn g-1. Iron concentrations >1900 μg g-1 were measured in Colchicum persicum (3325 μg g-1), Crepis kotschyana (1995 μg g-1), and Anisosciadium orientale (1940 μg g-1). The lowest Fe concentration was 79 μg g-1 in Buhsea coluteoides. Magnesium concentrations ranged from 32,530 μg g-1 in Rheum ribes to 385 μg g-1 in Haplophyllum bakhteganicum. Diplotaxis hara contained the highest Ca concentration (10,170 μg g-1). The lowest Ca concentration was in Secale cereale (285 μg g-1). Mg/Ca quotients in most plants were <2, the highest and the lowest values were in Rheum ribes (25.2) and Paracaryum persicum (0.2), respectively. Discussion The serpentine soils of Neyriz contained high concentrations of Ni, Co, Mn, Fe, and Mg. These metal concentrations were in the range for typical serpentine soils elsewhere, especially in the wider near-Middle Eastern region (Freitas et al. 2004, Lombini et al. 1998, Shallari et al. 1998, Wenzel and Jockwer 1999). The Mg/Ca quotient for these soils was very high. These Ni concentrations and the high Mg/Ca quotient can provide a stressful environment for growth of most plants (Proctor and Nagy 1992); however, plants growing on serpentine soils may contain some physiological tolerance mechanisms to survive and grow. The overall species number, floral composition, and life spectra of plants growing on the serpentine soils of Neyriz, with few exceptions, are similar to those growing on nearby non-serpentine areas. The number of endemic species for the flora of Iran collected from these areas is high (about 40 species). Two species, Haplophyllum bakhteganicum and Centaurea microlonchoides, were narrow endemics to the Bakhtegan lake area where serpentine soils of Neyriz occurred. The population of Argylobium roseum, growing on serpentine soils of these areas, has dark red-colored leaves. Similarly Polygonum sp. found on the serpentine soils contains some morphological characters that are different from non-serpentine populations. More taxonomical and physiological studies should be done to explore possible differences between serpentine and non-serpentine species. In some parts of the world (most notably the tropics), the number of serpentine endemic plants is generally high. For example, in Cuba there are 920 serpentine endemics (of the total 6375 species) (Reeves et al. 1996, Reeves et al. 1999), and in New Caledonia more than 90% of plants growing over the serpentines are endemic (Jaffrè 1992). In some more temperate areas (e.g., 14 Northeastern Naturalist Vol. 16, Special Issue 5 the UK), however, there may be only one or two endemic species (Brooks 1998). Similarly, in the southern parts of New Zealand, only one endemic serpentine plant has been reported (Reeves 1992b). In serpentine soils of the Polar Urals in arctic Russia, very limited endemism was found (Proctor et al. 2004). Turkey, located at the western border of Iran, is estimated to contain about 100 endemic serpentine plants (Reeves et al. 2001). The few endemic taxa (3.4%) in serpentine soils of Neyriz are the same as those found in serpentines of Central Iran (Ghaderian and Baker 2007). While about 40 species collected from serpentine soils are endemic to