The European Zoological Journal

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Presence and distribution of pests and diseases of

Apis mellifera (Hymenoptera: Apidae) in Mexico: a
review

G. Peña-Chora, E. Toledo-Hernández, C. Sotelo-Leyva, P. Damian-Blanco, A. G.

Villanueva-Flores, P. Alvarez-Fitz, F. Palemón-Alberto & S. Á. Ortega-Acosta

To cite this article: G. Peña-Chora, E. Toledo-Hernández, C. Sotelo-Leyva, P. Damian-Blanco, A.

G. Villanueva-Flores, P. Alvarez-Fitz, F. Palemón-Alberto & S. Á. Ortega-Acosta (2023) Presence
and distribution of pests and diseases of Apis mellifera (Hymenoptera: Apidae) in Mexico: a
review, The European Zoological Journal, 90:1, 224-236, DOI: 10.1080/24750263.2023.2182920

To link to this article: https://doi.org/10.1080/24750263.2023.2182920

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The European Zoological Journal, 2023, 224–236
Vol. 90, No. 1, https://doi.org/10.1080/24750263.2023.2182920

Presence and distribution of pests and diseases of Apis mellifera

(Hymenoptera: Apidae) in Mexico: a review

G. PEÑA-CHORA1, E. TOLEDO-HERNÁNDEZ 2*, C. SOTELO-LEYVA2,

P. DAMIAN-BLANCO2, A. G. VILLANUEVA-FLORES2, P. ALVAREZ-FITZ2,
F. PALEMÓN-ALBERTO3, & S. Á. ORTEGA-ACOSTA3
1
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, México, 2Facultad de
Ciencias Químico Biológicas, Universidad Autónoma de Guerrero, Chilpancingo, México, and 3Facultad de Ciencias
Agropecuarias y Ambientales, Universidad Autónoma de Guerrero, Iguala de la Independencia, México

(Received 16 May 2022; accepted 15 February 2023)

Abstract
The European honey bee, Apis mellifera L., is the bee species with the largest geographic distribution in the world. It is considered
a pollinator generalist of wild plants and agricultural crops, as well as honey bee products as honey, beeswax, and propolis. For this
reason, it plays an extremely important role in the world’s ecosystems, economy, and food security. However, Apis mellifera is
facing population declines due to biotic and abiotic factors, such as climate change, habitat loss, agrochemical use, and emerging
pests and diseases. Pests and diseases are directly associated with a phenomenon known as colony collapse disorder (CCD), which
is linked with the loss of millions of bee colonies annually worldwide. One particularly important pest is the varroa mite, which is
already widely distributed and is considered the major threat to apiculture. In this review, we compile documentation of the
presence and distribution of pests and diseases reported to affect Apis mellifera in Mexico. Surveys demonstrate that the following
pests are present: Varroa destructor, Acarapis woodi, Aethina tumida, Galleria mellonella, as well as the diseases caused by Melissococcus
plutonius, Paenibacillus larvae, Vairimorpha (Nosema) apis, V. ceranae, Ascosphaera apis and several viruses. It should be noted that
the distribution and presence of European bee pathogens throughout the beekeeping states of Mexico is not very well defined, due
to the lack of current bee health studies in apiaries or nationwide databases to quickly update information on their distribution and
incidence.

Keywords: Varroa destructor, Aethina tumida, Acarapis woodi, Melissococcus plutonius, Vairimorpha spp, Ascosphaera
apis

1. Introduction Mexico is composed of 32 states and shares land

Between 60% and 90% of plants species on the planet
require visitation by pollinators to reproduce (Kremen
et al. 2007). Given that many agricultural crops are
dependent on pollinators, bees play a very important
role in the ecology, economy, and food production of
all countries (García-Anaya et al. 2016; Hamadache
et al. 2017). Pollination is also critical to maintain
plant biodiversity. In addition to their pollination ser­
vices, pollinators like honey bees also provide products
of economic value such as honey, pollen, beeswax, and
propolis (Hamadache et al. 2017).
borders with the United States of America to its
north and Guatemala and Belize to its south
(Central America) (Figure 1). The country’s climate
is highly diverse with tropical, subtropical and tem­
perate climatic zones (Vergara-Castaneda et al.
2012). This diversity of climates has allowed for
the development of a beekeeping industry. The
regions in Mexico with the highest honey produc­
tion are Campeche, Yucatán and Quintana Roo on
the Yucatan Peninsula, as well as the states of Jalisco
and Veracruz (Figure 1) (Baena-Díaz et al. 2022).
Beekeeping has great socio-economic importance in

