Seasonal dependence and functional implications of macrophyte–phytoplankton allelopathic interactions

Abstract

Invasive plant species such as Ludwigia hexapetala might have a competitive advantage if they produce allelopathically active compounds against primary producers. Both phytoplankton and plant community structure may be affected due to different, species‐specific sensitivity to allelochemicals. Moreover, such allelopathic interactions could vary over the year depending on (i) the plant's phenological stage and (ii) the abilities of the native macrophytes to suppress—or the non‐native macrophytes to stimulate—the non‐native macrophyte population. We tested the allelopathic effects of aqueous leaf extracts of L. hexapetala on the photosynthetic activity of three target phytoplankton strains (Scenedesmus communis, a toxic Microcystis aeruginosa strain and a non‐toxic Microcystis aeruginosa strain) over three seasons of development (spring, summer and autumn). We also tested seasonal allelopathic effects of aqueous leaf extracts of both L. hexapetala (i.e. the non‐native invasive species) and the native Mentha aquatica on L. hexapetala seed germination. Finally, we identified three main secondary compounds present in the aqueous leaf extracts of L. hexapetala and we tested each individual compound on the phytoplankton's photosynthetic activity and on L. hexapetala seed germination. We observed marked seasonal and species‐specific patterns of L. hexapetala allelopathy on phytoplankton. The photosynthetic activities of S. communis and the toxic M. aeruginosa strain were stimulated by L. hexapetala aqueous leaf extracts in autumn and spring, respectively, whereas the non‐toxic M. aeruginosa strain was strongly inhibited in these two seasons. In summer, photosynthesis of all phytoplankton strains was inhibited. The germination rate of L. hexapetala seeds was stimulated by both L. hexapetala and M. aquatica aqueous leaf extracts, especially in summer, concomitant with the strong negative effects observed on the three phytoplankton strains. Three flavonoid glycosides (myricitrin, prunin and quercitrin) were identified as the main secondary compounds present in the L. hexapetala aqueous leaf extracts. The photosynthetic activity of S. communis was slightly stimulated by the three compounds. The photosynthetic activity of the toxic M. aeruginosa strain was stimulated by myricitrin and quercitrin, whereas that of the non‐toxic M. aeruginosa strain was inhibited by prunin. Finally, the germination rate and the germination velocity of L. hexapetala seeds were stimulated by myricitrin and prunin. These findings suggest that L. hexapetala could favour the photosynthetic activity of toxic cyanobacteria in spring and reduce their photosynthetic activity in summer, potentially leading to drastic changes in the phytoplankton communities and therewith ecological functioning of invaded ponds. Moreover, the stimulation of its seed germination could give a strong competitive advantage to L. hexapetala, thus promoting its invasiveness.

Phytochemical profile, cytotoxic, antioxidant, and allelopathic potentials of aqueous leaf extracts of Olea europaea

“…The inhibitory potential of allelopathy is complex, and different groups of chemicals can be involved such as phenolic compounds, terpenoids, flavonoids, alkaloids, amino acids, steroids, and carbohydrates (Al‐Samarai et al., 2018). It can be due to the congenital effects of plant containment in soluble substances in water and to biotic and the fluctuations of abiotic parameters, such as climatic conditions (Petrussa et al., 2013), the presence of herbivores and/or pathogens (Gatti et al., 2014; Silva, Overbeck, & Soares, 2014) and stage in the life history of the plant (Lombardo, Mjelde, Källqvist, & Brettum, 2013; Santonja, Le Rouzic, & Thiébaut, 2018; Thiébaut et al., 2018). In recent data, it was reported that the inhibitory activity may be attributed to the accumulation of glucosinolate in the plant parts, especially the leaves (Al‐Samarai et al., 2018).…”

Allelopathic effects of volatile organic compounds released from Pinus halepensis needles and roots

“…Interestingly, in contrast with the trend reported by Nektarios et al () with the use of P. halepensis needle leachates, we observed a clear increasing inhibitory effect related to VOC according to the evolution of needle physiological stage (green needle < senescent needle < needle litter). Since the allelochemicals released in leachates belong usually to phenolics (Fernandez et al, ; Santonja, Le Rouzic, et al, ), the water solubility, and rapid leaching of these compounds, could explain the decreasing allelopathic potentialities along needle physiological stages (Chomel et al, ; Hashoum et al, ). Santonja, Baldy, et al () and Chomel et al () reported that 40% and 80% of phenolics disappeared after 2 and 6 months of P. halepensis needle litter decomposition, respectively, supporting the findings of Nektarios et al ().…”

“…Seed germination percentage was calculated as [(number of germinated seeds)/(number of sown seeds)] × 100 (Bousquet-Mélou et al, 2005;Gavinet et al, 2019;Santonja, Le Rouzic, et al, 2018). Regarding seedling growth, root length (mm) was measured for each individual 5 days after germination (Fernandez et al, 2006(Fernandez et al, , 2013Hashoum et al, 2017).…”

“…A strong attention has been paid during the last decades to allelopathy, demonstrating the key implication of plantplant chemical interaction as a driver of plant community structure and ecosystem functioning (Inderjit, Wardle, Karban, & Callaway, 2011;Meiners, Kong, Ladwig, Pisula, & Lang, 2012;Wardle, Nilsson, Gallet, & Zackrisson, 1998). Seed germination and seedling performance are the main life stages usually affected by allelochemicals, and frequent negative allelopathic effects are inhibition of seed germination (Fernandez et al, 2013;Herranz, Ferrandis, Copete, Duro, & Zalacain, 2006), delay of seed germination (Fernandez et al, 2013;Hashoum et al, 2017), and inhibition of seedling growth (Gavinet et al, 2019;Santonja, Le Rouzic, & Thiebaut, 2018) by altering physiological processes (e.g., photosynthesis, nutrient uptake, cell division, or elongation; Inderjit & Duke, 2003). However, the persistence, availability, and biological impacts of the allelochemicals could be modulated by soil microbial communities (Cipollini, Rigsby, & Barto, 2012;Inderjit, 2005).…”

Soil scarification favors natural regeneration of Pinus pinea in Lebanon forests: Evidences from field and laboratory experiments

“…Seed germination and seedling performance are the main life stages usually affected by allelochemicals (i.e. phenolics or terpenoids), and frequent negative allelopathic effects are inhibition of seed germination (Herranz et al, 2006;Fernandez et al, 2013), delay of seed germination (Fernandez et al, 2013;Hashoum et al, 2017) and inhibition of seedling growth (Santonja et al, 2018;Gavinet et al, 2019). Several plant physiological processes such as photosynthesis, nutrient uptake, cell division or elongation can be influenced by the allelochemicals released (Chou, 1999;Inderjit and Duke, 2003).…”