Iran, only a few are found exclusively on ultramafic soils. More research is needed to determine whether ecotypes of more widespread species have become locally adapted to these areas. Hyperaccumulators of Ni or other metals were not discovered in this preliminary plant survey. This situation is consistent with studies of other serpentine floras, e.g., New Zealand, where none of the serpentine taxa have been found to be Ni hyperaccumulators (Reeves 1992b). The total number of Ni hyperaccumulator plants discovered to date worldwide is about 350 (Reeves and Baker 2000). Most Ni hyperaccumulators from southern Europe and Anatolia belong to the family Brassicaceae, and most of these are species of the genus Alyssum, which contains more than 50 species of Ni hyperaccumulators (Reeves and Adigüzel 2008). All of the Ni hyperaccumulators in this genus belong to section Odontarrhena (C.A. Meyer) Hooker, in which all species are perennials. Anatolia is the site of maximum Alyssum multiplicity and diversity; most Ni hyperaccumulators of this genus exist in this area, while few are found east of Turkey. The only Ni hyperaccumulators reportedly found in the serpentines of Iran were three Alyssum Ni hyperaccumulators from serpentines of western parts of Iran reported by Ghaderian et al. (2007a, b). In the present work, perennial Alyssum species from section Odontarrhena were not found growing on serpentines of Neyriz. The relatively high concentrations of Ni, Cr, and Co in some plant species in the present work are notable. Rheum ribes contained 140 μg Ni g-1 and some other species contained more than 70 μg Ni g-1, while the amounts of Ni in serpentine plants of central Iran have been reported as much lower (Ghaderian and Baker 2007). The accumulation of Cr and Co by some of the Neyriz species is also of interest. Typical amounts of Cr in Neyriz serpentine plants are relatively high when compared to the concentrations of Cr in the serpentine plants of Goiás, Brazil (Reeves et al. 2007), while the amounts of Cr in the Brazilian serpentine soils were much higher than those of the serpentine soils in Neyriz. Also the concentrations of Co in the plants growing on the serpentines of Neyriz typically were higher than those in the serpentine plants of Goiás. The concentrations of Cr and Co in plants in this study were much higher than those reported from serpentine soils of central Iran (Ghaderian and Baker 2007). Further work is needed on other serpentines in Iran in order to fully document the serpentine flora and investigate the metal-uptake characteristics of its plants. 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 15 Acknowledgments This research was carried out using an M.Sc. grant to H. Fattahi, offered by the Graduate School, University of Isfahan. Literature Cited Baker, A.J.M., and R.R. Brooks. 1989. Terrestrial higher plants which hyperaccumulate metallic elements: A review of their distribution, ecology, and phytochemistry. Biorecovery 1:81–126. Brooks, R.R. 1987. Serpentine and its Vegetation: A Multidisciplinary Approach. Dioscorides Press, Portland, OR, USA. 454 pp. Brooks, R.R. 1998. Plants that Hyperaccumulate Heavy Metals. CAB International, Wallingford, UK. 380 pp. Freitas, H., M.N.V. Prasad, and J. Prasad. 