Nosema infection in bees

Domesticated and native bees face a variety of lethal threats that cause mortality and reduced fecundity and, by extension, endanger agriculture and native plant communities that depend on bees for pollination. Biotic factors that negatively affect bees include viruses, nematodes, mites, bacteria and fungi. In addition, abiotic threats include the destruction of nesting resources and flora from anthropogenic sources, as well as a plethora of negative factors linked to climate change.

Nosema species belong to the Microsporidia, which are all unicellular, obligate symbionts of vertebrate or invertebrate organisms. Although long regarded as protists, microsporidia are now recognized as a highly reduced fungal lineage [1]. Tokarev and colleagues [2] have recently placed the Nosema species infecting bees (Anthophila, Hymenoptera) in a new genus, Vairimorpha, but for the sake of consistency with the existing literature, this review article will simply refer to them as Nosema. More specifically, Nosema completes its life cycle by infecting the cells of the bees’ midgut. Once a spore is ingested by a bee and reaches the midgut, it germinates. It then injects its contents into the host cell, where it consumes the cellular contents via phagocytosis until it ultimately multiplies before rupturing the host cell to release a large number of spores [3]. These spores can then infect other cells of the digestive tract or be expelled from the host in the faeces, thereby contaminating floral resources, collected pollen and the environment of the entire colony. Other bees may then ingest spores in the hive via faecal–oral transmission, or if they are excreted on a floral resource, the fungus can infect any susceptible hosts that come into contact with that flower [4,5]. Because of 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 new 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 in the intestine and Malpighian tubules. This leads to host frailty, lethargy and worker loss in eusocial bees, which reduces colony foraging capacity due to mortality, reduced homing ability, shorter foraging flights and inefficient foraging behaviour [5,7]. Nosema bombi infections also reduce colony fecundity through detrimental physical effects on male reproductive organs, increased worker mortality, and a negative impact on the ability of queens in the following season to found new colonies under laboratory conditions [8]. Although studies have observed the detrimental effects of Nosema infections in Bombus and Apis species, as reviewed in Brown [9] and Martin-Hernandez and colleagues [10], almost nothing is known about the impact on native and solitary bees.

Although microscopic detection of Nosema infections is possible, it can be difficult to determine which species is responsible for the infection. N. bombi can be morphologically differentiated from N. apis and N. ceranae, but distinguishing the latter two is impossible without molecular techniques. In general, identifying the pathogen(s) that may be causing an infection requires specialised molecular primers for the small subunit of the rDNA cassette [11]. Using these molecular primers, other Nosema species have been detected in bees: Nosema neumanni in commercial honey bee colonies in Uganda, Nosema cf. thomsoni in Andrena vaga in Belgium, Nosema thomsoni and Nosema portugal in commercial Bombus species in Chile and Argentina [12,13,14], although the detrimental effects of these pathogens are unclear and require further study.

Shifts in distributions

Historically, N. apis and N. ceranae were found in distinct geographic locations: Europe and North America for N. apis, and Southeast Asia for N. ceranae [15]. With the increasing export of commercial hives from Europe, N. apis has spread. For many decades, N. apis was the dominant strain infecting honey bee colonies. While it causes dysentery in A. mellifera, the seasonality of the infection cycle was such that it would not cause total devastation of the hive. Research over the past decades, since N. ceranae was first described, has shown a dramatic increase in its contribution to the total number of Nosema infections in A. mellifera [16,17]. Studies have shown that N. ceranae has replaced N. apis across the range of A. mellifera [18,7]. N. ceranae has replaced N. apis as the primary Nosema pathogen of A. mellifera because it lacks seasonality. Ceranae infections have led to year-round infection cycles that are ultimately more damaging to A. mellifera [7]. In addition to shifts in the distribution of these pathogens, genomic studies have revealed that isolates from geographically distinct countries have a very high level of genetic diversity and are potentially polyploid, and that local populations in its native range have a unique set of single nucleotide polymorphisms indicating evolutionary adaptation within the indigenous range [19,20].

