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The health and sustainability of honeybee populations are essential for global food production and ecological balance. More than one-third of agricultural crops depend on pollination, making honeybees indispensable to the global economy. However, colonies worldwide are increasingly threatened by the gut parasite Nosema ceranae , whose recurrent outbreaks cause severe productivity losses and economic damage to the apicultural and agricultural sectors. Despite its prevalence, the nonlinear mechanisms responsible for the persistence and resurgence of Nosema ceranae remain poorly understood. This study aims to develop a mathematical model that interpret the complex epidemiological behaviour of Nosema ceranae under realistic biological conditions, specifically focusing on renewal of colony-level susceptibility and the strained resources available for control and management. A nonlinear Susceptible-Infected-Recovered-Susceptible (SIRS) model incorporating renewal of colony-level susceptibility and resource saturation is formulated and analysed using stability theory and numerical bifurcation techniques. Analytical derivations identify the conditions for transcritical and Hopf bifurcations, while numerical continuation analysis and time series simulations validate the theoretical predictions and reveal the rich dynamical structure. The analysis uncovers two critical thresholds governing colony dynamics. A forward (transcritical) bifurcation marks the transition from disease eradication to endemic persistence, while a Hopf bifurcation arising from resource limitations induces sustained oscillations representing recurrent infection waves. The coexistence of stable equilibria and periodic orbits highlights bistability, indicating that small perturbations or change in control interventions can trigger large amplitude outbreaks. These nonlinear feedbacks provide a mechanistic explanation for the cyclical prevalence of Nosema ceranae observed in distinct colonies. The proposed framework establishes, for the first time, how the interplay between partial recovery and limited resource availability can drive complex epidemic patterns in honeybee colonies. Beyond its theoretical contribution, the study provides actionable insight for the agriculture industry: efficient allocation of control resources and timely interventions are essential to prevent recurrent epidemics that threaten pollination services and agricultural productivity. The results bridge mathematical modelling and ecological management, offering a predictive foundation for mitigating the economic and environmental impact of Nosema ceranae on global food security.

The Western honey bee (Apis mellifera L., Hymenoptera: Apidae) is a species of crucial economic, agricultural and environmental importance. In the last ten years, some regions of the world have suffered from a significant reduction of honey bee colonies. In fact, honey bee losses are not an unusual phenomenon, but in many countries worldwide there has been a notable decrease in honey bee colonies. The cases in the USA, in many European countries, and in the Middle East have received considerable attention, mostly due to the absence of an easily identifiable cause. It has been difficult to determine the main factors leading to colony losses because of honey bees’ diverse social behavior. Moreover, in their daily routine, they make contact with many agents of the environment and are exposed to a plethora of human activities and their consequences. Nevertheless, various factors have been considered to be contributing to honey bee losses, and recent investigations have established some of the most important ones, in particular, pests and diseases, bee management, including bee keeping practices and breeding, the change in climatic conditions, agricultural practices, and the use of pesticides. The global picture highlights the ectoparasitic mite Varroa destructor as a major factor in colony loss. Last but not least, microsporidian parasites, mainly Nosema ceranae, also contribute to the problem. Thus, it is obvious that there are many factors affecting honey bee colony losses globally. Increased monitoring and scientific research should throw new light on the factors involved in recent honey bee colony losses. The present review focuses on the main factors which have been found to have an impact on the increase in honey bee colony losses.

Nosemosis, caused by microsporidian parasites of the genus Nosema , is considered a significant health concern for insect pollinators, including the economically important honeybee ( Apis mellifera ). Despite its acknowledged importance, the impact of this disease on honeybee survivorship remains unclear. Here, a standard laboratory cage trial was used to compare mortality rates between healthy and Nosema -infected honeybees. Additionally, a systematic review and meta-analysis of existing literature were conducted to explore how nosemosis contributes to increased mortality in honeybees tested under standard conditions. The review and meta-analysis included 50 studies that reported relevant experiments involving healthy and Nosema -infected individuals. Studies lacking survivorship curves or information on potential moderators, such as spore inoculation dose, age of inoculated bees, or factors that may impact energy expenditure, were excluded. Both the experimental results and meta-analysis revealed a consistent, robust effect of infection, indicating a threefold increase in mortality among the infected group of honeybee workers (hazard ratio for infected individuals = 3.16 [1.97–5.07] and 2.99 [2.36–3.79] in the experiment and meta-analysis, respectively). However, the meta-analysis also indicated high heterogeneity in the effect magnitude, which was not explained by our moderators. Furthermore, there was a serious risk of bias within studies and potential publication bias across studies. The findings underscore knowledge gaps in the literature. It is stressed that laboratory cage trials should be viewed as an initial step in evaluating the impact of Nosema on mortality and that complementary field and apiary studies are essential for identifying effective treatments to preserve honeybee populations.