*Correspondence: E. Toledo-Hernández Facultad de Ciencias Químico Biológicas, Universidad Autónoma de Guerrero. Av. Lázaro Cárdenas s/n, Apdo,
Chilpancingo 39070, México. Email: erubieltoledo@gmail.com

© 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/
licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly
cited.
 Pests and diseases of Apis mellifera in Mexico 225

Figure 1. Mexico country consists of 32 states and shares land borders with USA to its north and with Guatemala and Belize to its south
(Central America). The regions in Mexico with more production of honey are the Yucatan peninsula (Campeche, Yucatan and Quintana
Roo), as well as the states of Jalisco and Veracruz (highlighted in beige).

Mexico, as it is a major source of employment and
income from the sale of different bee-derived pro­
ducts. In this context, Mexico contributes an annual
production of 62,320 tons of honey (Zavala-Beltrán
et al. 2021), ranking sixth in terms of honey produc­
tion and third in exports worldwide, generating
a foreign exchange of $93,725 million USD
(Gallardo-López et al. 2021).
However, in recent years the European honey bee
has experienced a collapse in its populations,
a phenomenon directly related to the increase pests
and diseases, and anthropogenic activities such as
agrochemical use, habitat loss, climate change (Potts
et al. 2010; Paudel et al. 2015; Toledo-Hernández
et al. 2021;). Bee pests and diseases affect
A. mellifera populations by causing an abrupt col­
lapse in their populations. The presence of pests and
diseases in A. mellifera has been a triggering factor
for the phenomenon known as colony collapse dis­
order (CCD), which has been shown to significantly
compromise the survival of A. mellifera (Oldroyd,
2007; VanEngelsdorp et al. 2009). To date, there
are some published works regarding pests and dis­
eases affecting A. mellifera worldwide (Bradbear
1988; Allen & Ball 1996; Matheson 1996; Ellis &
Munn 2005). However, further studies on the regio­
nal distribution of pests and diseases may help to
avoid the spillover of the pathogens among states
and counties within the same country, as well as
safeguarding the borders with other countries
where the pathogens are not present.
The sanitary status and problems of A. mellifera in
Mexico are poorly known. Reports of pests and dis­
eases are general and/or focused only on certain
states within the country. The objective of this
review was therefore to compile the current knowl­
edge of the presence and distribution of pests and
diseases that affect A. mellifera in Mexico. This
information will be useful to help understand the
dynamics of spread or migration of these pathogens.
The scientific literature analyzed showed that the
most serious zoosanitary problems faced by honey
226 G. Peña-Chora et al.
bees in Mexico are the pests Varroa destructor,
Acarapis woodi, Aethina tumida, Galleria mellonella,
as well as diseases caused by Melissococcus plutonius,
Paenibacillus larvae, Vairimorpha (Nosema) apis,
V. ceranae, Ascosphaera apis, and different viruses
such as Black Queen Cell Virus, Kashmir Bee
Virus, Deformed Wing Virus among others
(Medina-Flores et al. 2014; Martínez-Cesáreo
et al. 2016; Beaurepaire et al. 2020). This informa­
tion may help the animal and health authorities to
promote management programs for these patho­
gens, as well as in the generation of strategies to
prevent their spread to other states of the republic
in order to safeguard the country’s beekeeping
activity.
2. Pests of A. mellifera reported in Mexico
2.1 Varroa destructor (Mesostigmata: Varroidae)
The mite Varroa destructor (Anderson & Trueman),
erroneously identified in Mexico as Varroa jacobsoni
until 2000, is the etiological agent of the disease
known as Varroosis and the most important threat
to honey bees worldwide (Traynor et al. 2020). The
natural host of Varroa destructor is the Asian honey
bee Apis cerana; however during the 1950ʹs it was
