Skip to main content

Advertisement

Log in

Allelochemicals of Pinus halepensis as Drivers of Biodiversity in Mediterranean Open Mosaic Habitats During the Colonization Stage of Secondary Succession

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The Mediterranean region is recognized as a global biodiversity hotspot. However, over the last 50 years or so, the cessation of traditional farming has given way to strong afforestation at the expense of open habitats. Pinus halepensis Miller, known to synthesize a wide range of secondary metabolites, is a pioneer expansionist species colonizing abandoned agricultural land that present high species richness. Here, laboratory bioassays were used to study the potential impact of P. halepensis on plant diversity through allelopathy, and the role of microorganisms in these interactions. Germination and growth of 12 target species naturally present in fallow farmlands were tested according to concentration of aqueous extracts obtained from shoots of young pines (aged about 5 years), with or without the presence of soil microorganisms (autoclaved or natural soil). Under the highest concentrations and autoclaved soil, more than 80 % of target species were germination and/or growth-inhibited, and only two species were non-sensitive. Under more natural conditions (lower extracts concentrations and natural soil with microorganisms), only 50 % of species were still inhibited, one was non-sensitive, and five were stimulated. Thus, microorganisms alter the expression of allelochemicals released into the ecosystem, which highlights their key role in chemical plant-plant interactions. The results of allelopathic experiments conducted in the lab are consistent with the community patterns observed in the field. These findings suggest that allelopathy is likely to shape vegetation composition and participate to the control of biodiversity in Mediterranean open mosaic habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams, R. P. 2007. Identification of essential oil components by gas chromatography / mass spectrometry, 4th ed. Allured Publishing Corporation, Carol Stream.

    Google Scholar 

  • Alef, K. and Nannipieri, P. 1995. Methods in applied soil microbiology and biochemistry. Academic, London.

    Google Scholar 

  • Alrababah, M., Tadros, M. J., Samarah, N. H., and Ghosheh, H. 2009. Allelopathic effects of Pinus halepensis and Quercus coccifera on the germination of Mediterranean crop seeds. New Forest 38:261–272.

    Article  Google Scholar 

  • Anderson, J. P. E. and Domsch, K. H. 1978. A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biol. Biochem. 10:215–221.

    Google Scholar 

  • Anderson, R. C. and Loucks, O. L. 1966. Osmotic pressure influence in germination tests for antibiosis. Science 152:771–773.

    Google Scholar 

  • Barbero, M., Bonin, G., Loisel, R., and Quezel, P. 1990. Changes and disturbances of forest ecosystems caused by human activities in the western part of the Mediterranean basin. Vegetatio 87:151–173.

    Article  Google Scholar 

  • Barkosky, R. R., Einhellig, F. A., and Butler, J. L. 2000. Caffeic acid-induced changes in plant-water relationship and photosynthesis in leafy spurge Euphorbia esula. J. Chem. Ecol. 26:2095–2109.

    Article  CAS  Google Scholar 

  • Beare, M. H., Neely, C. L., Coleman, D. C., and Hargrove, W. L. 1990. A substrate-induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biol. Biochem. 22:585–594.

    Article  Google Scholar 

  • Blondel, J. and Aronson, J. 1995. Biodiversity and ecosystem function in the Mediterranean basin: human and non-human determinants. In biodiversity and ecosystem function in Mediterranean-type ecosystems. Ecol. Stud. 109:44–119.

    Google Scholar 

  • Blum, U. and Gerig, T. M. 2006. Interrelationships between p-coumaric acid, evapotranspiration, soil water content and leaf expansion. J. Chem. Ecol. 32:1817–1834.

    Article  PubMed  CAS  Google Scholar 

  • Blum, U. and Shafer, S. R. 1988. Microbial populations and phenolic acids in soils. Soil Biol. Biochem. 20:793–800.

    Article  CAS  Google Scholar 

  • Braun-Blanquet, J. 1932. Plant sociology. The study of plant communities. McGraw-Hill Eds, New York.

    Google Scholar 

  • Callaway, R. M. and Walker, L. R. 1997. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965.

    Article  Google Scholar 

  • Callaway, R. M., Ridenour, W. M., Laboski, T., Weir, T., and Vivanco, J. M. 2005. Natural selection for resistance to the allelopathic effects of invasive plants. J. Ecol. 93:576–583.

