Differential Effects of the Allelochemical Juglone on Growth of Harmful and Non-Target Freshwater Algae

Abstract

Allelopathy has been applied to control nuisance algae in aquatic systems, but the effects of allelochemicals on the broad spectrum of algae are not well understood. We investigate algicidal effects of the allelochemical juglone on the bloom-forming, harmful algae Microcystis aeruginosa and Stephanodiscus hantzschii, and on several non-target algal species including cyanobacteria (Anabaena flos–aquae, Oscillatoria curviceps, and Phormidium subfuscum), diatoms (Asterionella formosa, Fragilaria crotonensis, and Synedra acus), and green algae (Chlorella vulgaris, Scenedesmus ecornis, and Scenedesmus quadricauda), in laboratory and field enclosure bioassays. Under three treatment concentrations (0.01, 0.1, and 1 mg L−1) of juglone, Microcystis cell density is significantly reduced by 35–93%. Concentrations of 0.1 and 1 mg L−1 inhibits Stephanodiscus growth almost equally (66% and 75%, respectively). To contrast, juglone produces a stimulatory allelopathic effect on three green algae, and other tested diatoms showed hormesis. Overall, the cyanobacteria are more sensitive to juglone than the green algae and diatoms. These results indicate that the allelopathic effects of juglone on microalgae vary depending on their characteristic cellular morphology and anatomy.

Agricultural Uses of Juglone: Opportunities and Challenges

“…Stimulation of a particular trait in one species at a given concentration may not be the same in another species. For example, at 5.7 µM, juglone inhibited the growth of Stephanodiscus hantzschii by more than 60%, while at the same time exhibited hormetic activity on three other diatoms, Asterionella formosa, Fragilaria crotonensis, and Synedra acus [92]. Along the same lines, Table 1 summarizes a range of reported inhibitory and stimulatory effects of juglone, juglone-producing species, and juglone-containing materials on various plant species.…”

“…Growth of Streptophytic (Closterium acerosum, Micrasterias thomasiana, and Spirogyra grevilleana) and chlorophytic (Pandorina morum and Eudorina californica) freshwater green algae is also inhibited by juglone at concentrations ranging from 0.1-1 mM [91]. Interestingly, lower concentrations, 0.1-1 mg L −1 (0.57-5.7 µM), were found to stimulate growth of chlorophytic freshwater green algae Chlorella vulgaris, Scenedesmus ecornis, and S. quadricauda and the freshwater diatoms Asterionella formosa, Fragilaria crotonensis, and Synedra acus [92]. Park et al [92] also found that juglone can inhibit the harmful bloom-forming nuisance cyanobacterium Microcystis aeruginosa and the freshwater diatom Stephanodiscus hantzschii by up to 93% and 75%, respectively, at 1 mg L −1 (5.7 µM).…”

“…Interestingly, lower concentrations, 0.1-1 mg L −1 (0.57-5.7 µM), were found to stimulate growth of chlorophytic freshwater green algae Chlorella vulgaris, Scenedesmus ecornis, and S. quadricauda and the freshwater diatoms Asterionella formosa, Fragilaria crotonensis, and Synedra acus [92]. Park et al [92] also found that juglone can inhibit the harmful bloom-forming nuisance cyanobacterium Microcystis aeruginosa and the freshwater diatom Stephanodiscus hantzschii by up to 93% and 75%, respectively, at 1 mg L −1 (5.7 µM). The same study found that even less juglone (0.1 mg L −1 ; 0.57 µM) inhibits growth of the cyanobacterial species A. flos-aquae, Oscillatoria curviceps, and Phormidium subfuscum.…”

“…This is important to consider for allelochemicals like juglone given that under natural settings soil concentrations may not be sufficient to achieve inhibitory effects observed in vitro or in other controlled conditions, and instead have a biostimulatory effect. Indeed, the presence of J. nigra has been reported to improve forage cover in pastures [134] and bioassays have indicated that at low concentrations (typically ≤ 1 µM) juglone exhibits biostimulatory activity e.g., [1,92,118,135]. Other studies (e.g., [136]) have indicated similar effects testing dilutions of extracts from juglone-containing plant materials.…”

Low Levels of Contaminants Stimulate Harmful Algal Organisms and Enrich Their Toxins

“…Low, sub-NOAEL concentrations of contaminants may also lead to changes in the species composition of algal assemblages. ,, They may even impair the chemosensory system of organisms depending on dissolved chemical cues for their survival by depleting inorganic carbon and highly elevating pH due to increased photosynthesis. , For example, low, environmentally relevant, stimulatory doses of a mixture of ciprofloxacin, sulfamethoxazole, and tetracycline antibiotics could enhance the competitiveness and increase the proportion of the “harmful” M. aeruginosa in a mixed culture of four phytoplankton species . Similarly, algaecidal hydrogen peroxide at 0.2 mg L –1 increased and at 0.5–1.5 mg L –1 decreased the relative abundance of Anabeana , Microcystis , and Oscillatoria within a community of cyanobacteria and the relative abundance of Cyanobacteria within a prokaryotic community .…”