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

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Allelochemicals of Pinus Halepensis As Drivers of Biodiversity in Mediterranean Open Mosaic Habitats During the Colonization Stage of Secondary Succession J Chem Ecol DOI 10.1007/s10886-013-0239-6 Allelochemicals of Pinus halepensis as Drivers of Biodiversity in Mediterranean Open Mosaic Habitats During the Colonization Stage of Secondary Succession Catherine Fernandez & Mathieu Santonja & Raphael Gros & Yogan Monnier & Mathilde Chomel & Virginie Baldy & Anne Bousquet-Mélou Received: 14 September 2012 /Revised: 30 October 2012 /Accepted: 15 November 2012 # Springer Science+Business Media New York 2013 Abstract The Mediterranean region is recognized as a stimulated. Thus, microorganisms alter the expression of global biodiversity hotspot. However, over the last 50 years allelochemicals released into the ecosystem, which high- or so, the cessation of traditional farming has given way to lights their key role in chemical plant-plant interactions. strong afforestation at the expense of open habitats. Pinus The results of allelopathic experiments conducted in the halepensis Miller, known to synthesize a wide range of lab are consistent with the community patterns observed in secondary metabolites, is a pioneer expansionist species the field. These findings suggest that allelopathy is likely to colonizing abandoned agricultural land that present high shape vegetation composition and participate to the control species richness. Here, laboratory bioassays were used to of biodiversity in Mediterranean open mosaic habitats. study the potential impact of P. halepensis on plant diversity through allelopathy, and the role of microorganisms in these Keywords Allelopathy . Plant-plant interaction . interactions. Germination and growth of 12 target species Community structure . Mediterranean biodiversity . naturally present in fallow farmlands were tested according Secondary succession . Aleppo pine . Soil microorganisms 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 Introduction than 80 % of target species were germination and/or growth- inhibited, and only two species were non-sensitive. Under The Mediterranean basin is characterized by a long history more natural conditions (lower extracts concentrations and of farming that has profoundly modified its landscapes since natural soil with microorganisms), only 50 % of species the Neolithic (Blondel and Aronson 1995). This history were still inhibited, one was non-sensitive, and five were pressure has selected a typical biodiversity from open hab- itats with numerous vital conservation species (Fonderflick Catherine Fernandez and Mathieu Santonja has equal contribution to et al. 2010), which is partly why the incredibly species-rich the work. Mediterranean biomes (Cowling et al. 1996) now count as “biodiversity hotspots” (Myers et al. 2000). Although orig- C. Fernandez (*) : M. Santonja : Y. Monnier : M. Chomel : V. Baldy : A. Bousquet-Mélou inal Mediterranean forest continues to be lost in the south Aix-Marseille Université Institut Méditerranéen de Biodiversité et part of the basin (largely through conversion to agriculture), d’Ecologie (IMBE UMR CNRS IRD 7263), further north, rural flight has significantly lessened the Campus St Charles, Case 4, pressure on ecosystems. This rural exodus has led to the 13331 Marseille Cedex 03, France e-mail: [email protected] afforestation of abandoned agricultural land (Barbero et al. 1990) and a large-scale progression of forest land cover R. Gros (Debussche et al. 2001). Pines generally recolonize aban- Aix-Marseille Université Institut Méditerranéen de Biodiversité et doned land (Richardson et al. 2007). This process, called d’Ecologie (IMBE UMR CNRS IRD 7263), Campus Saint-Jérôme, Case 441, secondary succession, directly threatens a mosaic of habitats 13397 Marseille Cedex 20, France of high patrimonial value by driving a homogenization of J Chem Ecol plant communities and a loss of biodiversity (Chauchard et (Inderjit and Weston 2000; Inderjit 2006). Specific objec- al. 2007; Sheffer 2012). tives were to: i) determine whether allelochemicals of P. Community organization and plant succession are under halepensis affect the germination and seedling growth of the control of biotic processes, particularly plant-plant inter- several species native to Mediterranean open habitats by actions such as resource competition, facilitation, and alle- using 12 target species naturally present in open habitats lopathy (Callaway and Walker 1997). Allelopathy is a typical of land abandonment; ii) evaluate the role of micro- process by which a plant releases biochemicals that influ- organisms in these effects by using natural and autoclaved ence the growth and establishment of other plants (Inderjit soil; and