Recent declines in honey bee populations and increasing demand for insect-pollinated crops raise concerns about pollinator shortages. Pesticide exposure and pathogens may interact to have strong negative effects on managed honey bee colonies. Such findings are of great concern given the large numbers and high levels of pesticides found in honey bee colonies. Thus it is crucial to determine how field-relevant combinations and loads of pesticides affect bee health. We collected pollen from bee hives in seven major crops to determine 1) what types of pesticides bees are exposed to when rented for pollination of various crops and 2) how field-relevant pesticide blends affect bees’ susceptibility to the gut parasite Nosema ceranae . Our samples represent pollen collected by foragers for use by the colony, and do not necessarily indicate foragers’ roles as pollinators. In blueberry, cranberry, cucumber, pumpkin and watermelon bees collected pollen almost exclusively from weeds and wildflowers during our sampling. Thus more attention must be paid to how honey bees are exposed to pesticides outside of the field in which they are placed. We detected 35 different pesticides in the sampled pollen, and found high fungicide loads. The insecticides esfenvalerate and phosmet were at a concentration higher than their median lethal dose in at least one pollen sample. While fungicides are typically seen as fairly safe for honey bees, we found an increased probability of Nosema infection in bees that consumed pollen with a higher fungicide load. Our results highlight a need for research on sub-lethal effects of fungicides and other chemicals that bees placed in an agricultural setting are exposed to.

Microsporidium Nosema ceranae is well known for exerting a negative impact on honey bee health, including down-regulation of immunoregulatory genes. Protein nutrition has been proven to have beneficial effects on bee immunity and other aspects of bee health. Bearing this in mind, the aim of our study was to evaluate the potential of a dietary amino acid and vitamin complex \"BEEWELL AminoPlus\" to protect honey bees from immunosuppression induced by N. ceranae. In a laboratory experiment bees were infected with N. ceranae and treated with supplement on first, third, sixth and ninth day after emergence. The expression of genes for immune-related peptides (abaecin, apidaecin, hymenoptaecin, defensin and vitellogenin) was compared between groups. The results revealed significantly lower (p<0.01 or p<0.001) numbers of Nosema spores in supplemented groups than in the control especially on day 12 post infection. With the exception of abacein, the expression levels of immune-related peptides were significantly suppressed (p<0.01 or p<0.001) in control group on the 12th day post infection, compared to bees that received the supplement. It was supposed that N. ceranae had a negative impact on bee immunity and that the tested amino acid and vitamin complex modified the expression of immune-related genes in honey bees compromised by infection, suggesting immune-stimulation that reflects in the increase in resistance to diseases and reduced bee mortality. The supplement exerted best efficacy when applied simultaneously with Nosema infection, which can help us to assume the most suitable period for its application in the hive.

Honeybees are important pollinators, having an essential role in the ecology of natural and agricultural environments. Honeybee colony losses episodes reported worldwide and have been associated with different pests and pathogens, pesticide exposure, and nutritional stress. This nutritional stress is related to the increase in monoculture areas which leads to a reduction of pollen availability and diversity. In this study, we examined whether nutritional stress affects honeybee gut microbiota, bee immunity, and infection by Nosema ceranae, under laboratory conditions. Consumption of Eucalyptus grandis pollen was used as a nutritionally poor-quality diet to study nutritional stress, in contraposition to the consumption of polyfloral pollen. Honeybees feed with Eucalyptus grandis pollen showed a lower abundance of Lactobacillus mellifer and Lactobacillus apis (Firm-4 and Firm-5, respectively) and Bifidobacterium spp. and a higher abundance of Bartonella apis, than honeybees fed with polyfloral pollen. Besides the impact of nutritional stress on honeybee microbiota, it also decreased the expression levels of vitellogenin and genes associated to immunity (glucose oxidase, hymenoptaecin and lysozyme). Finally, Eucalyptus grandis pollen favored the multiplication of Nosema ceranae. These results show that nutritional stress impacts the honeybee gut microbiota, having consequences on honeybee immunity and pathogen development. Those results may be useful to understand the influence of modern agriculture on honeybee health.

Nosema ceranae is an intracellular parasite invading the midgut of honeybees, which causes serious nosemosis implicated in honeybee colony losses worldwide. The core gut microbiota is involved in protecting against parasitism, and the genetically engineering of the native gut symbionts provides a novel and efficient way to fight pathogens. Here, using laboratory-generated bees mono-associated with gut members, we find that Snodgrassella alvi inhibit microsporidia proliferation, potentially via the stimulation of host oxidant-mediated immune response. Accordingly, N. ceranae employs the thioredoxin and glutathione systems to defend against oxidative stress and maintain a balanced redox equilibrium, which is essential for the infection process. We knock down the gene expression using nanoparticle-mediated RNA interference, which targets the γ-glutamyl-cysteine synthetase and thioredoxin reductase genes of microsporidia. It significantly reduces the spore load, confirming the importance of the antioxidant mechanism for the intracellular invasion of the N. ceranae parasite. Finally, we genetically modify the symbiotic S. alvi to deliver dsRNA corresponding to the genes involved in the redox system of the microsporidia. The engineered S. alvi induces RNA interference and represses parasite gene expression, thereby inhibits the parasitism significantly. Specifically, N. ceranae is most suppressed by the recombinant strain corresponding to the glutathione synthetase or by a mixture of bacteria expressing variable dsRNA. Our findings extend our previous understanding of the protection of gut symbionts against N. ceranae and provide a symbiont-mediated RNAi system for inhibiting microsporidia infection in honeybees. Microsporidia parasitism affect honeybees health and has been implicated in colony losses. Here, the authors show that members of the honeybee gut microbiota inhibit microsporidia proliferation, and engineer a gut symbiont that protects against Nosema ceranae infection via inhibiting its redox system.

