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Nosemosis is a disease triggered by the single-celled spore-forming fungi Nosema apis and Nosema ceranae, which can cause extensive colony losses in honey bees (Apis mellifera L.). Fumagillin is an effective antibiotic treatment to control nosemosis, but due to its toxicity, it is currently banned in many countries. Accordingly, in the beekeeping sector, there is a strong demand for alternative ecological methods that can be used for the prevention and therapeutic control of nosemosis in honey bee colonies. Numerous studies have shown that plant extracts, RNA interference (RNAi) and beneficial microbes could provide viable non-antibiotic alternatives.
Plant Species | Extract | Bioactive Compounds | Relevant Reported Effects | Ref. |
---|---|---|---|---|
Achillea millefolium | Aqueous | terpenes and terpenoids (artemisia ketone, camphor, linalyl acetate and 1,8-cineole) | Antimicrobial activity, reduction of Nosema spores, improvement of honey bee survival. | [59] |
Agastache foeniculum | Ethanolic | phenolic acids and flavonoids (chlorogenic acid, isoquercitrin, quercetin, vanillin, acacetin, gallic acid, caffeic acid, p-OH cinnamic acid, resveratrol) | Reduction of Nosema spores. | [60] |
Allium sativum | Ethanolic | essential oils | Reduction of Nosema spores. | [61] |
Andrographis paniculata | Aqueous | terpenoids (andrographolide, dehydrographolide) | Reduction of Nosema spores; mitigation of gut epithelium degeneration caused by N. ceranae. | [62] |
Annona squamosa | Ethanolic | steroids, terpenes, alkaloids, flavonoids, saponins, phenolic acids | Reduction of Nosema spores. | [63] |
Aristotelia chilensis | Methanolic | phenolic acids, flavonoids (caffeic acid, apigenin and pinocembrin) | Reduction of N. ceranae spore loads, improvement of honey bee survival. |
[64] |
Artemisia absinthium | Ethanolic | flavonoids (isoquercitrin, quercetin, rutin) | Antimicrobial and antioxidant activity, reduction of Nosema spore loads. | [60][65] |
Artemisia dubia | Aqueous | benzopyrones, phenolic compounds and quinic acids derivatives (coumarin, chlorogenic acid, 4,5-dicaffaeoylquinic acid) | In vitro and in vivo anti-nosemosis activity. | [66][67] |
Aster scaber | Aqueous | benzopyrones, phenolic compounds and quinic acids derivatives (coumarin, chlorogenic acid, 4,5-dicaffaeoylquinic acid) | In vitro and in vivo anti-nosemosis activity. | [66][67] |
Brassica nigra | Organic | glucosinolates (glucoerucin, glucoraphanin, sinigrin) and isothiocyanates | In vivo and in vitro reduction of N. ceranae infections, improvement of honey bee survival. | [68] |
Cryptocarya alba | Aqueous | terpenes and terpenoids (β-phellandrene, α-terpineol, eucalyptol) | Antimicrobial activity and reduction of Nosema spores. | [69] |
Cucurbita pepo | Ethanolic | Essential Oils | Reduction of Nosema spores. | [61] |
Eleutherococcus senticosus | Ethanolic | saponins and flavonoids (eleutheroside B, eleutheroside E and naringenin) | Prophylactic effect in vivo against Nosema infections does not affect Nosema spores’ viability, improvement of honey bee survival. | [70] |
Eruca sativa | Hexan | glucosinolates (glucoerucin, glucoraphanin, sinigrin) | In vivo and in vitro reduction of N. ceranae infections, improvement of honey bee survival. | [68] |
Eucalyptus globulus | Ethanolic | essential oils | Reduction of Nosema spores. | [61] |
Evernia prunastri | Ethanolic | phenolic acids and flavonoids (chlorogenic acid, vanilic acid, vanillin, rosmarinic acid, crisin, o-Cumaric acid and acacetin) | Reduction of Nosema spores. | [60] |
Humulus lupulus | Ethanolic | flavonoids (isoquercitrin, rutin, epicatechin) | Reduction of Nosema spores. | [60] |
Laurus nobilis | Ethanolic | phenolic acids and flavonoids (syringic acid, isoquercitrin, quercetin, kaempferol, rutin, epicatechin, resveratrol and monoterpenes (1,8-cineole, sabinene and linalool) | Reduction of Nosema spores. | [59][60][71][72] |
Ocimum basilicum | Ethanolic | phenylpropanoid and phenylpropene (methyl eugenol, methyl chavicol) | Reduction of Nosema spores. | [63] |
Origanum vulgare | Ethanolic | phenolic acids, flavonoids (isoquercitrin, rosmarinic acid, apigenin, vitexin 2-o-ramnoside, sinapic acid, resveratrol) and essential Oils | Reduction of Nosema spores. | [60][73] |
Plantago lanceolata | Aqueous | flavonoids, alkaloids, terpenoids, phenolic compounds (caffeic acid derivatives), fatty acids, polysaccharides | Antimicrobial, antioxidant and cytotoxic activity; reduction of Nosema spores; improvement of honey bee survival. | [59] |
Psidium guajava | Ethanolic | terpenes (limonene, β-Pinene, α-Pinene, caryophyllene) | Reduction of Nosema spores. | [63] |
