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. | |||||||||||||||||||||||||||||
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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) | ParasaccharibacterapiumIn vitro | and | in vivo | anti-nosemosis activity. | Improvement of honey bee survival. | [126][137][66][67] | |||||||||||||||||||||||||
Brassica nigra | |||||||||||||||||||||||||||||||||
Honey bee | Organic | glucosinolates (glucoerucin, glucoraphanin, sinigrin) and isothiocyanates |
hive | Multiple strains: | Bifidobacterium | asteroides | DSM 20431 | Bifidobacterium | coryneforme | C155 | Bifidobacterium | indicumIn vivo | and | in vitro | reduction of | N. ceranae | infections, improvement of honey bee survival. | C449 | L. kunkeei | * Dan39 | L. plantarum | * Dan91 | L | . | johnsonii | Dan92 | Reduction of | Nosema | spores. | [68] | |||
[ | 138 | ] | Cryptocarya alba | Aqueous | terpenes and terpenoids (β-phellandrene, α-terpineol, eucalyptol) | Antimicrobial activity and reduction of | |||||||||||||||||||||||||||
Commercial | probiotic | Protexin | ® | ( | Enterococcus faecium | ) | Reduction of | N. ceranae | incidence increased the population of adult bees and increased honey production. | Nosema | spores. | [127][[69] | |||||||||||||||||||||
139 | ] | Cucurbita pepo | Ethanolic | ||||||||||||||||||||||||||||||
Bactocell | ® | ( | Pediococcus acidilactici | ) Levucell SBEssential Oils |
® | ( | Saccharomyces boulardii | ) | Improvement of honey bee survival. | [126] | Reduction of | Nosema | spores. | [61] | |||||||||||||||||||
Eleutherococcus senticosus | Ethanolic | saponins and flavonoids (eleutheroside B, eleutheroside E and naringenin) | |||||||||||||||||||||||||||||||
EM | ® | probiotic for bees: Multiple species of LAB and photosynthetic bacteria. |
Reduction of | Nosema | spores increased strength of colonies. | [128] | 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) | |||||||||||||||||||||||||||||||
APIFLORA (Biowet, Poland) lyophilized selected L | actobacillus | strains (Maria Curie-Skłodowska University in Lublin and University of Life Sciences in Lublin, Poland) | In vivo | Antagonistic effect toward | N. ceranae | and increased bee survival. and | in vitro | Available at: | https://biowet.pl/en/produkty/apiflora-2/ | accessed on 9 March 2022 reduction of | N. ceranae | infections, improvement of honey bee survival. | [68] | ||||||||||||||||||||
Eucalyptus globulus | Ethanolic | essential oils | Reduction of | Nosema | spores. | [61] | |||||||||||||||||||||||||||
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. | [ | 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.
The phytotherapeutic product Protofil®, rich in flavonoids (rutin and quercetin) and volatile compounds such as eucalyptol (1.8-cineol) and chavicol-methyl-ether, prevents the growth cycle of N. apis [75][76], but in the description of this hydroalcoholic extract, the mechanism of action is not specified. Other studies have evaluated the integration of the honey bee diet with vitamins and nitrogen compounds. Dietary supplementation with an amino acid and vitamin complex called “BEEWELL AminoPlus” (Provet, Ankara, Turkey) decreases N. ceranae spores and prevents bees from immune suppression by increasing the expression of genes for immune peptides (abaecin, apidaecin, hymenoptaecin, defensin and vitellogenin) [77] However, not always the products advertised as anti-nosemosis supplements have beneficial effects on honey bees infected with N. ceranae [78]. According to the study conducted by Botías et al. [79], three therapeutic agents (Nosestat®, Phenyl salicylate and Vitafeed Gold®) were screened to control N. ceranae infection in bee colonies and compared with the use of fumagillin. Nosestat® is a combination of iodine and formic acid and is commercialized for the treatment and prevention of nosemosis in bees. Vitafeed Gold® is a natural extract based on beet extract and molasses. None of the investigated products were effective against Nosema under the used experimental conditions. Among the natural products explored hitherto against nosemosis, there is propolis extract: a mixture of resinous substances collected by bees from various plant sources. Of the emerging effective treatments against N. ceranae, propolis extract is effective in three of the four bee species (A. cerana, A. mellifera and A. florea) [64][80][81][82][83][84].Source | Microbial Cultures | Relevant Reported Effects | Ref. | |||||||
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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 | |||||||||
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] |