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PEARLS
A growing pandemic: A review of Nosema
parasites in globally distributed domesticated
and native bees
Arthur C. Grupe, IIID*, C. Alisha Quandt ID
Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States of America
*arthur.grupe@colorado.edu
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, nema-
todes, mites, bacteria, and fungi. Additionally, abiotic threats include the destruction of nest-
ing 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 recog-
nized 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 environ-
ment. 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 patho-
gens [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 infec-
tions also reduce the fecundity of the colony through detrimental physical effects to the repro-
ductive organs in male bumblebees, increased mortality of workers, and negatively impacting
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OPEN ACCESS
Citation: Grupe AC, II, Quandt CA (2020) A
growing pandemic: A review of Nosema parasites
in globally distributed domesticated and native
bees. PLoS Pathog 16(6): e1008580. https://doi.
org/10.1371/journal.ppat.1008580
Editor: Anuradha Chowdhary, Vallabhbhai Patel
Chest Institute, INDIA
Published: June 18, 2020
Copyright: ©2020 Grupe, Quandt. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Funding: University of Colorado Boulder
Department of Ecology and Evolutionary Biology.
The funders had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
the ability of next season’s queens to found new colonies under laboratory conditions [8].
While there have been studies to observe the detrimental effects of Nosema infections in both
Bombus and Apis species, as reviewed in Brown [9] and Martin-Hernandez and colleagues
[10], almost nothing is known about the impact on native, solitary bees.
While microscopic detection of Nosema infections is possible, determining which species is
causing the infection can be difficult. N.bombi can be morphologically differentiated from N.
apis and N.ceranae, but distinguishing between these two is impossible without molecular
techniques. Typically, identifying which pathogen or pathogens may be causing an infection
requires specialized molecular primers for the small subunit of the rDNA cassette [11].
Through the use of these molecular primers, other species of Nosema have been detected in
bees: Nosema neumanni in commercial honeybee colonies in Uganda, Nosema cf.thomsoni in
Andrena vaga in Belgium, Nosema thomsoni, and Nosema portugal in commercial Bombus spe-
cies in Chile and Argentina [12,13,14], although the detrimental effects of these pathogens are
unclear and require further study.
Changing distributions
Historically, N.apis and N.ceranae were found in distinct geographic locations: Europe and
North America for N.apis, and South East Asia for N.ceranae [15]. With the increasing export
of commercial hives from Europe, N.apis followed. For many decades, N.apis was the domi-
nant strain infecting 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 few 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 been replacing N.apis throughout the range of A.mellifera [18,7].
Not only has N.ceranae replaced N.apis as the main Nosema pathogen in A.mellifera, the lack
of seasonality of N.ceranae infections has led to year-round infection cycles that are ultimately
more damaging to A.mellifera hives [7]. In addition to the changing distribution of these path-
ogens, genomic studies have revealed that isolates from geographically distinct countries have
a very high level of genetic diversity and are potentially polyploid, and local populations within
its native range have a unique set of single nucleotide polymorphisms that indicate evolution-
ary adaption within the native range [19,20].
Sampling of native bees
While much of the work documenting the prevalence and distribution of Nosema species in
bees of commercial interest has been done, some researchers have investigated the distribution
of Nosema infections in native bees (Fig 1,Table 1, and S1 Table). Given the economic impor-
tance of domesticated bees to agriculture, this imbalance is understandable. However, when
the ecosystem service of pollination is viewed in the wider lens of native plant communities,
and the consequences of diminished pollination on community fitness, the distribution and
impacts of Nosema species in native bees becomes a significant concern. Several studies have
recognized this threat and investigated the distribution of Nosema species in native bees [Fig 1,
21,22,23,24]. The decline of pollination services to native plants is of concern not only in eco-
system maintenance but also conservation and restoration efforts. Furthermore, additional
research is needed to determine both the pathology and distribution of infections in native
bees. Through studying native bees and the distribution of Nosema infections in them, we can
better understand the long-term consequences to native bees and the plant communities reli-
ant on them.
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Fig 1. Worldwide distribution of Nosema species infecting bees. Distribution of Nosema species infecting domesticated, wild, or both bees from environmental survey
studies (15,16,18, 21–24, 28–72).
https://doi.org/10.1371/journal.ppat.1008580.g001
Table 1. Host genera of bees that have a species with a documented infection of a species by Nosema.
