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Environmental Science and Pollution Research

, Volume 25, Issue 34, pp 34753–34764 | Cite as

Tolerance strategies of two Mediterranean native xerophytes under fluoride pollution in Tunisia

  • Asma Boukhris
  • Isabelle Laffont-SchwobEmail author
  • Hélène Folzer
  • Jacques Rabier
  • Imed Mezghani
  • Marie-Dominique Salducci
  • Thierry Tatoni
  • Mohamed Chaieb
Research Article

Abstract

A field study was conducted along a fluorine gradient of soil pollution in Tunisia from Gabes, the most polluted site, to Smara, the reference site. Variations of fluoride (F) concentrations in soils were detected over 1 year in Gabes, Skhira, and Smara. F concentrations in the aerial part of two native plant species, i.e., Erodium glaucophyllum and Rhanterium suaveolens, were above the usual background concentrations. Bioaccumulation factors ranged from 0.08 to 1.3. With F concentrations in aerial parts up to 355 mg kg−1, both species may be described as F accumulators. Both species showed an earlier vegetative growth in Gabes than in Smara. However, some difference between their strategies could be observed, i.e., E. glaucophyllum shortening the period of its vegetative growth with an escape strategy and R. suaveolens decreasing its ratio of alive/dead parts potentially lowering the F toxicity by storage in dead cells. However, at a tissue level, mechanisms of tolerance were similar. Leaf section micrographs of both species showed a higher calcium accumulation in leaf midveins at Gabes than at Smara, confirming the role of calcium in plant F tolerance strategies.

Keywords

Calcium accumulation Erodium glaucophyllum Rhanterium suaveolens Vegetative growth Alive/dead part ratio Escape effect 

Notes

Acknowledgments

The authors thank Lefi El Kadri for his help in harvesting and sampling in the field and are grateful to Alain Tonetto for his help in the use of SEM coupled with EDAX. We thank the Groupe Chimique Tunisien, in particular the Direction Centrale de la Recherche, for its assistance and logistical support in carrying out this study. The authors would also like to thank Michael Paul for revising the English of this text and are grateful to the two anonymous reviewers for their suggestions that helped to improve the quality of the manuscript.

Funding

This study was partly funded by the Action Intégrée Franco-Tunisienne of the French Ministère des Affaires Etrangères et Européennes (EGIDE UTIQUE 2012–2014) and the Tunisian Ministère de l’Enseignement Supérieur, de la Recherche Scientifique (UR 11ES71) entitled: “Réponse écophysiologique de la végétation naturelle vis-à-vis de la pollution atmosphérique fluorée, Tunisie.”

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2018_3431_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 16 kb)