recorded in A. mellifera hives in northeastern Asia,
then spread rapidly to all continents through the
global honey bee trade (Ramsey et al. 2019;
Traynor et al. 2020). The life cycle of this ectopar­
asite is closely related to that of its host, and its
reproductive cycle is synchronized with the develop­
ment of bee broods (Rosenkranz et al. 2010). It
feeds on the fatty tissue of pupal and adult bees
(Ramsey et al. 2019). However, the lethality of
V. destructor is mainly due to the fact that it is
a vector of entomopathogenic viruses including
Acute Bee Paralysis Virus (ABPV), Kashmir Bee
Virus (KBV), Deformed Wing Virus (DWV), and
Israeli Acute Paralysis Virus (IAPV) (Bakonyi et al.
2002; Chen et al. 2004; Yue & Genersch 2005; Di
Prisco et al. 2011), thus contributing to the abrupt
decline of A. mellifera populations. The presence of
V. destructor was first reported in Mexico by Chihu-
Amparan et al. (1992) in A. mellifera hives in the city
of Xalapa in the State of Veracruz. In the same year,
Rodriguez-Dehaibes et al. (1992) reported it in
other apiaries in the same state. Later, it was
reported in three municipalities of the neighboring
state of Tamaulipas (Ambriz et al. 1995). The
absence of an effective management program for
V. destructor, together with the exponential growth
of the mite population and the presence of viruses in
A. mellifera, lead to the collapse of a colony in 2 or
3 years (Levin et al. 2019; Mondet et al. 2020). To
date, this mite is distributed throughout the
Mexican Republic (Table I) and is one of the most
widespread and aggressive pests in apiaries, making
it one of the main causes of damage to bee health in
Mexico.
2.2 Aethina tumida (Coleoptera: Nitidulidae)
Aethina tumida (Murray) or small hive beetle (SHB)
discovered in 1867 (Murray 1867), is a parasitic
insect native to sub-Saharan Africa; it is now dis­
tributed worldwide and has become a devastating
pest of A. mellifera hives outside its natural range
(Neumann & Elzen 2004). The beetles infest the
inside of hives, where they feed, develop and ovipo­
sit. Both adults and larvae of A. tumida feed primar­
ily on bee broods (larvae and pupae), as well as
honey, pollen, and dead bees (Hood 2004).
However, the larval stage of A. tumida causes the
most damage to the colony due to the formation of
galleries in the panels and contamination of honey
with Kodamaea ohmeri, a yeast associated with SHB.
The rapid decline of the population size within
A. mellifera colonies is due to hive destruction and
honey fermentation, which compromises the bees’
capacity to store food and generate a new brood,
thereby causing colony collapse (Ramírez &
Calderón 2018; Tucuch-Haas et al. 2020).
In Mexico, A. tumida was first recorded in 2007 in
apiaries in the northern region of the state of
Coahuila (Del Valle-Molina 2007). Since then, it
has been reported in more than 14 states, including
the main honey producers in the country, such as
Veracruz, Quintana Roo, Yucatán and Campeche
(Saldaña-Loza et al. 2014; Hernández-Torres et al.
2021). The high incidence of A. tumida recently
reported in different states (Table I) demonstrates
the need for a coordinated, nationwide effort to
combat this threat to bee health and beekeeping.
2.3 Acarapis woodi (Acari: Tarsonemidae)
Acarapis woodi (Rennie) is a tracheal endoparasite of
honey bees that has spread rapidly to all continents
since it was first identified on the Isle of Wight,
England (Rennie 1921). The mite parasitizes mainly
the prothoracic trachea of bees, which it perforates to
feed on hemolymph (Loeza-Concha et al. 2020).
However, mites can also infest the air sacs of the
bees’ abdomen and head (Sammataro et al. 2013).
The disease produces nonspecific clinical symptoma­
tology that is associated with an inability to thermo­
regulate in hives during winter, causing a decrease in
 Pests and diseases of Apis mellifera in Mexico 227

Table I. Geographical distribution of A. mellifera pests in Mexico.