    Article  Google Scholar 

  • Chauchard, S., Carcaillet, C., and Guibal, F. 2007. Patterns of land-use abandonment control tree-recruitment and forest dynamics in Mediterranean mountains. Ecosystems 10:936–948.

    Article  Google Scholar 

  • Chou, C. H. 1999. Roles of allelopathy in plant biodiversity and sustainable agriculture. Crit. Rev. Plant Sci. 18:609–636.

    Article  Google Scholar 

  • Cipollini, D., Rigsby, C. M., and Barto, E. K. 2012. Microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol. 38:714–727.

    Article  PubMed  CAS  Google Scholar 

  • Cowling, R. M., Rundel, P. W., Lamont, B. B., Arroyo, M. K., and Arianoutsou, M. 1996. Plant diversity in Mediterranean climate regions. Trends Ecol. Evol. 11:362–366.

    Article  PubMed  CAS  Google Scholar 

  • Debussche, M., Debussche, G., and Lepart, J. 2001. Changes in the vegetation of Quercus pubescens woodland after cessation of coppicing and grazing. J. Veg. Sci. 12:81–92.

    Google Scholar 

  • El-Khawas, S. A. and Shehata, M. M. 2005. The allelopathic potentialities of Acacia nilotica and Eucalyptus rostrata on monocot (Zea mays L.) and dicot (Phaseolus vulgaris L.) plants. Biotechnology 42:3–34.

    Google Scholar 

  • FAO 1998. World reference base for soil resources. International Society of Soil Science, Rome.

    Google Scholar 

  • Fernandez, C., Lelong, B., Vila, B., Mévy, J. P., Robles, C., Greff, S., Dupouyet, S., and Bousquet-Mélou, A. 2006. Potential allelopathic effect of Pinus halepensis in the secondary succession: an experimental approach. Chemoecology 16:97–105.

    Article  CAS  Google Scholar 

  • Fernandez, C., Voiriot, S., Mevy, J. P., Vila, B., Ormeño, E., Dupouyet, S., and Bousquet-Melou, A. 2008. Regeneration failure of Pinus halepensis Mill.: the role of autotoxicity and some abiotic environmental parameters. Forest Ecol Manag. 255:2928–2936.

    Article  Google Scholar 

  • Fernandez, C., Monnier, Y., Ormeño, E., Baldy, V., Greff, S., Pasqualini, V., Mévy, J. P., and Bousquet-Melou, A. 2009. Variations in allelochemical composition of leachates of different organs and maturity stages of Pinus halepensis. J. Chem. Ecol. 35:970–979.

    Article  PubMed  CAS  Google Scholar 

  • Fonderflick, J., Lepart, J., Caplat, P., Debussche, M., and Marty, P. 2010. Managing agricultural change for biodiversity conservation in a Mediterranean upland. Biol. Conserv. 43:737–746.

    Article  Google Scholar 

  • Gachet, S., Vela, E., and Tatoni, T. 2005. BASECO: a floristic and ecological database of Mediterranean french flora. Biodivers. Conserv. 14:1023–1034.

    Article  Google Scholar 

  • Gallet, C. 1994. Allelopathic potential in bilberry-spruce forests: influence of phenolic compounds on spruce seedlings. J. Chem. Ecol. 20:1009–1024.

    Article  CAS  Google Scholar 

  • Gondard, H.,Romane, F.,Aronson, J., and Shater, Z. 2003. Impact of soil surface disturbances on functional group diversity after clear-cutting in Allepo pine (Pinus halepensis) forests in southern France. Forest Ecol. Manag. 180:165–174.

    Article  Google Scholar 

  • Green, J. J., Baddeley, J. A., Cortina, J., and Watson, C. A. 2005. Root development in Mediterranean shrub Pistacia lentiscus as affected by nursery treatments. J. Arid. Environ. 61:1–12.

    Article  Google Scholar 

  • Herranz, J. M., Ferrandis, P., Copete, M. A., Duro, E. M., and Zalacain, A. 2006. Effect of allelopathic compounds produced by Cistus ladanifer on germination of 20 Mediterranean taxa. Plant Ecol. 184:259–272.