Rosmarinus officinalis | Aqueous | phenolic acid, terpenes and terpeinods (rosmarinic acid, caffeic acid, ursolic acid, betulinic acid, carnosic acid and carnosol, camphor, 1,8-cineole, α-pinene, borneol, camphene, β-pinene and limonene) | Antimicrobial and antioxidant activity, reduction of Nosema spores; improvement of honey bee survival. | [59] |
Rosmarinus officinalis | Hydroalcoholic | essential oils | Reduction of Nosema spores. | [73] |
Rumex acetosella | Aqueous | phenolic compounds and inorganic salt derivates (tannic acid, binoxalate of potassium, and nitrogenous matter) | Reduction of Nosema spores and improvement of honey bee survival. | [59] |
Salvia officinalis | Aqueous | terpenes and terpenoids (cis-thujone, camphor, cineole, humulene, trans-thujone, camphene, pinene, limonene, bornyl acetate and linalool) | Antimicrobial and antioxidant activity, reduction of Nosema spores, improvement of honey bee survival. | [59] |
Syzygium jambos | Ethanolic | phenolic compounds, anthraquinones, and steroids | Reduction of Nosema spores. | [63] |
Thymus vulgaris | Ethanolic | essential oils | Reduction of Nosema spores. | [61] |
Thymus vulgaris | Aqueous | terpenes and terpenoids (geraniol, linalool, gamma-terpineol, carvacrol, thymol and trans-thujan-4-ol/terpinen-4-ol, p-cymene, γ-terpinene and thymol) | Antimicrobial and antioxidant activity, reduction of Nosema spores, improvement of honey bee survival. | [59] |
Ugni molinae | Methanolic | phenolic acids (caffeic acid) | Reduction of N. ceranae spores and improvement of honey bee survival. | [64] |
Urtica dioica | Ethanolic | essential oils | Reduction of Nosema spores. | [61] |
Vaccinium myrtillus | Ethanolic | phenolic acids and flavonoids (chlorogenic acid, syringic acid, ferulic acid, isoquercitrin, quercetin, myricetin, naringenin, kaempferol) | Reduction of Nosema spores. | [60] |
Some scientific investigations have used products already available on the market. In the trial by Cilia et al. [74], the efficacy of two commercial products, ApiHerb® and Api-Bioxal®(Chemicals Laif SpA, Padua, Italy), was compared. ApiHerb® is composed of Allium sativum and Cinnamomum zeylanicum extracts. Instead, Api-Bioxal® is a registered veterinary drug against Varroa destructor containing oxalic acid dihydrate. While both treatments lowered the abundance of N. ceranae, ApiHerb® also diminished the prevalence of infected bees.
Source | Microbial Cultures | Relevant Reported Effects | Ref. |
---|---|---|---|
Honey bee gastrointestinal tract |
Lactobacillus johnsonii AJ5 L. johnsonii CRL1647 |
Oral administration of the metabolites produced by L. johnsonii (mainly organic acids) supplemented in syrup reduced the intensity of the disease. | [130][131] |
L. johnsonii CRL1647 | Reduction of Nosema spores. | [132] | |
Lactobacillus kunkeei * | [133] | ||
Lactobacillus salivarius * A3iob | [134] | ||
Lactobacillus plantarum * | The dysbiosis induced by Nosema spp. was lessened by the probiotic L. plantarum. | [121] | |
Bacillus subtilis subsp. Subtilis Mori2 | Reduction of Nosema incidence. | [135] | |
Honey samples |
B. subtilis | Surfactin S2, a cyclic lipopeptide produced by B. subtilis C4 exhibited statistically significant anti-Nosema activity. | [136] |
Bacillus sp. (PC2) | Improvement of honey bee survival. | [126] | |
Honey bee larvae |
Parasaccharibacterapium | Improvement of honey bee survival. | [126][137] |
Honey bee hive |
Multiple strains: Bifidobacterium asteroides DSM 20431 Bifidobacterium coryneforme C155 Bifidobacterium indicum C449 L. kunkeei * Dan39 L. plantarum * Dan91 L. johnsonii Dan92 |
Reduction of Nosema spores. | [138] |
Commercial probiotic |
Protexin® (Enterococcus faecium) | Reduction of N. ceranae incidence increased the population of adult bees and increased honey production. | [127][139] |
Bactocell® (Pediococcus acidilactici) Levucell SB® (Saccharomyces boulardii) |
Improvement of honey bee survival. | [126] | |
EM® probiotic for bees: Multiple species of LAB and photosynthetic bacteria. |
Reduction of Nosema spores increased strength of colonies. | [128] | |
APIFLORA (Biowet, Poland) lyophilized selected L actobacillus strains (Maria Curie-Skłodowska University in Lublin and University of Life Sciences in Lublin, Poland) | Antagonistic effect toward N. ceranae and increased bee survival. | Available at: https://biowet.pl/en/produkty/apiflora-2/ accessed on 9 March 2022 | |
VETAFARM: Lactobacillus acidophilus Lactobacillus delbruekii sub.bulgaricus L. plantarum * L. rhamnosus B. bifidum Enterococcus faecium |
Reduction of N. ceranae incidence increased the population of adult bees and increased honey production. | [127] | |
P. acidilactici (Lallemand SAS Blagnac, France | Regulate genes involved in honey bee development (vitellogenin), immunity (serine protease 40, defensin) and possibly prevent infection by the parasite N. ceranae. | [129] |