Causal agent Organism Order: Family Instar affected State References

Varroa Mite
destructor
- -
- -
- -
- -
- -
- -
- -
- -
- -
- -
- -
Acarapis woodi Mite
- -
- -
- -
- -
- -
- -
- -
- -
- -
Aethina tumida Beetle Coleoptera:Nitidulidae
- -
- -
- -
- -
- -
- -
Mesostigmata: Larvae and Campeche Gutiérrez & Collí-Ucán 1996
Varroidae pupae Yucatan
Quintana Roo
- - Yucatan Medina-Medina 1997
- - Estado de Mexico de Guzman et al. 1999
- Yucatan Medina-Medina & Vicario-Mejia 1999
- - Chiapas Mondragón et al. 2005
- - Zacatecas Medina-Flores et al. 2011
- - Yucatan Martínez-Puc et al. 2011
- - Estado de Mexico Ruíz-Flores et al. 2012
- - Tabasco Contreras-Ramírez et al. 2016
- - Estado de Mexico Martínez-Cesáreo et al. 2016
Campeche Martínez-Puc et al. 2018
- - Jalisco Tapia-González et al., 2019a
- - Coahuila Vargas-Valero et al. 2021
Durango
Acari: Tarsonemidae Adults Baja California Clark et al. 1986
- - Tamaulipas Eischen 1987
Nuevo Leon
- - Tamaulipas Lozano et al. 1989
- - Coahuila Eischen et al. 1990
Chihuahua
- - Yucatan Echazarreta et al. 1997
- - Baja California Aguirre et al. 1999
Sur
- - Yucatan Martínez-Puc et al. 2011
- - Estado de Mexico Ramírez et al. 2012
- - Estado de Mexico Martínez-Cesáreo et al. 2016
- - Morelos García-Figueroa & Arechavaleta-Velasco
2018
Larvae and Yucatan Duarte-Chávez et al. 2017
pupae
- - Chihuahua Bayona-Celis et al. 2018
Jalisco
Veracruz
Campeche
Oaxaca
Aguascalientes
Queretaro
- - Coahuila Hernández-Torres et al. 2018
- - Yucatan Canto et al. 2020
- - Campeche Hernández-Torres et al. 2021
- - Tamaulipas Reyna-Fuentes et al. 2021
- - Morelos Toledo-Hernández et al. 2022

(-) same information in the column.