References

  1. Álvarez-Ayuso E, Giménez A, Ballesteros JC (2011) Fluoride accumulation by plants grown in acid soils amended with flue gas desulphurisation gypsum. J Hazard Mater 192:1659–1666CrossRefGoogle Scholar
  2. Ben Abdallah F, Elloumi N, Mezghani I, Boukhris M, Garrec J-P (2006a) Survival strategies of pomegranate and almond trees in a fluoride polluted area. Comptes Rendus Biologies 329:200–207CrossRefGoogle Scholar
  3. Ben Abdallah F, Elloumi N, Mezghani I, Garrec J-P, Boukhris M (2006b) Industrial fluoride pollution of Jerbi grape leaves and the distribution of F, Ca, Mg, and P in them. Fluoride 39:43–48 http://www.fluorideresearch.org/391/files/39143-48.pdf. Accessed 4 July 2018Google Scholar
  4. Bokhorst S, Bjerkew JW, Streetz LE, Callaghan TV, Phoenix GK (2011) Impacts of multiple extreme winter warming events on sub-Arctic heathland: phenology, reproduction, growth, and CO2 flux responses. Glob Chang Biol 17:2817–2830.  https://doi.org/10.1111/j.1365-2486.2011.02424.x Accessed 4 July 2018CrossRefGoogle Scholar
  5. Boukhris A, Laffont-Schwob I, Mezghani I, El Kadri L, Prudent P, Pricop A, Tatoni T, Chaieb M (2015a) Screening biological traits and fluoride contents of native vegetations in arid environments to select efficiently fluoride-tolerant native plant species for in-situ phytoremediation. Chemosphere 119:217–223CrossRefGoogle Scholar
  6. Boukhris A, Laffont-Schwob I, Rabier J, Salducci M-D, El Kadri L, Tonetto A, Tatoni T, Chaieb M (2015b) Changes in mesophyll element distribution and phytometabolite contents involved in fluoride tolerance of the arid gypsum-tolerant plant species Atractylis serratuloides Sieber ex Cass. (Asteraceae). Environ Sci Pollut Res 22(10):7918–7929CrossRefGoogle Scholar
  7. Chaieb M, Boukhris M (1998) Flore Des Zones Arides Et Sahariennes De Tunisie, Ed. L’Or du Temps, Tunis 290 p (In French)Google Scholar
  8. Davison AW, Weinstein LH (2006) Some problems relating to fluorides in the environment: effects on plants and animals. In: Tressaud A (ed) Fluorine and the environment, atmospheric chemistry, emissions and lithosphere, vol 1. Elsevier, Amsterdam, pp 251–298CrossRefGoogle Scholar
  9. Domingos M, Klumpp A, Rinaldi MCS, Modesto IF, Klumpp G, Delitti WBC (2003) Combined effects of air and soil pollution by fluoride emissions on Tibouchina pulchra Cogn., at Cubatão, SE Brazil, and their relations with aluminium. Plant Soil 249:297–308CrossRefGoogle Scholar
  10. Ebbs SD, Bradfield SJ, Kumar P, White JC, Musante C, Ma X (2016) Accumulation of zinc, copper, or cerium in carrot (Daucus carota) exposed to metal oxide nanoparticles and metal ions. Environ Sci Nano 3(1):114–126CrossRefGoogle Scholar
  11. Emberger L (1954) Une Classification Biogéographique Des Climats. Rec Trav Lab Bot Géol Zool Univ Montpellier Sér Bot 7:3–43 (in French)Google Scholar
  12. Floret C (1981) The effects of protection on steppic vegetation in the Mediterranean arid zone of Southern Tunisia. Vegetatio 46(1):117–129CrossRefGoogle Scholar
  13. Floret C, Pontanier R (1978) Relations climat-sol-végétation dans quelques formations végétales spontanées du sud Tunisien (production végétale et bilan hydrique des sols). Inst. Rég. Arides–Médenine, Dir. Ress. Eau et Sols Tunis, CEPE/CNRS Montpellier et Orstom—Paris, 96 p (in French)Google Scholar
  14. Floret C, Pontanier R (1982) L’aridité en Tunisie présaharienne: Climat, sol, végétation et aménagement. Trav. et Doc. ORSTOM, n° 150—Paris, 544 p (in French)Google Scholar
  15. Fornasiero RB (2001) Phytotoxic effects of fluorides. Plant Sci 161:979–985CrossRefGoogle Scholar
  16. Fornasiero RB (2003) Fluorides effects on Hypericum perforatum plants: first field observations. Plant Sci 165:507–513CrossRefGoogle Scholar
  17. Franks SJ (2011) Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa. New Phytol 190:249–257CrossRefGoogle Scholar
  18. Franzaring J, Klumpp A, Fangmeier A (2007) Active biomonitoring of airborne fluoride near an HF producing factory using standardised grass cultures. Atmos Environ 41:4828–4840CrossRefGoogle Scholar
  19. Gounot M (1969) Méthodes d'étude quantitative de la végétation. Masson, Paris 314 pGoogle Scholar
  20. Haneklaus N, Schnug E, Tulsidas H, Tyobeka B (2015) Using high temperature gas-cooled reactors for greenhouse gas reduction and energy neutral production of phosphate fertilizers. Ann Nucl Energy 75:275–282CrossRefGoogle Scholar
  21. Haworth M, McElwain J (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeoecology 262:79–90CrossRefGoogle Scholar
  22. Jablonski LM, Wang X, Curtis PS (2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol 156(1):9–26CrossRefGoogle Scholar
  23. Kabata-Pendias A, Szteke B (2015) Trace elements in abiotic and biotic environments, chapter 15: Fluorine, CRC Press, pp 109–118Google Scholar
  24. Kozlov MV, Eränen JK, Zverev VE (2007) Budburst phenology of white birch in industrially polluted areas. Environ Pollut 148:125–131CrossRefGoogle Scholar