Sampling native bees

Although much of the work documenting the prevalence and distribution of Nosema species in bees of commercial interest has been carried out, some researchers have investigated the distribution of Nosema infections in native bees (Fig 1, Table 1 and Table S1). Given the economic importance of domesticated bees to agriculture, this imbalance is understandable. However, when the ecosystem service of pollination is viewed through the broader lens of native plant communities and the consequences of reduced pollination for community fitness, the distribution and impacts of Nosema species in native bees become an important concern. Several studies have recognised this threat and examined the distribution of Nosema species in native bees [Fig 1, 21,22,23,24]. The decline in pollination services for native plants is concerning not only for ecosystem maintenance but also for conservation and restoration efforts. Moreover, additional research is needed to determine both the pathology and the distribution of infections in native bees. By studying native bees and the distribution of Nosema infections in them, we can better understand the long-term consequences for native bees and the plant communities that depend on them.

 

Fig 1. Global distribution of Nosema species infecting bees.

 

Table 1. Bee host genera for which infection by a Nosema species is documented.

Genera containing one or more species with a documented infection by a Nosema species. “D” corresponds to domesticated species and “N” to native species. The number of bee species with a documented infection is given in parentheses; those with “>” come from studies in which multiple species of the genus were found infected but not identified below the genus level (see Table S1 for an expanded list). Study citations are given in superscript.

Pathogen spillover

While Nosema species spread within eusocial colonies via the faecal–oral route, this also leads to pathogen spread through contamination of floral resources. When an infected bee visits a floral resource and defecates, the resource is now contaminated and can lead to what is termed pathogen spillover, defined as the transmission of diseases from domesticated animals to nearby wildlife [25]. All bees that subsequently visit the resource, native or domesticated, are now at risk of infection. This can result in host infection, which will then transmit the pathogen to other floral resources, exposing the bee community not only to infection risk and potential fitness consequences, but also potentially spreading the pathogen across the full foraging range of the infected bee with a cumulative effect. As this spread can lead to a pathogen load in the landscape, it is possible to substantially reduce pollinator efficiency. Moreover, pathogen spillover can lead to extinction events in small populations lacking defences against new pathogens, reverse spillback onto domesticated animals, and drive the evolution of new strains [25,26,27].

Management and future directions

Given the consequences of Nosema infections, the ability to control pathogen load in infected bees is of the highest necessity. Historically, the antifungal pesticide Fumagilin-B produced by Medivet Pharmaceuticals Ltd. was the most effective and widely used treatment for Nosema infections in managed hives. However, in 2018, Medivet Pharmaceuticals Ltd. announced that because production of fumagiline-B precursors had ceased, the company would discontinue production of the compound. This led to increased research into alternatives for disease management. While selective breeding for Nosema-resistant honey bee lineages has been pursued for more than a decade with some success [73], chemical alternatives are also under study. One such study [74] showed that a combination of aqueous extracts of Artemisia dubia (Asteraceae, Plantae) and Aster scaber (Asteraceae, Plantae) worked best to inhibit the proliferation of ceranae spores. Continued exploration and testing of anti-Nosema compounds is necessary, as managing these fungi will most likely require a combination of solutions. A recent review by Burnham [75] effectively summarised the range of treatments studied, including small molecules, interfering RNAs (iRNA), extracts and supplements, and microbial supplements. In addition to continued research on treatments for Nosema diseases, further environmental studies must be conducted to determine the distribution of Nosema species in managed and wild bees. Particular attention should be paid to studying the distribution of the pathogen and its impact on native wild bees, although this is logistically challenging. With a better understanding of the impact and distribution of these pathogens in native bee communities, improved management strategies for domesticated and native bees and the ecosystems they service will be of vital importance.

 

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See also:

• Stress factors in bees and honey bee immunity
• A very social immunity
• On the contagion of foulbrood
• Safeguarding pollinators
• Bee health guide

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