brood area, lower honey production, and increased
adult mortality (McMullan & Brown 2009; Szawarski
et al. 2017). In addition, there is evidence of synergistic
interactions between tracheal mite and other patho­
gens, such as V. destructor, resulting in a rapid weaken­
ing of the colonies (McMullan & Brown 2009).
Acarapis woodi was first discovered in Mexico in
1980, in apiaries near the city of Guadalajara, Jalisco
(Wilson & Nunamaker 1982). Subsequently, studies
revealed a high incidence of acarapisosis in the states of
Nuevo Leon and Tamaulipas (Guzman-Novoa &
Zozaya-Rubio 1984), even though it was believed
that areas further south and northwest of Mexico
were likely to remain free of this parasite (Wilson &
Nunamaker 1985). Later reports throughout the coun­
try suggest that acarapisosis had already spread rapidly
despite the efforts of animal health authorities to pre­
vent its spread in the beekeeping regions of the country
(Table I).
2.4 Galleria mellonella (Lepidotera: Pyralidae)
The greater wax moth, Galleria mellonella (Linnaeus)
is a pest of the two honey bee species, A. mellifera
228 G. Peña-Chora et al.
and A. cerana. It was first reported affecting honey
bee colonies of Asian honey bee Apis cerana, but
later spread to northern Africa, Great Britain, some
parts of Europe, Northern America, and New
Zealand (Paddock 1918; Akratanakul 1987). Wax
moths feed only while they are in the larval life stage;
they feed on wax combs, cast skins of bee larvae, and
honey in the weakened colonies, casing the majority
of their damage in stored combs (Ellis et al. 2013).
The presence of G. mellonella larvae is identified by
the presence of silk threads when the larvae create
tunnels in the comb and leave masses of threads on
the frame (Sohail et al. 2017). The feeding habits of
the larvae of G. mellonella reduce the combs to a pile
of wax debris. In addition, the silken threads pro­
duced by the larvae can trap developing honey bee
broods inside the cells and entangle emerging bees,
causing death by starvation; this phenomenon is
described as galleriasis (Ellis et al. 2013). In
Mexico, there are no reports that record this pest
for the first time, however, it is well known that it is
spreading in the beekeeping states of the republic.
Since 1997, it has already been reported their pre­
sence in honey bee hives of Yucatan state, Mexico
(Echazarreta et al. 1997).
3. Diseases of A. mellifera reported in Mexico
3.1 Melissococcus plutonius (Lactobacillales:
Enterococcaceae)
Before Varroa destructor jumped from A. cerana to
A. mellifera, the most important threats to European
honey bees were the bacterial diseases European
foulbrood (EFB) and American foulbrood (AFB)
(Genersch 2008). European foulbrood (EFB), an
important disease of honey bee brood, is caused by
the bacterium Melissococcus plutonius, a Gram-
positive, lanceolate, microaerophilic coccus (Bailey
& Collins 1982). The infectious cycle begins when
M. plutonius is introduced into the digestive tract of
larvae through contaminated food provided by adult
bees. The pathogen reaches the midgut of the larvae,
where it multiplies vigorously until it colonizes com­
pletely (Nakamura et al. 2020). Diseased larvae
change from white to yellowish, then brown,
become flaccid, give off a foul or sour odor, and
die 4–5 days after infection and before reaching the
pupal stage (Budge et al. 2010; Grossar et al. 2020).
Melissococcus plutonius is considered to kill its host
before it can successfully invade body tissues
(Nakamura et al. 2020). Massive brood loss due to
infection weakens the colony and in severe cases,
can lead to its collapse (Djukic et al. 2018).
Because there is no effective treatment and given
the severity of outbreaks, it is considered
a notifiable disease in Mexico and many countries
worldwide (Diario Oficial de la Federación (DOF)
2018; Grossar et al. 2020). In Mexico, there are few
reports about the distribution of this pathogen.
Wilson et al. (1984) reported the presence of this
bacterium in the country for the first time in 1984,
but it was not reported again until 2018, in honey
bee colonies in the state of Chihuahua (de
León-Door et al. 2018). Although to date there are
no other reports in the scientific literature, anecdotal
evidence suggests that bacterial infection by
M. plutonius is common in Mexican hives, leading
some beekeepers resort to the application of antibio­
tics of the tetracycline group (personal communica­
tion) despite their use being banned by animal
health agencies due to the contamination of pro­
ducts such as honey, pollen, wax, and propolis,
making it even more difficult to control this
pathogen.
3.2 Paenibacillus larvae (Bacillales:
Paenibacillaceae)
One of the most damaging pathogens of honey bee
broods is the gram-positive, facultative anaerobic,
spore-forming bacterium Paenibacillus larvae, which
causes the disease known as American foulbrood
(AFB) (Genersch et al., 2006). Endospores are the
only infectious form of this organism, which are
acquired by larvae through ingestion of contami­
nated food. The vegetative bacteria colonize the
midgut of the larvae where they proliferate mas­
sively, then penetrate the epithelium and invade
the hemocoel, causing death by septicemia (Yue
et al. 2008; Genersch 2010). Detection of AFB in
the field is based on the clinical symptoms of dis­
eased brood, including the decomposition of the
larval body into a brownish and viscous mass (the
basis for the “ropiness” test), which later dry into
hard scales that bees cannot removed from brood
cells (Sarwar 2016). These scales are then a constant
focus of reinfection, since they contain millions of
environmentally stable spores (Ueno et al. 2018).
Although AFB occurs worldwide and cases have
been reported on all continents (Antúnez et al.
2004; Ueno et al. 2018), in Mexico there is poor
documentation of the distribution of P. larvae within
the country, including the states with important
beekeeping industries. However, the presence of
this bacterium in the country has been reported
since 1994 (Djordjevic et al. 1994), and more
recently it was isolated from European honey bee
larvae in the Xochimilco municipality of Mexico
City (Peréz de la Rosa et al. 2015). In addition,
 Pests and diseases of Apis mellifera in Mexico 229