2004. Analysis of serpentinophytes from northeast of Portugal for trace metal accumulation: Relevance to the management of mine environments. Chemosphere 54:1625–1642. Ghaderian, S.M., and A.J.M. Baker. 2007. Geobotanical and biogeochemical reconnaissance of the ultramafics of Central Iran. Journal of Geochemical Exploration 92:34–42. Ghaderian, S.M., A. Mohtadi, M.R. Rahiminejad, and A.J.M. Baker. 2007a. Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environmental Pollution 145:293–298. Ghaderian, S.M., A. Mohtadi, M.R. Rahiminejad, R.D. Reeves, and A.J.M. Baker. 2007b. Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant and Soil 145:293–298. Jaffré, T. 1992. Floristic and ecological diversity of the vegetation on ultramafic rocks in New Caledonia. Pp.101–108, In A.J.M. Baker, J. Proctor, and R.D. Reeves (Eds). The Vegetation of Ultramafic (Serpentine) Soils. Intercept Ltd., Andover, UK. 509 pp. Jalili, A., and Z. Jamzad. 1999. Red Data Book of Iran. RIFR, Tehran, Iran. 748 pp. Lombini, A., E. Dinelli, C. Ferrari, and A. Simoni. 1998. Plant-soil relationships in the serpentinite screes of Mt. Prinzera (Northern Apennines, Italy). Journal of Geochemical Exploration 64:19–33. Proctor, J. 1999. Toxins, nutrient shortages, and droughts: The serpentine challenge. Trends in Ecology and Evolution 14:334–335. Proctor, J., and L. Nagy. 1992. Ultramafic rocks and their vegetation: An overview. Pp.469–494, In A.J.M. Baker, J. Proctor, and R.D. Reeves (Eds). The Vegetation of Ultramafic (Serpentine) Soils. Intercept Ltd., Andover, UK. 509 pp. Proctor, J., N.V. Alexeeva-Popova , I.M. Kravkina, B.A. Yurtsev, I.V. Drozdova, and M.N. Kataeva. 2004. Arctic ultramafics: New investigations on Polar Ural vegetation. Pp. 121–135, In R.S. Boyd, A.J.M. Baker, and J. Proctor (Eds.). Ultramafic Rocks: Their Soils, Vegetation, and Fauna. Science Reviews, Herts, UK. Rechinger, K.H. (Ed.). (1963–1997): Flora Iranica 1–127. Akademisché Druck und Verlagsanstalt, Graz, Austria. Reddy, R.A., K. Balkwill, and T. McLellan. 2001. Is there a unique serpentine flora on the Witwatersrand? South African Journal of Science 97:485–495. Reeves, R.D. 1992a. New Zealand serpentines and their flora. Pp. 129–138, In A.J.M. Baker, J. Proctor, and R.D. Reeves (Eds). The Vegetation of Ultramafic (Serpentine) Soils. Intercept Ltd., Andover, UK. 509 pp. 16 Northeastern Naturalist Vol. 16, Special Issue 5 Reeves, R.D. 1992b. The hyperaccumulation of nickel by serpentine plants. Pp. 253–278, In A.J.M. Baker, J. Proctor and R.D. Reeves (Eds.). The Vegetation of Ultramafic (Serpentine) Soils. Intercept Ltd., Andover, UK. 509 pp. Reeves, R.D., and A.J.M. Baker. 2000. Metal-accumulating plants. Pp. 193–229, In I. Raskin and B.D. Ensley (Eds.). Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. John Wiley and Sons Inc., New York, NY, USA. Reeves, R.D. 2005. Hyperaccumulation of trace elements by plants. Pp. 25–52, In J-L Morel, G. Echevarria, and N. Goncharova (Eds.). Proceedings of the NATO Advanced Study Institute, Třešt Castle, Czech Republic, 18–30, August 2002. NATO Science Series: IV: Earth and Environmental Sciences, Volume 68. Springer-Verlag, Berlin, Germany. Reeves, R.D., and N. Adigüzel. 