Biocontrol of Nosemosis in Honey Bees: Comparison
Please note this is a comparison between Version 1 by Massimo Iorizzo and Version 2 by Lindsay Dong.

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.

  • beneficial microbes
  • biocontrol
  • nosemosis
  • plant extract

1. Introduction

The microsporidia Nosema apis and Nosema ceranae are among the main pathogens of honey bees; they are spore-forming, obligate, intracellular parasites and are acknowledged as belonging to the kingdom of Fungi [1][2].
Most recently, Tokarev et al. [3] placed the Nosema species, which infects bees (Anthophila, Hymenoptera), under the new genus Vairimorpha. N. apis. This new genus was first isolated from the European honey bee Apis mellifera (Hymenoptera, Apidae), whereas N. ceranae was first reported from the Asian honey bee Apis cerana (Hymenoptera, Apidae). Currently, these two parasites have a worldwide distribution [4][5][6][7][8][9][10][11][12][13][14][15][16].
Both N. apis and N. ceranae are the etiological agents of nosemosis, one of the adult honey bee’s most widespread and serious diseases, causing significant economic losses to beekeepers [5][17][18][19]. N. apis is responsible for nosemosis type A, a disease that increases bee mortality in winter and causes a slow build-up in spring, making bees weak and reducing honey yield [20]. Field experiments demonstrated that N. apis infection is also responsible for the onset of foraging at a younger age than in healthy worker bees. [21][22]. Dosselli et al. [23] demonstrated that N. apis infected worker bees quickly altered their flight behavior, reducing the foraging trip duration and increasing the number of flights. In addition, the disease causes diarrhea and fecal spots inside and outside the hive [9]. Nosemosis type C, caused by N. ceranae [24], includes a wide range of effects on honey bee physiology and behavioral changes, weakness and colony mortality increase, decreased brood-rearing capacity and honey production, all of which may contribute to colony collapse [25][26][27][28][29][30][31]. Moreover, N. ceranae infection may lead to the impairment of hormone production and lipid synthesis [32][33], the induction of nutritional and energetic stress [32][34][35][36] and the degeneration of the host’s midgut tissues [37][38]. N. ceranae infection can also induce immune system suppression in the host [39][40]. Recently, different scholarauthors demonstrated that both N. apis and N. ceranae inhibit apoptosis in the host cells [41][42][43]. N. ceranae infection also affects the neurobiology of honey bees by impairing olfactory learning and memory [44] and, on a behavioral level, premature foraging in worker bees [29][34][45], decreased homing ability [46] and weaker flight ability [47].
The acquisition of Nosema occurs via the fecal-oral route through the ingestion of spores. In the midgut lumen, the spores extrude a polar filament through which the sporoplasm is transferred into the epithelial cells and merogony begins. Shortly, meronts can either turn into primary spores or mature spores; primary spores transmit the disease to adjacent cells, whereas mature spores are released into the midgut lumen, from which they can pass through the rectum into the feces or remain in the midgut to infect other cells [5][48][49][50][51]. The spores excreted by the host through the feces may then contaminate the nesting environment, comb, floral resources, collected pollen and water [20][26][52]. Beyond horizontal transmission (e.g., via trophallaxis) [53][54], both N. apis and N. ceranae may be airborne [55] and sexually transmitted [56][57]. Because of the disastrous consequences of Nosema infections, there is a strong demand for the management of these pathogens.

2. Plant Extracts

In recent years, several studies have evaluated plant extracts and organic compounds, reporting their effectiveness for the biocontrol of nosemosis [58] (Table 1).
Table 1.
List of plant species whose extracts, and relative bioactive compounds, are effective against nosemosis.
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.
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 beeOrganic

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

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: 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]

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].

3. RNA Interference

RNA interference (RNAi) is a post-transcriptional process triggered by the introduction of double-stranded RNA (dsRNA) as a tool that limits the transcript level by either suppressing transcription (transcriptional gene silencing [TGS]) or activating a sequence-specific RNA degradation process (post-transcriptional gene silencing [PTGS]/RNA interference [RNAi]) [85][86]. RNA interference (RNAi) is currently being explored for pesticide activity in agriculture and as a potent and specific strategy for controlling infections of parasites and pathogens in insects, including honey bees [87][88][89][90][91][92][93][94]. Several studies evidence that RNAi might be exploited to regulate Nosema gene expression within bee hosts [95][96][97].

4. Beneficial Microbes

The gut microbiota plays a key role in the maintenance of honey bee health, contributing to growth and development, immune function and protection against pathogens [98][99][100]. However, the honey bee microbiota is destabilized (dysbiosis) by natural events such as immunosenescence or by various exogenous factors such as climate, diet, nutritional deficiencies, pathogens, pesticides and environmental pollution [101][102][103][104][105][106][107][108]. The functional outcomes of dysbiosis include poor host development, early mortality and increased susceptibility of bees to pathogens [99][102][109][110][111]. Recent studies provide experimental evidence for a link between nosemosis and dysbiosis in the honey bees’ gut [112][113][114][115][116][117][118][119][120][121][122]. Other studies suggested that management strategies based on re-establishing the microbiota are a promising path to restoring or improving the health of honey bees and that probiotics and several bacterial metabolites may participate in the control of nosemosis, other than increase the survival of infected honey bees [123][124][125][126][127]. Table 2 provides a detailed list of the main effects obtained in the biocontrol of Nosema spp. through the use of different microbial cultures. As shown in Table 2, the most commonly used bacteria belong to the group of lactic acid bacteria and specifically to the species related to Bifidobacterium, Enterococcus and Pediococcus. The action of these bacteria is expressed essentially through an antimicrobial action directed against Nosema [126][128] or through the stimulation of the immune system of the honey bee [129].
Table 2.
Overview of the main effects obtained in the biocontrol of
using different microbial cultures.
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]

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

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]
* Taxonomic correspondence: Lactobacillus kunkeei (currently Apilactobacillus kunkeei); Lactobacillus plantarum (currently Lactiplanbacillus plantarum); Lactobacillus salivarius (currently Ligilactobacillus salivarius).

5. Conclusions

The use in beekeeping practice of beneficial microbes, plant extracts and RNAi has enormous potential for biocontrol of nosemosis. However, for systematic application, further studies are needed for these techniques to become reliable and effective tools. The antimicrobial activity of plant extract is mainly due to the presence of phenolic compounds and terpenoids, which possess well-known antimicrobial activity. The effect that these substances may have on bee gut microflora and symbiotic LAB, however, is not fully known. Regarding the RNAi-based antiviral effect, the molecular mechanisms have not been thoroughly characterized, and little is known about the optimal RNAi delivery method for treating honey bees at different developmental stages. The use of appropriate probiotics, unlike synthetic or natural chemical compounds, does not adversely affect the balance of the gut microbiota and is also a technique that can help prevent and treat nosemosis as well as positively impact honey bee welfare.


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