some cases of AFB have been detected and isolated 3.4 Vairimorpha (Nosema) ceranae
by the Mexican Ministry of Agriculture, but no (Dissociodihaplophasida: Nosematidae)
further data were provided on the incidence or dis­
Vairimorpha (Nosema) ceranae is another microspori­
tribution of P. larvae in the country (Peréz de la
dian intestinal parasite of Apis mellifera, considered the
Rosa et al. 2015). The detection of this pathogen
etiological agent of Nosemosis type C (Martín-
plays an important role in the efficient control of its
Hernández et al. 2018). This fungus was originally
dissemination, so it is necessary to update this infor­
described as a pathogen of the Asian honey bee Apis
mation. Mexico is one of the countries where AFB is
cerana, but research over the past few decades has
considered a notifiable disease, and the destruction
shown that N. ceranae has replaced N. apis as the
of diseased hives by fire is the only viable control
main cause of Nosemosis in honey bees, and that it
measure. This causes considerable economic losses
exhibits higher virulence than N. apis (Fleites-Ayil
to beekeepers, which is one of the reasons for the
et al., 2018). Compared to infection caused by
lack of reporting in the country.
N. apis, which presents apparent symptoms and sea­
sonality, N. ceranae infection in honey bees results in
3.3 Vairimorpha (Nosema) apis high mortality, causing population decline and colony
(Dissociodihaplophasida: Nosematidae) collapse during all seasons of the year (Grupe &
Quandt 2020; Higes et al. 2020). Vairimorpha ceranae
Vairimorpha (Nosema) apis was the first microspori­
affects the immune response, produces nutritional
dian parasite described in A. mellifera. It was thought
stress, increases sugar consumption, and induces
to be the only etiological agent of nosemosis, however,
early foraging (Pașca et al. 2019). Nosemosis
in 2007 the species V. ceranae was also identified
(Vairimorpha spp) has been known to affect
affecting the European honey bee (Paxton et al.
A. mellifera in Mexico since the 1960s; however, sam­
2007). Vairimorpha spp. carries out its life cycle inside
ples of Africanized honey bees (A. mellifera scutellata)
the epithelial cells of the bee midgut. Infection in bees
collected on the Yucatan Peninsula in 1980 and later
occurs by fecal-oral transmission, through ingestion of
analyzed by Guzman-Novoa et al. (2011) demon­
spores during fecal cleansing activities in the comb and
strated the presence of N. ceranae for the first time in
the consumption of contaminated food and water
Mexico. In a similar case, Africanized bees collected
(Martín-Hernández et al. 2011). During the foraging
between 1995 and 1996 in the State of Mexico and
activity of infected bees, they contaminate floral
later analyzed by Guerrero-Molina et al. (2016) were
resources with their droppings, as well as the collected
found to have this pathogen. Vairimorpha ceranae was
pollen and the hive, thus contributing to the infection
then confirmed in other hives from Mexico State as
cycle (Grupe & Quandt 2020). Infection with N. apis
well as other states in central Mexico, including
is considered a low virulence disease whose typical
Morelos, Hidalgo, and Mexico City (Guzman-Novoa
characteristics are dysentery, lethargy, reduced long­
et al. 2011). To date, there is little information on the
evity of workers, inefficient foraging, lower honey
overall geographic distribution of this pathogen in the
yields, and increased mortality during winter (Grupe
beekeeping states of Mexico (Table II), but like
& Quandt 2020; Higes et al. 2020). However, there is
N. apis, the presence of N. ceranae may be common
evidence that concurrent exposure to pesticides such
in apiaries throughout the country. Nosemosis, caused
as neonicotinoids during Vairimorpha (Nosema) infec­
by V. apis and V. ceranae, is recognized as one of the
tion exacerbates the disease and accelerates bee death
most widespread diseases worldwide in European
(Alaux et al. 2010). Zozaya reported the presence of
honey bees. These pathogens contribute to the reduc­
this disease in Mexico for the first time affecting
tion of populations, putting the survival of A. mellifera
A. mellifera hives in the state of Mexico in 1965
at risk (Cueto-González et al. 2020).
(Tapia-González et al. 2017). Later, in 1980, Wilson
& Nunamaker reported the presence of this etiological
agent in the states of Sonora, Oaxaca, and Tamaulipas
3.5 Ascosphaera apis (Onygenales:
(Wilson & Nunamaker 1983). To date, there are few
Ascosphaeraceae)
studies on the presence of this pathogen in apiaries in
Mexico (Table II), so little is known about its current Ascospherosis or chalkbrood disease is a mycosis
distribution in the states of the country. It is important caused by the fungus Ascosphaera apis, which affects
to learn more about the spread of this disease in order the brood of all castes of A. mellifera. The two main
to help beekeepers in regions with severe problems by routes of infection are by germination of fungal
information campaigns and recommendations of spores on the cuticle of the larva and by ingestion
hygienic hive management practices. of food contaminated with spores of the fungus.
230 G. Peña-Chora et al.

