Silent effect of the fungicide pyraclostrobin on the larval exposure of the non-target organism Africanized Apis mellifera and its interaction with the pathogen Nosema ceranae in adulthood

Honeybees, Apis mellifera, are important pollinators of many economically important crops. However, one of the reasons for their decline is pathogenic infection. Nosema disease and American foulbrood (AFB) disease are the most common bee pathogens that propagate in the gut of honeybees. This study investigated the impact of gut-propagating pathogens, including Nosema ceranae and Paenibacillus larvae, on bacterial communities in the gut of A. mellifera using 454-pyrosequencing. Pyrosequencing results showed that N. ceranae was implicated in the elimination of Serratia and the dramatic increase in Snodgrassella and Bartonella in adult bees’ guts, while bacterial communities of P. larvae-infected larvae were not affected by the infection. The results indicated that only N. ceranae had an impact on some core bacteria in the gut of A. mellifera through increasing core gut bacteria, therefore leading to the induction of dysbiosis in the bees’ gut.

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Effects of Prebiotics and Probiotics on Honey Bees (Apis mellifera) Infected with the Microsporidian Parasite Nosema ceranae

Microorganisms ◽

10.3390/microorganisms9030481 ◽

2021 ◽

Vol 9 (3) ◽

pp. 481

Author(s):

Daniel Borges ◽

Ernesto Guzman-Novoa ◽

Paul H. Goodwin

Keyword(s):

Apis Mellifera ◽

Honey Bees ◽

Bifidobacterium Bifidum ◽

Nosema Ceranae ◽

Food Supplementation ◽

Microsporidian Parasite ◽

Single Strain ◽

Acacia Gum ◽

Bee Health ◽

Commercial Probiotics

Nosema ceranae is a microsporidian fungus that parasitizes the midgut epithelial cells of honey bees, Apis mellifera. Due to the role that midgut microorganisms play in bee health and immunity, food supplementation with prebiotics and probiotics may assist in the control of N. ceranae. The dietary fiber prebiotics acacia gum, inulin, and fructooligosaccharides, as well as the commercial probiotics Vetafarm Probotic, Protexin Concentrate single-strain (Enterococcus faecium), and Protexin Concentrate multi-strain (Lactobacillus acidophilus, L. plantarum, L. rhamnosus, L. delbrueckii, Bifidobacterium bifidum, Streptococcus salivarius, and E. faecium) were tested for their effect on N. ceranae spore loads and honey bee survivorship. Bees kept in cages were inoculated with N. ceranae spores and single-dose treatments were administered in sugar syrup. Acacia gum caused the greatest reduction in N. ceranae spore numbers (67%) but also significantly increased bee mortality (62.2%). However, Protexin Concentrate single-strain gave similarly reduced spore numbers (59%) without affecting the mortality. In a second experiment, multiple doses of the probiotics revealed significantly reduced spore numbers with 2.50 mg/mL Vetafarm Probotic, and 0.25, 1.25, and 2.50 mg/mL Protexin Concentrate single-strain. Mortality was also significantly reduced with 1.25 mg/mL Protexin Concentrate single-strain. N. ceranae-inoculated bees fed 3.75 mg/mL Vetafarm Probotic had higher survival than N. ceranae-inoculated bees, which was similar to that of non-inoculated bees, while N. ceranae-inoculated bees fed 2.50 mg/mL Protexin Concentrate single-strain, had significantly higher survival than both N. ceranae-inoculated and non-inoculated bees. Protexin Concentrate single-strain is promising as it can reduce N. ceranae proliferation and increase bee survivorship of infected bees, even compared to healthy, non-infected bees.

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Effects of Nosema ceranae (Dissociodihaplophasida: Nosematidae) and Flupyradifurone on Olfactory Learning in Honey Bees, Apis mellifera (Hymenoptera: Apidae)

Journal of Insect Science ◽

10.1093/jisesa/ieaa130 ◽

2020 ◽

Vol 20 (6) ◽

Author(s):

Heather Christine Bell ◽

Corina N Montgomery ◽

Jaime E Benavides ◽

James C Nieh

Keyword(s):

Apis Mellifera ◽

Learning And Memory ◽

Honey Bees ◽

Food Reward ◽

Nosema Ceranae ◽

Olfactory Conditioning ◽

Agricultural Use ◽

High Doses ◽

Neonicotinoid Pesticides ◽

Term Field

Abstract The health of insect pollinators, particularly the honey bee, Apis mellifera (Linnaeus, 1758), is a major concern for agriculture and ecosystem health. In response to mounting evidence supporting the detrimental effects of neonicotinoid pesticides on pollinators, a novel ‘bee safe’ butenolide compound, flupyradifurone (FPF) has been registered for use in agricultural use. Although FPF is not a neonicotinoid, like neonicotinoids, it is an excitotoxic nicotinic acetylcholine receptor agonist. In addition, A. mellifera faces threats from pathogens, such as the microsporidian endoparasite, Nosema ceranae (Fries et al. 1996). We therefore sought 1) to increase our understanding of the potential effects of FPF on honey bees by focusing on a crucial behavior, the ability to learn and remember an odor associated with a food reward, and 2) to test for a potential synergistic effect on such learning by exposure to FPF and infection with N. ceranae. We found little evidence that FPF significantly alters learning and memory at short-term field-realistic doses. However, at high doses and at chronic, field-realistic exposure, FPF did reduce learning and memory in an olfactory conditioning task. Infection with N. ceranae also reduced learning, but there was no synergy (no significant interaction) between N. ceranae and exposure to FPF. These results suggest the importance of continued studies on the chronic effects of FPF.