2008. The nickel hyperaccumulating plants of the serpentines of Turkey and adjacent areas: A review with new data. Turkish Journal of Biology 32:143–153. Reeves, R.D., A.J.M. Baker, A. Borhidi, and R. Berazaín. 1996. Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytologist 133:217–224. Reeves, R.D., A.J.M. Baker, A. Borhidi, and R. Berazaín. 1999. Nickel hyperaccumulation in the serpentine flora of Cuba. Annals of Botany 83:29–38. Reeves, R.D., A.R. Kruckeberg, N. Adigüzel, and U. Krämer. 2001. Studies on the flora of serpentine and other metalliferous areas of Western Turkey. South African Journal of Science 97:513–517. Reeves, R.D., A.J.M. Baker, T. Becquer, G. Echevarria, and Z.J.G. Miranda. 2007. The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant and Soil 293:107–119. Shallari, S., C. Schwartz, A. Hasko, and J.L. Morel. 1998. Heavy metals in soils and plants of serpentine and industrial sites of Albania. Science of the Total Environment 209:133–142. Wenzel, W.W., and F. Jockwer. 1999. Accumulation of heavy metals in plants grown on mineralized soils of the Austrian Alps. Environmental Pollution 104:145–155. Zhang, X.H., J. Liu, H.T. Huang, J. Chen, Y.N. Zhu, and D.Q. Wang. 2007. Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere 67:1138–1143. 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 17 Appendix 1. List of species, their growth form and the concentrations of elements (μg g-1) in leaf dry matter of plants collected from serpentine soils of Neyriz, Iran. Subscripted letters indicate where more than one specimen was analyzed: A = 2, B = 3, and C = 4. Key to growth forms: Th = therophytes, Ch = chamaephytes, Hemi = hemicryptophytes, and Ph = phanerophytes. Growth Mg/ Species form Ni Cr Co Mn Fe Mg Ca Ca Anacardiaceae Pistacia mutica DESF. Ph 12 7 4 90 920 2700 760 3.5 Apiaceae Anisosciadium orientale DC. Th 26 19A 4 140 1940 3180 1510 2.1 Dicyclophora persica Boiss Th 38A 10 3 97 565 3610 3250 1.1 Eryngium bungii Boiss Hemi 18 6 14 97 790 4705 3600 1.3 Ferula sp. Hemi 89B 23A 4 100 370 3280 5320 0.6 Johrenia platycarpa Boiss. Hemi 36 16 3 73 670 7110 4245 1.7 Prangos uloptera DC. Hemi 22 7 16 100 655 3945 3090 1.3 Scandix aucheri Boiss. Th 22 6 13 89 500 1075 320 3.4 Thecocarpus meifolius Boiss. Hemi 33 11 19B 14 890 9550 9290 1.0 Trachyspermum copticum (L.) Th 38 14 19 71 740 3400 1475 2.3 Link. Zosimia absinthifolia (Vent.) Link. Hemi 16 8 11 61 740 3010 2865 1.0 Asteraceae Achillea eriophora DC. Ch 14 6 8 98 1480 2950 555 5.3 Anthemis rhodocentra M. Iranshahr Th 43A 13 21 98 1310 3200 2095 1.5 Anthemis sp. Th 66B 18A 19A 130 1380 3200 2095 1.5 Centaurea bruguierana Hand. Th 36 12 5 64 1295 1470 440 3.3 -Mazz. Centaurea ispahanica Boiss. Hemi 33 11 8 81 1240 4330 2705 1.6 Centaurea microlonchoides Ch 67B 8 37B 130 900 3755 3630 1.0 Boiss. Crepis kotschyana (Boiss.) Boiss. Th 32 16 2 123 1995 3895 4623 0.8 Crepis sancta (L.) Bodcock Th 16 8 11 108 1240 3010 2865 1.1 Echinops sp. Hemi 28 11 3 39 293 1210 1820 0.7 Gundelia tournefortii L. Hemi 11 6 4 72 340 4500 3400 1.3 Gymnarrhena micrantha DESF. Th 65B 18A 16 127 1340 3880 1530 