Host genera Nosema apis Nosema bombi Nosema ceranae
Apis
D,N
X
[16,18,28,29,30,31,32,33,34,
35,36,37,38,39,40,41]
(5)
X
[43]
(>1) X
[4,13,16,18,29,30,31,32,33,35,36,37,40,41,43,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67]
(>10)
Bombus
D,N
X
[42]
(1) X
[23,24,44,45,46,47,48,49,50,51,52]
(>53)
X
[4,21,22,42,47,68,69,70,71]
(21)
Andrena
N
X
[21,53]
(4)
Anthophora
N
X
[21]
(1)
Chelostoma
N
X
[21]
(1)
Colletes
N
X
[21]
(1)
Halictus
N
X
[21]
(1)
Heriades
N
X
[21,53]
(1)
Hylaeus
N
X
[21]
(1)
Lasioglossum
N
X
[21]
(3)
Melipona
N
X
[72]
(5)
Melitta
N
X
[21]
(1)
Osmia
N
X
[21,53]
(3)
Scaptotrigona
N
X
[72]
(1)
Tetragonisca
N
X
[72]
(1)
Genera with a single or multiple species with a documented Nosema species infection. “D” is for domesticated species, and “N” is for native. The number of bee species
with a documented infection are in parenthesis, those with “>” are from studies where multiple species of the genus were found infected but not identified below the
generic level (see S1 Table for an expanded list of species and geographic distribution). Study citations are written as superscripts.
https://doi.org/10.1371/journal.ppat.1008580.t001
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Pathogen spillover
While Nosema species are spread within eusocial colonies via the fecal–oral pathway, this also
leads to the spread of the pathogen through floral resource contamination. When an infected
bee visits a floral resource and defecates, the resource is now contaminated and can lead to
what is called pathogen spillover and is defined as the transmission of diseases from domesti-
cated animals to wildlife living in close proximity [25]. Any bees that subsequently visit the
resource, native or domesticated, are now at risk for infection. This can lead to infection of the
host, which will thereby spread the pathogen to other floral resources, which puts the bee com-
munity at risk of not only infection and potential fitness consequences but can spread the path-
ogen throughout the foraging range of the infected bee with a compounding effect. As this
spread can lead to a broad landscape pathogen load, there is the potential for significantly
reduced pollinator efficacy. Additionally, pathogen spillover can lead to extinction events of
small populations that lack defenses against novel pathogens, reverse spillover back to domes-
ticated animals, and evolution of novel strains [25,26,27].
Management and future directions
Given the consequences of Nosema infections, the ability to control the pathogen load within
infected bees is of utmost necessity. Historically, the antifungal pesticide Fumagilin-B pro-
duced by Medivet Pharmaceuticals Ltd. was the most effective and widespread treatment of
Nosema infections within managed hives. However, in 2018, Medivet Pharmaceuticals Ltd.
announced that due to the cessation of production of the precursors to Fumagilin-B, the com-
pany was ceasing production of the compound. This has led to increased research on alterna-
tives for the management of the disease. While breeding for Nosema resistant lines of honey
bees has been conducted for over a decade with some success [73], chemical alternatives are
also being investigated. One such investigation [74] showed that the combination of aqueous
extracts of Artemisia dubia (Asteraceae, Plantae) and Aster scaber (Asteraceae, Plantae) worked
best at inhibiting N.ceranae spore proliferation. Continued exploration and testing of Anti-
Nosema compounds is necessary, as management of these fungi will most likely require a com-
bination of solutions. A recent review by Burnham [75] efficiently summarized the breadth of
treatments being investigated that includes small molecules, RNA interference, extracts and
supplements, and microbial supplements. In addition to continued research into treatments
for Nosema diseases, further environmental surveys must be conducted to determine the dis-
tribution of Nosema species in both managed and wild bees. Particular focus should be given
to the investigation of the pathogen’s distribution and impact on wild, native bees, although
this is logistically difficult. Through better understanding of the impact and distribution of
these pathogens on native bee communities, better management strategies for domesticated
and native bees and the ecosystems they serve will be of vital importance.
Supporting information
S1 Table. Nosema species infecting species of bees. Species of Nosema infecting different bee
species with the location and corresponding citation.
(XLSX)
Acknowledgments
The authors would like to thank two anonymous reviewers for their helpful and insightful
comments during the review process.
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