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Nosema ceranae has been infecting honey bees Apis mellifera in Italy since at least 1993

Journal of Apicultural Research ◽

10.3896/ibra.1.52.2.11 ◽

2013 ◽

Vol 52 (2) ◽

pp. 60-61 ◽

Cited By ~ 13

Author(s):

Ezio Ferroglio ◽

Stefania Zanet ◽

Nancy Peraldo ◽

Elisa Tachis ◽

Anna Trisciuoglio ◽

...

Keyword(s):

Apis Mellifera ◽

Honey Bees ◽

Nosema Ceranae

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Natural extracts as potential control agents for Nosema ceranae infection in honeybees, Apis mellifera

Journal of Invertebrate Pathology ◽

10.1016/j.jip.2021.107688 ◽

2021 ◽

pp. 107688

Author(s):

Veeranan Chaimanee ◽

Aticha Kasem ◽

Tananya Nuanjohn ◽

Thummanoon Boonmee ◽

Apiradee Siangsuepchart ◽

...

Keyword(s):

Apis Mellifera ◽

Nosema Ceranae ◽

Potential Control ◽

Natural Extracts

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Dynamics of Nosema apis and Nosema ceranae Co-Infection Seasonally in Honey Bee (Apis mellifera L.) Colonies

Journal of Apicultural Science ◽

10.2478/jas-2019-0001 ◽

2019 ◽

Vol 63 (1) ◽

pp. 41-48 ◽

Cited By ~ 1

Author(s):

Asli Özkırım ◽

Aygün Schiesser ◽

Nevіn Keskin

Keyword(s):

Apis Mellifera ◽

Apis Cerana ◽

Winter Season ◽

Nosema Ceranae ◽

Molecular Techniques ◽

Winter Period ◽

Nosema Apis ◽

Infection Level ◽

Seasonal Infection ◽

Asian Honeybee

AbstractNosema apis is a pathogen spesific for the European honeybee, Apis mellifera L., while Nosema ceranae is specific for the Asian honeybee, Apis cerana. Turkey provides different environmental and host conditions for both Nosema species. The aim of the study is to determine the dynamic of N. cerenae and N. apis seasonal infection. A number of samples were collected from different apiaries between 2009-2016 years. The samples were kept at −20°C in the laboratory. Light microscopy was used for spore counting and molecular techniques were used to identify the Nosema species. The results showed that winter season had an impact on the type of Nosema as well as on infection rates. The number of N. ceranae spores decreases significantly at low temperatures (≤ 5°C). The winter period was found to be the main factor affecting nosema infection level and dominancy of Nosema ceranae. Furthermore, co-infection of both species is an indicator of the dynamics of N. apis and N. ceranae. This study suggests, that there is a dynamic prevalence among the Nosema species depending of the average winter temperature and not a replacement of N. apis by N. ceranae.

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Permanent prevalence of Nosema ceranae in honey bees (Apis mellifera) in Hungary

Acta Veterinaria Hungarica ◽

10.1556/004.2015.034 ◽

2015 ◽

Vol 63 (3) ◽

pp. 358-369 ◽

Cited By ~ 1

Author(s):

Tamás Csáki ◽

Miklós Heltai ◽

Ferenc Markolt ◽

Balázs Kovács ◽

László Békési ◽

...

Keyword(s):

Apis Mellifera ◽

Honey Bees ◽

Mediterranean Climate ◽

Laboratory Method ◽

Seasonal Distribution ◽

Nosema Ceranae ◽

Infection Rates ◽

Infection Level ◽

Spore Count ◽

The Mean

Nosema ceranae is present in honey bee (Apis mellifera L.) colonies worldwide. Studies on the comparative virulence of N. ceranae and N. apis showed significant differences in individual mortality, and the prevalence of N. ceranae seems to be predominant in both the continental and the Mediterranean climate regions. This study attempted to monitor the geographical and seasonal distribution of these two Nosema species in Hungary, using a simple laboratory method. The distribution of N. ceranae and N. apis infection rates along all seasons was homogeneous (P = 0.57). In co-infected samples, the intensity of N. ceranae infection was always significantly higher than that of N. apis infection (P < 0.001). The infection rate of infected bees in exterior samples was higher than in interior samples in each season; however, the differences were not statistically significant. The species N. ceranae had been present in Hungary already in 2004. Statistical analysis of data shows that the infection level is best represented by sampling exterior bees to establish the proportion of infected bees rather than by determining the mean spore count.

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