Table II. Geographical distribution of A. mellifera diseases in Mexico.

Instar
Causal agent Organism Order: Family affected State References

Vairimorpha (Nosema) apis Fungi Dissociodihaplophasida: Adults Yucatan García-Millán & Quezada-
Nosematidae Euán 1993
- - - - Yucatan Echazarreta et al. 1997
- - - - Yucatan Martínez-Puc et al. 2011
- - - - Zacatecas Medina-Flores et al. 2014
- - - - Estado de Martínez-Cesáreo et al. 2016
Mexico
- - - - Baja Cueto-González et al. 2020
California
Vairimorpha (Nosema) spp. - - - Jalisco Tapia-González et al. 2017
- - - - Campeche Martínez-Puc et al. 2018
Vairimorpha (Nosema) ceranae Fungi Dissociodihaplophasida: Adults Estado de Guzman-Novoa et al. 2011
Nosematidae Mexico
Jalisco Tapia-González et al. 2017
- - - - Yucatan Fleites-Ayil et al. 2018
Baja Cueto-González et al. 2020
California
Ascosphaera apis Fungi Onygenales: Ascosphaeraceae Larvae Jalisco Álvarez-Ramírez et al. 2017
- - - - Campeche Martínez-Puc et al. 2018
- - - - Jalisco Tapia-González et al. 2020
Black Queen Cell Virus Virus Picornavirales: Pupae Estado de Guzman-Novoa et al. 2013
(BQCV) Dicistroviridae Mexico
- - - - Chihuahua García-Anaya et al. 2016
- - - - Jalisco Tapia-González et al., 2019b
Zacatecas
Puebla
- - - - Jalisco Morfin et al. 2020
Kashmir Bee Virus (KBV) - Picornavirales: Adults and Chihuahua García-Anaya et al. 2016
Dicistroviridae brood
Deformed Wing Virus (DWV) - Picornavirales: Iflaviridae Adults and Estado de Anguiano-Baez et al. 2016
brood Mexico
Nayarit
- - - - Chihuahua García-Anaya et al. 2016
- - - - Jalisco Tapia-González et al., 2019b
Zacatecas
Puebla
- - - - Jalisco Morfin et al. 2020
Sacbrood Virus (SBV) - Picornavirales: Iflaviridae Larvae Chihuahua García-Anaya et al. 2016
Israeli Acute Paralysis Virus - Picornavirales: Larvae and Chihuahua García-Anaya et al. 2018
(IAPV) Dicistroviridae adults
A. mellifera Filamentous Virus - Megavirales: Baculoviridae Larvae and Chihuahua García-Anaya et al. 2018
(AmFV) adults

(-) same information in the column.

Both forms of infection produce mycelia that pass
through the intestinal wall of the larvae and spread
throughout the body, causing their death and gen­
erating a mummified appearance (Reynaldi et al.
2015). Ascosphaera apis is characterized as an
opportunistic pathogen; it has been shown that its
development requires susceptible brood, which is
stressed by the presence of other pathogens, such
that A. apis generally established in colonies
affected by other diseases, thus aggravating larval
mortality (Castagnino et al. 2020). In Mexico,
A. apis was reported before the introduction of
V. destructor, so it was considered the most wide­
spread brood disease among honey bees in different
beekeeping regions, with the exception of the state
of Yucatan (Wilson et al. 1984). Later, Medina-
Medina and Vicario-Mejia (1999) reported the pre­
sence of A. apis in hives in the state of Yucatan. It is
important to note that there are currently few
reports and studies related to the incidence and
distribution of this fungus in the beekeeping states
of Mexico (Table II).
 Pests and diseases of Apis mellifera in Mexico 231