It has been suggested that the widespread use of neonicotinoid insecticides threatens bees, but research on this topic has been surrounded by controversy. In order to synthesize which research approaches have been used to examine the effect of neonicotinoids on bees and to identify knowledge gaps, we systematically reviewed research on this subject that was available on the Web of Science and PubMed in June 2015. Most of the 216 primary research studies were conducted in Europe or North America (82%), involved the neonicotinoid imidacloprid (78%), and concerned the western honey bee Apis mellifera (75%). Thus, little seems to be known about neonicotinoids and bees in areas outside Europe and North America. Furthermore, because there is considerable variation in ecological traits among bee taxa, studies on honey bees are not likely to fully predict impacts of neonicotinoids on other species. Studies on crops were dominated by seed-treated maize, oilseed rape (canola) and sunflower, whereas less is known about potential side effects on bees from the use of other application methods on insect pollinated fruit and vegetable crops, or on lawns and ornamental plants. Laboratory approaches were most common, and we suggest that their capability to infer real-world consequences are improved when combined with information from field studies about realistic exposures to neonicotinoids. Studies using field approaches often examined only bee exposure to neonicotinoids and more field studies are needed that measure impacts of exposure. Most studies measured effects on individual bees. We suggest that effects on the individual bee should be linked to both mechanisms at the sub-individual level and also to the consequences for the colony and wider bee populations. As bees are increasingly facing multiple interacting pressures future research needs to clarify the role of neonicotinoids in relative to other drivers of bee declines.

Pathogen spillover from managed bees is increasingly considered as a possible cause of pollinator decline. Though spillover has been frequently documented, evidence of the pathogen's virulence in the new host or mechanism of transmission is rare. Stingless bees (Apocrita: Meliponini) are crucial pollinators pan-tropically and overlap with managed honeybees ( Apis mellifera ) in much of their range. Nosema ceranae is the most prevalent disease of adult A. mellifera. We used laboratory experiments and field surveys to investigate the susceptibility of stingless bees ( Tetragonula hockingsi ) to N. ceranae , infection prevalence and transmissibility via flowers. We found that 67% of T. hockingsi fed sucrose with N. ceranae had detectable spores in their ventriculus, and they died at 2.96 times the rate of sucrose-only fed bees. Five of six field hives harboured bees with N. ceranae present at least once during our five-month survey, with prevalence up to 20%. In our floral transmission experiment, 67% of inflorescences exposed to infected A. mellifera yielded N. ceranae spores, and all resulted in T. hockingsi with N. ceranae spores in their guts. We conclude that N. ceranae is virulent in T. hockingsi under laboratory conditions, is common in the local T. hockingsi population and is transmissible via flowers.

Honey bee colonies are highly dependent upon the availability of floral resources from which they get the nutrients (notably pollen) necessary to their development and survival. However, foraging areas are currently affected by the intensification of agriculture and landscape alteration. Bees are therefore confronted to disparities in time and space of floral resource abundance, type and diversity, which might provide inadequate nutrition and endanger colonies. The beneficial influence of pollen availability on bee health is well-established but whether quality and diversity of pollen diets can modify bee health remains largely unknown. We therefore tested the influence of pollen diet quality (different monofloral pollens) and diversity (polyfloral pollen diet) on the physiology of young nurse bees, which have a distinct nutritional physiology (e.g. hypopharyngeal gland development and vitellogenin level), and on the tolerance to the microsporidian parasite Nosemaceranae by measuring bee survival and the activity of different enzymes potentially involved in bee health and defense response (glutathione-S-transferase (detoxification), phenoloxidase (immunity) and alkaline phosphatase (metabolism)). We found that both nurse bee physiology and the tolerance to the parasite were affected by pollen quality. Pollen diet diversity had no effect on the nurse bee physiology and the survival of healthy bees. However, when parasitized, bees fed with the polyfloral blend lived longer than bees fed with monofloral pollens, excepted for the protein-richest monofloral pollen. Furthermore, the survival was positively correlated to alkaline phosphatase activity in healthy bees and to phenoloxydase activities in infected bees. Our results support the idea that both the quality and diversity (in a specific context) of pollen can shape bee physiology and might help to better understand the influence of agriculture and land-use intensification on bee nutrition and health.