  25. Le Houérou HN (2008) Bioclimatology and biogeography of Africa. Springer-Verlag, Heidelber 240 pGoogle Scholar
  26. Mesquita GL, Tanaka FAO, Cantarella H, Mattos D Jr (2011) Atmospheric absorption of fluoride by cultivated species. Leaf structural changes and plant growth. Water Air Soil Pollut 219:143–156CrossRefGoogle Scholar
  27. Mezghani I, Elloumi N, Ben Abdallah F, Chaieb M, Boukhris M (2005) Fluoride accumulation by vegetation in the vicinity of a phosphate fertiliser plant. Fluoride 38:69–75 https://pdfs.semanticscholar.org/df02/76856028881ac0bc96142195dbc2e06e36d0.pdf. Accessed 4 July 2018Google Scholar
  28. Mighri H, Akrout A, Neffati M (2011) Assessment of essential oil yield of Artemisia herba-alba cultivated in Tunisian arid zone. J Med Plants Res 5(21):5296–5300 https://academicjournals.org/article/article1380533387_Mighri%20et%20al.pdf Accessed 4 July 2018Google Scholar
  29. Mtimet A (2001) Soils of Tunisia. In: Zdruli P, Steduto P, Lacirignola C, Montanarella L (eds) Soil resources of southern and eastern Mediterranean countries CIHEAM, Bari, pp 243–262Google Scholar
  30. Nakata PA, McConn MM (2000) Isolation of Medicago trunculata mutants defective in calcium oxalate formation. Plant Physiol 124:1097–1110CrossRefGoogle Scholar
  31. Pack MR, Sulzbach CW (1976) Response of plant fruiting to hydrogen fluoride fumigation. Atmos Environ 10:73–81CrossRefGoogle Scholar
  32. Rabier J, Laffont-Schwob I, Notonier R, Fogliani B, Bouraïma-Madjebi S (2008) Anatomical element localization by EDXS in Grevillea exul var. exul under nickel stress. Environ Pollut 156:1156–1116CrossRefGoogle Scholar
  33. Ryser P, Sauder WR (2006) Effects of heavy-metal-contaminated soil on growth, phenology and biomass turnover of Hieracium piloselloides. Environ Pollut 140:52–61CrossRefGoogle Scholar
  34. Saini P, Khan S, Baunthiyal M, Sharma V (2013) Effects of fluoride on germination, early growth and antioxidant enzyme activities of legume plant species Prosopis juliflora. J Environ Biol 34:205–209Google Scholar
  35. Shantz HL (1927) Drought resistance and soil moisture. Ecology 8(2):145–157CrossRefGoogle Scholar
  36. Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6(article 1143):1–36Google Scholar
  37. Singh G, Kumari B, Sinam G, Kumar KN, Shekhar M (2018) Fluoride distribution and contamination in the water, soil and plants continuum and its remedial technologies, an Indian perspective—a review. Environ Pollut 239:95–108CrossRefGoogle Scholar
  38. Small E (1973) Xeromorphy in plants as a possible basis for migration between arid and nutritionally-deficient environments. Bot Notiser 126:534–539Google Scholar
  39. Smith SD, Monson RK, Anderson JE (1997) Physiological ecology of North American desert plants. Springer-Verlag, Berlin 286 pCrossRefGoogle Scholar
  40. Song W-Y, Zhang Z-B, Shao H-B, Guo X-L, Cao H-X, Zhao H-B, Fu Z-Y, Hu X-J (2008) Relationship between calcium decoding elements and plant abiotic-stress resistance. Int J Biol Sci 4(2):116–125CrossRefGoogle Scholar
  41. Taib M (2013) The mineral industry of Tunisia. In: USGS (eds), United States Geological Survey 2011 minerals yearbook, pp 41.1-41.7Google Scholar
  42. Tarhouni M, Ben Salem F, Ouled Belgacem A, Neffati M (2010) Acceptability of plant species along grazing gradients around watering points in Tunisian arid zone. Flora 205:454–461CrossRefGoogle Scholar
  43. Tayibi H, Choura M, López FA, Alguacil FJ, López-Delgado A (2009) Environmental impact and management of phosphogypsum. J Environ Manag 90:2377–2386CrossRefGoogle Scholar
  44. Thévenard F, Gomez B, Daviero-Gomez V (2005) Xeromorphic adaptations of some Mesozoic gymnosperms. A review with palaeoclimatological implications. Comptes Rendus Palevol 4:67–77CrossRefGoogle Scholar
  45. Vike E, Håbjørg A (1995) Variation in fluoride content and leaf injury on plants associated with three aluminium smelters in Norway. Sci Total Environ 163:25–34CrossRefGoogle Scholar
  46. Weinstein LH, Davison A (2003) Native plant species suitable as bioindicators and biomonitors for airborne fluoride. Environ Pollut 125:3–11CrossRefGoogle Scholar
  47. Zahran MA (2010) Climate vegetation. Afro-Asian Mediterranean and Red Sea coastal lands. Plant and Vegetation. Springer Dordrecht Heidelberg, London New York 344 pGoogle Scholar
  48. Zhou Q, Sun T (2002) Effects of chromium (VI) on extractability and plant uptake of fluorine in agricultural soils of Zhejiang Province, China. Water Air Soil Pollut 133: 145 p:145–160CrossRefGoogle Scholar
  49. Zvereva EL, Roitto M, Kozlov MV (2010) Growth and reproduction of vascular plants in polluted environments: a synthesis of existing knowledge. Environ Rev 18:355–367CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Aix Marseille Univ, CNRS, IRD, IMBEAvignon UniversitéMarseilleFrance
  2. 2.Plant diversity and Ecosystems in Dry Environment, Faculty of ScienceUniversity of SfaxSfaxTunisia
  3. 3.Aix Marseille Univ, IRD, LPEDMarseille Cedex 3France

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