3.6 Bee viruses identify the health problems of honey bees in Mexico,
researchers and health agencies have been conducting
Honey bees are also infected by different viruses that
studies on A. mellifera populations in the beekeeping
often persist as covert asymptomatic infections, then
states for the last decades. These studies have shown
act synergistically with other biotic and abiotic stres­
the presence of aggressive pests and diseases such as
sors, causing the collapse of host colonies (DeGrandi-
parasites, bacteria, fungi and viruses, which is why
Hoffman & Chen 2015). Currently, about 18 viruses
beekeeping is at risk. The information presented in
have been identified in honey bees; the most frequent
this work shows evidence of spillover of the pathogens
are single-stranded RNA viruses, such as Sacbrood
of A. mellifera among states with apiculture activity in
Virus (SBV), Deformed Wing Virus (DWV), Israeli
Mexico. Pests and diseases can furthermore spread
Acute Paralysis Virus (IAPV), Acute Bee Paralysis
across international borders to the USA and Central
Virus (ABPV), Kashmir Bee Virus (KBV), and Black
American countries where these pathogens are not
Queen Cell Virus (BQCV) (De Miranda et al. 2013;
present, which is a real threat for their beekeeping
Wang et al. 2016). All viruses are asymptomatic at low
activities. Alger et al. (2018) claimed that other threats
levels of infection, and most significantly decrease bee
to beekeeping include the migration of swarms of
longevity by affecting various morphological, physio­
Africanized honey bees between countries, facilitating
logical, and behavioral traits (Beaurepaire et al. 2020).
the introduction and spillover of pests and diseases to
Some viruses produce symptoms that are clearly iden­
healthy colonies of A. mellifera. So too, the legal or
tifiable by beekeepers at high viral titers, allowing
illegal introduction of new races of A. mellifera, as well
a simple and direct diagnosis. However, many other
as contaminated products such as honey, wax, and
viruses do not generate apparent symptoms and their
pollen have contributed to the arrival of pathogens to
association with A. mellifera colony mortality remains
other regions (Mutinelli 2011).
unexplained (De Miranda et al. 2013; Wang et al.
There is currently limited and heterogeneous
2016). According to epidemiological data, the distri­
information and little communication among Latin
bution of viruses in A. mellifera appears to be world­
American and Caribbean countries with respect to
wide (Beaurepaire et al. 2020). In Mexico, the first
pests and diseases affecting beekeeping, and more
viral disease in honey bees was reported by Bailey
regional surveys are needed to improve this situation
(1967), caused by Chronic Bee Paralysis Virus
(Olate-Olave et al. 2021). For instance, Vandame
(CBPV). However, the author does not provide
and Palacio (2010) claimed that in Latin America
a specific description of the geographic distribution
there are no records of massive losses of honey bee
of this virus in Mexico. It was not until 2012 that
colonies, but just a few years later, honey bee colony
Guzman-Novoa et al. (2012), reported the presence
collapse and mortality were reported (Maggi et al.
of SBV, DWV, IAPV, and ABPV in colonies of
2016; Requier et al. 2018). It is necessary to carry
A. mellifera in the State of Mexico. Subsequently, the
out studies to determine the current health status of
presence of BQCV and A. mellifera Filamentous Virus
the honey bees as well as the distribution of pests
(AmFV) was also reported in other beekeeping regions
and diseases of A. mellifera throughout the Americas.
of the country (Table II).
This information could help in pathogen identifica­
tion and surveillance to understand their dynamics
of migration in the region. This would help to estab­
4. Conclusions and perspectives
lish pathogen management policies and generate
The honey bee (Apis mellifera L.) is an extremely pertinent bee health programs to safeguard beekeep­
important species for ecosystems; its role as ing in Mexico and other Latin America countries
a pollinator contributes to the conservation of plant such as Argentina, Brazil, Chile, Uruguay, and
biodiversity and increases the productivity of agricul­ Venezuela, among others, where beekeeping has
tural crops (Larsen et al. 2019). In addition, it is high economic and ecological relevance (Maggi
important for international trade due to its products. et al. 2016; Gallardo-López et al. 2021).
Honey bees live in an environment in which they can
be exposed to different biotic and abiotic stress factors, Disclosure statement
which affect all castes and are related to the phenom­ No potential conflict of interest was reported by the
enon known as colony collapse disorder (CCD). Pests author(s).
and diseases are part of the complex of factors that
A. mellifera faces and that put its survival at risk. They
can cause important population declines, leading ORCID
directly to the socio-economic issues of the beekeeping E. Toledo-Hernández http://orcid.org/0000-0003-
sector in Mexico and around the world. In order to 4211-5298
232 G. Peña-Chora et al.
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