2.5 Helichrysum leucocephalum Boiss. Ch 21 7 12 70 740 6390 4560 1.4 Outreya carduiformis Jaub. Hemi 13 6 3 73 670 3000 3300 0.9 & Spach Picris strigosa M.B. Hemi 13 13 4 30 400 2865 4215 0.7 Platychaete aucheri Boiss. Ch 24 12 8A 91 750 5220 4030 1.3 Scorzonera tortuosissima Boiss. Hemi 13 8 5 60 880 3400 2870 1.2 Senecio glaucus L. Th 67B 9 33B 76 790 3820 2365 1.6 Boraginaceae Arnebia decumbens (Vent.) Coss. Th 36 14 7 142 785 1920 6735 0.3 & Kral. Heliotropium aucheri DC. Hemi 11 8 3 14 890 1130 1370 0.8 Onosma kotschyi Boiss. Hemi 19 6 20 102 1120 3160 6380 0.5 Paracaryum persicum (Boiss.) Hemi 18 18A 3 85 1455 1790 8120 0.2 Boiss. P. rugulosum (DC.) Boiss. Hemi 40 17 17 110 920 2740 5415 0.5 Trichodesma aucheri DC. Hemi 31 10 14 112 630 7565 2840 2.7 Brassicaceae Alyssum marginatum Timb. Th 17 6 9A 70 530 1073 315 3.4 & Jeanb 18 Northeastern Naturalist Vol. 16, Special Issue 5 Growth Mg/ Species form Ni Cr Co Mn Fe Mg Ca Ca Arabis ottonis-schulzii Bornm. Th 28 11 17 78 400 5800 4015 1.4 & Gauba. Clypeola aspera (Grauer) Turrill Th 11 4 6 58 610 3775 1460 2.6 Diplotaxis harra (Forssk.) Boiss. Hemi 56B 23B 29 95 830 5735 10170 0.6 Pseudocamila glaucophylla Hemi 19 7 21 65 750 4740 4020 1.2 (DC.) N. Sinapis arvensis L. Th 29 55C 20A 120 985 5220 4025 1.3 Sterigmostemum longistylum Th 23 8 2 42 1340 3670 6880 0.5 (Boiss.) Bornm. Capparaceae Buhsea coluteoides Boiss. Hemi 44B 10 8 60 79 3400 2870 1.2 Cleome iberica DC. Th 25 10 23B 98 960 3640 3245 1.1 Caryophyllaceae Acanthophyllum gracile Bunge. Ch 20 7 3 72 315 3445 1450 2.4 Ex Boiss. Dianthus subaphyllus (Lemperg) Ch 23 6 15 100 900 4200 2930 1.4 Rech. F. Gymnocarpos decander Forssk. Ch 27 14 17 94 830 2010 2675 0.7 Silene austro-iranica Rech. F. Th 21 7 14 87 940 3710 2660 1.4 S. chaetodonta Boiss. Th 18 11 13 70 805 2025 1365 1.5 S. spergulifolia (Willd.) M.B. Ch 19 9 20 115 870 26660 2815 9.5 Cistaceae Helianthemum lipii (B.) Pers. Ch 41 12 2 45 530 1990 1265 1.6 Convolvulaceae Convolvulus acanthocladus Boiss. Ch 27 13 4 77 965 2760 1285 2.1 C. kotschyanus Boiss. Ch 21 8 13A 63 920 3775 1460 2.6 C. leiocalycinus Boiss. Ch 15 6 8 86 710 2225 625 3.5 C. oxypetalus Boiss. Ch 45 17 5 70 1420 6875 2895 2.4 Crassulaceae Rosularia sempervivum (M.B.) Hemi 36 13 4 97 1610 2910 5935 0.5 Berger R. persica (M.B.) Berger Hemi 22 7 19 73 1105 3115 4375 0.7 Dipsacaceae Scabiosa persica Boiss. Th 27 11 6 78 535 3400 2870 1.2 S. olivieri Coult. Th 24 10 3 70 1235 1880 1470 1.3 Ephedraceae Ephedra pachyclada Boiss. Ch 18 6 10 63 620 3010 2865 1.0 Euphorbiaceae Euphorbia szovitsii Fisch. & Mey Th 42A 9 2 69 1235 1880 1470 1.3 Fabaceae Argylobium roseum (Camb.) Hemi 25 6 13 81 1105 2600 2355 1.1 Jaub. & Spach Astragalus anserinifolius Boiss Hemi 16 7 3 69 670 3310 7170 0.5 A. cephalanthus D.C. Ch 22 6 10 86 1455 3780 1465 2.6 A. dactylocarpus Boiss. Ch 39 19B 3 72 830 2935 4085 0.7 A. fasciculifolius Boiss Ch 39B 6 18 56 1370 5770 4350 1.3 A. ledinghamii Barneby Hemi 21 6 13 106 995 4905 3765 1.3 A. mucronifolius Boiss. Ch 35 9 4 93 535 3505 940 3.7 A. podolobus Boiss. Ch 35 27B 8 90 500 2745 4615 0.6 A. spachianus Boiss. Hemi 48A 14 4 75 1780 2850 2340 1.2 Ebenus stellata Boiss. Ch 23 5 12 70 710 5705 