iii) verify that results obtained under lab conditions 2005). Allelopathic compounds are released into the envi- are consistent with community patterns observed in the field ronment through foliar leachates, root exudation, leaf litter, by performing floristic inventories along secondary other-residue decomposition, or volatilization (Rice 1984) succession. and may influence various physiological processes (e.g., photosynthesis, nutrient uptake, cell division, or elonga- tion). Through these detrimental but also beneficial effects Methods and Materials on receptor plants, allelochemicals play important roles in regulating species diversity (Chou 1999). However, if Study Site The study site is located in the Luberon Natural allelochemicals can directly affect plant neighbors, Regional Park, SE France. This site is in secondary succes- allelopathic expression mayinturnbemodifiedbysoil sion, including 5 stages of P. halepensis colonization: fallow microbial communities by influencing the persistence, land without pines, fallow land with a few young pines availability and biological impacts of the allelochemicals (about 5 yr old), young pine forest (about 10 yr old), mid- (for a review, see Cipollini et al. 2012). age forest (about 30 yr old), and old pine forest (>60 yr old). Studying how organisms interact with each other is rele- vant to understanding ecological community organization. Material Collection The study site used for material collec- Research is needed to test the sensitivity of wild plant tion (plants and soil) is fallow land (abandoned farmland, species to allelochemicals, factoring in the potential role of formerly vineyard and almond orchard; 43°45′34.26″N; 5° soil microbial community on the chemical plant-plant inter- 17′57.84″E) that represents early colonization by young P. actions. This is particularly important in Mediterranean halepensis (about 5 yr). plant communities that feature species rich in secondary Of the 50 species naturally present on the site, 12 were metabolites, and for which the ecological relevance of alle- selected: Arabis hirsuta (L.) Scop., Avena barbata Pott ex lopathy remains unclear. Link, Briza maxima L., Dactylis glomerata L., Daucus The long-term aim of our research is to analyze how carota L., Helichrysum stoechas (L.) Moench, Linum stric- allelochemicals of Pinus halepensis Miller influence plant tum L., Reichardia picroides (L.) Roth, Salvia verbenaca L., biodiversity in Mediterranean open mosaic habitats during Sedum sediforme (Jacq.) Pau, Tanacetum corymbosum (L.) the colonization stage of secondary succession. Pinus Sch. Bip., and Trifolium stellatum L. Our selection aimed to halepensis is a circum-Mediterranean species covering 2.5 test different plant families with different life history traits million hectares in the Mediterranean basin (Quezel 2000) (Table 1). Seeds of all species were collected from wild that has expanded massively over the last century, facilitated populations on the study site outside the zone of influence by forest fires and abandonment of farmland (Richardson et of Aleppo pine, then stored in a cold chamber at 5 °C until al. 2007). This pioneer and expansionist species has come to the start of the experiment. Pinus halepensis needles used to dominate the areas of agricultural decline (Gondard et al. prepare the aqueous extracts were collected from 10 young 2003), thus contributing to the homogenization of plant individual Aleppo pines (about 5 yr old) present in the study communities in the Mediterranean area. Moreover, P. site. Soil samples used as bioassay substrate also were halepensis is rich in secondary metabolites (Macchioni et collected outside the zone of influence of Aleppo pine al. 2003; Fernandez et al. 2009) that are thought to play (i.e., at least 10 m from trees), sieved through a 2 mm- a role in plant-plant interactions through allelopathic mesh screen, then stored at room temperature until the start processes (Fernandez et al. 2006, 2008, 2009). of the experiment. This soil was characterized as agricultural In order to test whether P. halepensis allelochemicals Rendzic Leptosol soil according to FAO criteria (FAO 1998) might drive plant biodiversity in Mediterranean open mosa- and as Rendoll according to “Soil Taxonomy” criteria (Soil ic habitats during secondary succession, we performed a lab Survey Staff 1999). experiment consisting of allelopathy bioassays that mim- icked natural conditions. These kinds of experiments are Allelopathy Bioassays Water-soluble compounds are prob- an important prerequisite for understanding the scale of ably the most involved in allelopathy (Vyvyan 2002). allelopathic mechanisms in plant community dynamics Previous studies on P. halepensis showed that needle J Chem Ecol Table 1 Characteristics
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