    Article  Google Scholar 

  • Inderjit 2005. Soil microorganisms: an important determinant of allelopathic activity. Plant Soil 274:227–236.

    Article  CAS  Google Scholar 

  • Inderjit 2006. Experimental complexities in evaluating the allelopathic activities in laboratory bioassays: a case study. Soil Biol. Biochem. 38:256–262.

    Article  CAS  Google Scholar 

  • Inderjit and Weiner, J. 2001. Plant allelochemical interference or soil chemical ecology? Perspect. Plant. Ecol. Evol. Syst. 4:3–12.

    Article  Google Scholar 

  • Inderjit and Weston, L. A. 2000. Are laboratory bioassays for allelopathy suitable for prediction of field responses? J. Chem. Ecol. 26:2111–2118.

    Article  Google Scholar 

  • Inderjit, Wardle, D. A., Karban, R., and Callaway, R. M. 2011. The ecosystem and evolutionary contexts of allelopathy. Trends Ecol. Evol. 26:655–662.

    Article  PubMed  Google Scholar 

  • Karamanoli, K., Vokou, D., Menkissoglu, U., and Constantinidou, H. I. 2000. Bacterial colonization of phyllosphere of Mediterranean aromatic plants. J. Chem. Ecol. 26:2035–2048.

    Article  CAS  Google Scholar 

  • Karamanoli, K., Menkissoglu-Spiroudi, U., Bosabalidis, A. M., Vokou, D., and Constantinidou, H. I. A. 2005. Bacterial colonization of the phyllosphere of nineteen plant species and antimicrobial activity of their leaf secondary metabolites against leaf associated bacteria. Chemoecology 15:59–67.

    Article  Google Scholar 

  • Kato-Noguchi, H., Fushimi, Y., and Shigemori, H. 2009. An allelopathic substance in red pine needles (Pinus densiflora). J. Plant Physiol. 166:442–446.

    Article  PubMed  CAS  Google Scholar 

  • Kaur, H., Kaur, R., Kaur, S., Baldwin, I. T., and Inderjit 2009. Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One 4:e4700.

    Article  PubMed  Google Scholar 

  • Kuiters, A. T. 1989. Effects of phenolic acids on germination and early growth of herbaceous woodland plants. J. Chem. Ecol. 15:467–479.

    Article  CAS  Google Scholar 

  • Lloret, F., Casanovas, C., and Peñuelas, J. 1999. Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Funct. Ecol. 13:210–216.

    Article  Google Scholar 

  • Macchioni, F., Cioni, P. L., Flamini, G., Morelli, I., Maccioni, S., and Ansaldi, M. 2003. Chemical composition of essential oils from needles, branches and cones of Pinus pinea, P. halepensis, P. pinaster and P. nigra from central Italy. Flavour Frag J. 18:139–143.

    Article  CAS  Google Scholar 

  • Mazliak, P. 1982. Physiologie végétale: croissance et développement. Hermann Publ, Paris.

    Google Scholar 

  • Meiners, S. J., Kong, C. H., Ladwig, L. M., Pisula, N. L., and Lang, K. A. 2012. Developing an ecological context for allelopathy. Plant Ecol. 213:1221–1227.

    Article  Google Scholar 

  • Myers, N., Mittermeier, N. A., Mittermeier, C. G., Da Fonseca, G. A. B., and Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853–858.

    Article  PubMed  CAS  Google Scholar 

  • Nektarios, P. A., Economou, G., and Avgoulas, C. 2005. Allelopathic effects of Pinus halepensis needles on turfgrasses and biosensor plants. Hortscience 40:246–250.

    Google Scholar 

  • Ormeño, E., Baldy, V., Ballini, C., and Fernandez, C. 2008. Production and diversity of volatile terpenes from plants on calcareous and siliceous soils: effect of soil nutrients. J. Chem. Ecol. 34:1219–1229.

    Article  PubMed  Google Scholar 

  • Quezel, P. 2000. Taxonomy and biogeography of Mediterranean pines (Pinus halepensis and P. brutia), pp. 1–12, in G. Ne’eman and L. Trabaud (eds.), Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean basin. Backhuys publishers, Leiden.

    Google Scholar 

  • Rameau, J. C., Mansion, D., and Dume, G. 1989. Flore forestière française (guide écologique illustré), Tome 1 : Plaines et Collines. Institut pour le développement forestier. IDF Publications.