940 6.1 Onobrychis aucheri Boiss. Th 17 5 4 69 540 2830 1570 1.8 Iridaceae Gynandriris sisyrinchium Parl. Hemi 15 11 6 42 385 1470 440 3.3 2009 S.M. Ghaderian, H. Fattahi, A.R. Khosravi, and M. Noghreian 19 Growth Mg/ Species form Ni Cr Co Mn Fe Mg Ca Ca Laminaceae Nepeta bracteata Benth. Th 44A 13 17 84 735 10600 3070 3.4 N. glomerulosa Boiss. Hemi 44 76C 17 91 890 7865 2820 2.8 N. ispahanica Boiss. Th 52B 18A 24 97 855 5860 4550 1.3 N. prostrata Benth. Hemi 46B 14 19 91 980 10600 3070 3.4 Otostegia persica Boiss. Ch 12 8 9 71 695 2790 1995 1.4 Phlomis oliveri Benth. Ch 17 9 4 65 470 2195 1435 1.5 Salvia macrosiphon Boiss. Th 24 22A 19 78 850 8500 2910 2.9 S. mirzayanii Rech. F. & Esfand. Ch 36A 12B 5 84 780 7110 4245 1.7 S. santolinifolia Boiss. Ch 50B 14A 2 66 805 2025 1365 1.5 Stachys inflata Benth. Ch 19 7 11 70 620 4255 1050 4.0 Teucrium polium L. Ch 12 9 3 53 120 3030 2810 1.1 Zataria multiflora Boiss. Ch 39 8 3 35 560 1545 2540 0.6 Ziziphora tenuior L. Th 21 12A 4 43 460 1070 2100 0.5 Liliaceae Allium ampleoprasum L. sp. Hemi 23 8 14 89 890 7525 3040 2.5 iranicum Wendelbo A. scabriscapum Boiss. Et Ky. Hemi 59B 8 32A 105 1260 6390 4560 1.4 A. stamineum Boiss. Hemi 25 9 16 90 1020 2860 1750 1.6 Colchicum persicum Baker Hemi 78B 19B 10A 105 3325 5825 2620 2.2 Orobanchaceae Orobanche mutelii F.W. Schultz Hemi 42A 12A 4 70 1115 2415 525 4.6 Papaveraceae Glaucium elegans Fisch. & Hemi 31 8 20 68 720 2515 595 4.2 C.A.Mey G. flavum Crantz Hemi 15 6 3 26 450 2210 7920 0.3 Papaver decaisnei Hochst. & Th 51A 10 5 95 550 8560 4990 1.7 Steud. Poacea Eremopoa persica (Trin.) Roshev. Th 17 13 9 56 480 4890 1340 3.6 Melica persica Kunth Hemi 11 5 5 71 680 5390 330 16.3 Secale cereale L. Th 14 9 8 48 620 912 285 3.2 Stipa parviflora Desf. Hemi 23 13 8 112 940 4420 645 6.8 Polygonaceae Polygonum paronychioides C.A. Ch 57B 6 19 81 990 5805 4020 1.4 Mey Polygonum thymifolium Jaub & Ch 70B 7 28 120 1230 20540 4795 4.3 Spach Pteropyrum olivieri Jaub & Spach Ch 35A 4 10 100 1200 6355 750 8.5 Rheum ribes L Hemi 140C 6 47B 115 1200 32530 1290 25.0 Rumex vesicarius L. Th 30 25A 20 120 1050 29415 3080 9.5 Ranunculaceae Delphinium gracile DC. Hemi 28 7 12 90 1020 9550 9290 1.0 D. pallidiflorum Freyn Hemi 32 8 8 90 1020 9550 9285 1.0 Resedaceae Reseda aucheri Boiss. Hemi 36A 16B 3 51 330 9300 3765 2.5 Rosaceae Amygdalus lycioides Spach. Ph 12 5 11 120 890 2665 1755 1.5 A. scoparia Spach. Ph 7 8 3 56 1370 3895 5685 0.7 Rubiaceae Asperula glomerata (M.B.) Griseb. Ch 38 11 4 58 705 4330 2705 1.6 Callipeltis cucullaria Stev. Th 19 5 12 76 890 3300 2035 1.6 20 Northeastern Naturalist Vol. 16, Special Issue 5 Growth Mg/ Species form Ni Cr Co Mn Fe Mg Ca Ca Rutaceae Haplophyllum bakhteganicum Ch 21 6 10 74 650 385 1100 0.3 Soltani & Khosravi Scrophulariaceae Verbascum sp. Hemi 40 8 5 26 530 1070 320 3.3 Veronica rubrifolia Boiss. Th 31 7 14 113 700 3880 1530 2.5 Sinapteridaceae Cheilanthes fragrans (L.F.) SW. Hemi 6 9 2 90 1045 6290 5470 1.1 Thymelaceae Daphne mucronata Royle Ch 9 7 8 83 620 1395 655 2.1 Dendrostellerae lessertii (Wikstr.) Ch 34 12 14A 53 420 3030 2810 1.1 Van Tiegh. Valerianaceae Valerianella oxyrrhyncha Fisch & Th 18 11 6 90 1080 6085 5525 1.1 C.A. Mey