A growing pandemic: A review of Nosema parasites in globally distributed domesticated and native bees

Abstract

Nosema infection in bees Domesticated and native bees face a variety of deadly threats that cause mortality and reduced fecundity and thus, by extension, endanger agriculture and native plant communities that rely on bees for pollination. Biotic factors negatively impacting bees include: viruses, nematodes, mites, bacteria, and fungi. Additionally, abiotic threats include the destruction of nesting and floral resources from anthropogenic sources as well as a plethora of negative factors from climate change. While a substantial amount of research has been done investigating the causes of colony collapse disorder in the European honey bee, Apis mellifera, there is growing evidence over the past two decades that another pandemic of bees, both domesticated and native, is growing. This pandemic is the result of the spread of fungal pathogens in the genus Nosema. Nosema species belong to Microsporidia, which are all unicellular, obligate symbionts of animals, and gregarines. Although long thought to be protists, Microsporidia are now recognized as a highly reduced lineage of fungi [1]. Tokarev and colleagues [2] recently placed Nosema species that infect bees (Anthophila, Hymenoptera) within a new genus, Vairimorpha, but for the sake of consistency with the existing literature this Review article will refer to them simply as Nosema. Specifically, Nosema carry out their life cycle by infecting the cells in the midgut of bees. Once a spore is ingested by a bee and reaches the midgut, it will germinate. It then injects its contents into the host cell where it consumes the cell contents via phagocytosis until it eventually lays down spore walls before rupturing the host cell to release the spores [3]. These spores can then infect other cells in the digestive tract or be passed out of the host in excrement, thereby contaminating floral resources, collected pollen, and the nesting environment. Other bees are then susceptible to ingest spores in the nest via fecal-oral transmission, or if excreted at a floral resource, the fungus can infect any susceptible hosts that come into contact with that flower [4,5]. Due to the extent of bee foraging ranges, this process not only increases the local pathogen load but also serves to disperse Nosema to new habitats and novel hosts. In addition to the natural transmission of these pathogens, commercial products such as honey, bee pollen, and royal jelly can be contaminated and potentially disperse these pathogens [6]. The most common symptoms of Nosema infection are dysentery and microscopic lesions within the gut and Malpighian tubules. This leads to host frailty, lethargy, and loss of workers in eusocial bees that reduces foraging ability for the colony through mortality, reduced homing ability, shorter foraging flights, and inefficient foraging behavior [5,7]. Nosema bombi infections also reduce the fecundity of the colony through detrimental physical effects to the reproductive organs in male bumblebees, increased mortality of workers, and negatively impacting

Pathogens Spillover from Honey Bees to Other Arthropods

“…Pathogens and parasites are deemed drivers of this decline, together with other factors including pesticides and global warming. Nonetheless, the global picture is certainly far from complete, since data may misrepresent the actual distribution and gaps remain in our understanding of both epidemiological features and invasion dynamics of many pathogens [ 12 , 20 , 21 , 22 , 23 , 24 , 25 ]. Apis mellifera is known to share pathogens with bumblebee species, including viruses, bacteria, fungi and protozoa [ 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 ].…”

Detection of Lotmaria passim, Crithidia mellificae and Replicative Forms of Deformed Wing Virus and Kashmir Bee Virus in the Small Hive Beetle (Aethina tumida)

“…Honey bees are exposed to pests and pathogens belonging to different groups (viruses, bacteria, fungi, protists, mites, insects, etc. ), some of which are responsible for severe health impairment and colony collapse [ 14 , 15 , 16 , 17 ]. Adult SHBs invade colonies, where they feed, thrive, and reproduce.…”

Environmental conditions and beekeeping practices associated with Nosema ceranae presence in Argentina

“…Nosemosis is a widely documented disease in temperate, tropical, and subtropical climates (Martín-Hernández et al, 2018;Grupe and Quandt 2020). Different reports proposed a climatic influence on the dynamics of N. ceranae and N. apis infections (Klee et al, 2007;Fries 2010) and virulence (Gisder et al 2010).…”