  • Reigosa, M. J. and Pazos-Malvido, E. 2007. Phytotoxic effects of 21 plant secondary metabolites on Arabidopsis thaliana germination and root growth. J. Chem. Ecol. 33:1456–1466.

    Article  PubMed  CAS  Google Scholar 

  • Reigosa, M. J., Sanchez-Moreiras, A., and Gonzalez, L. 1999. Ecophysiological approach in allelopathy. Crit. Rev. Plant Sci. 18:577–608.

    Article  CAS  Google Scholar 

  • Rice, E. L. 1984. Allelopathy. Academic, USA.

    Google Scholar 

  • Richardson, D. M., Rundel, P. W., Jackson, S. T., Teskey, R. O., Aronson, J., Bytnerowicz, A., Wingfield, M. J., and Proches, S. 2007. Human impacts in pine forests: past, present and future. Annu. Rev. Ecol. Evol. Syst. 38:275–297.

    Article  Google Scholar 

  • Robles, C., Greff, S., Pasqualini, V., Garzino, S., Bousquet-Melou, A., Fernandez, C., Korboulewsky, N., and Bonin, G. 2003. Phenols and flavonoids in Aleppo pine needles as bioindicators of air pollution. J. Environ. Qual. 32:2265–2271.

    Article  PubMed  CAS  Google Scholar 

  • Scherrer, B. 1984. Biostatistique. Gaëtan Morin publishers, Chicoutimi.

    Google Scholar 

  • Schmidt, S. K. 1990. Ecological implication of destruction of juglone (5-hydroxy-1,4-napthoquinone) by soil bacteria. J. Chem. Ecol. 16:3547–3549.

    Article  Google Scholar 

  • Schmidt, S. K. and Ley, R. E. 1999. Microbial competition and bioavailability limit the expression of allelochemicals in natural soils, pp. 339–351, in Inderjit, K. M. M. Dakshini, and C. L. Foy (eds.), Principles and practices in plant ecology: allelochemical interactions. CRC Press, Boca Raton.

    Google Scholar 

  • Sheffer, E. 2012. A review of the development of Mediterranean pine-oak ecosystems after land abandonment and afforestation: are they novel ecosystems? Ann. For. Sci. 69:429–443.

    Article  Google Scholar 

  • Soil survey staff. 1999. Soil Taxonomy. 2nd edition. USDA Natural Resources Conservation Service Agriculture Handbook 436. U.S. Government Printing Office, Washington, D.C.

  • Trevors, J. T. 1996. Sterilization and inhibition of microbial activity in soil. J. Microbiol. Meth. 26:53–59.

    Article  CAS  Google Scholar 

  • Valera-Burgos, J., Diaz-Barradas, M. C., and Zunzunegui, M. 2012. Effects of Pinus pinea litter on seed germination and seedling performance of three Mediterranean shrub species. Plant Growth Regul. 66:285–292.

    Article  CAS  Google Scholar 

  • Vyvyan, J. R. 2002. Allelochemicals as lead for new herbicides and agrochemicals. Tetrahedron 58:1631–1649.

    Article  CAS  Google Scholar 

  • Williams, R. D. and Hoagland, R. E. 1982. The effect of naturally-occurring phenolic compounds on seed germination. Weed Sci. 30:206–212.

    CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the CNRS [French national centre for scientific research] within the framework of the Zone Atelier “Arrière-pays Méditerranéen”. We are grateful to the staff of the Luberon Natural Regional Park. We would also like to thank Stéphane Greff (IMBE) for his contribution to the chemical analyses, Sylvie Dupouyet (IMBE) for her help with the bioassays, and A-T-T (Scientific and technical translation) for proofreading the draft manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine Fernandez.

Additional information

Catherine Fernandez and Mathieu Santonja has equal contribution to the work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernandez, C., Santonja, M., Gros, R. et al. Allelochemicals of Pinus halepensis as Drivers of Biodiversity in Mediterranean Open Mosaic Habitats During the Colonization Stage of Secondary Succession. J Chem Ecol 39, 298–311 (2013). https://doi.org/10.1007/s10886-013-0239-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-013-0239-6

Keywords

Navigation