Exp Appl Acarol (2012) 56:309–318

DOI 10.1007/s10493-012-9526-0

Genetic structure of Varroa destructor populations

infesting Apis mellifera colonies in Argentina

M. Maggi • S. Medici • S. Quintana • S. Ruffinengo • J. Marcángeli •

P. Gimenez Martinez • S. Fuselli • M. Eguaras

Received: 5 September 2011 / Accepted: 2 February 2012 / Published online: 16 February 2012
Ó Springer Science+Business Media B.V. 2012

Abstract Although mitochondrial DNA mapping of Varroa destructor revealed the

presence of several haplotypes, only two of them (Korean and Japanese haplotypes) were
capable to infest Apis mellifera populations. Even though the Korean haplotype is the only
one that has been reported in Argentina, these conclusions were based on mites sampled in
apiaries from a specific geographical place (Buenos Aires province). To study mites from
several sites of Argentina could reveal the presence of the Japanese genotype, especially
considering sites near to Brazil, where Japanese haplotype was already detected. The aim
of this work was to study the genetic structure of V. destructor populations from apiaries
located in various provinces of Argentina, in order to determine the presence of different
haplotypes. The study was carried out between January 2006 and December 2009. Phoretic
adult Varroa mites were collected from honey bee workers sampled from colonies of A.
mellifera located in Entre Rı́os, Buenos Aires, Corrientes, Rı́o Negro, Santa Cruz and
Neuquén provinces. Twenty female mites from each sampling site were used to carry out
the genetic analysis. For DNA extraction a nondestructive method was used. DNA
sequences were compared to Korean haplotype (AF106899) and Japanese haplotype
(AF106897). All DNA sequences obtained from mite populations sampled in Argentina,

M. Maggi (&)
S. Medici
J. Marcángeli
P. Gimenez Martinez
S. Fuselli
M. Eguaras

Laboratorio de Artrópodos, Facultad de Ciencias Exactas y Naturales,
Universidad Nacional de Mar del Plata, Funes 3350, 7600 Mar del Plata, Argentina
e-mail: biomaggi@gmail.com

M. Maggi
S. Medici
M. Eguaras

CONICET, Consejo Nacional de Investigaciones Cientı́ficas y Técnicas,
Rivadavia 1917, C1033AJ Buenos Aires, Argentina

S. Quintana
Fares Taie Instituto de Análisis, Rivadavia 3331, 7600 Mar del Plata, Argentina

S. Ruffinengo
Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Balcarce, Argentina

S. Fuselli
Comisión de Investigaciones Cientı́ficas (CIC), Calle 526 entre 10 y 11, 1900 La Plata,
Buenos Aires, Argentina

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share 98% of similitude with Korean Haplotype (AF106899). Taking into account these
results, we are able to conclude that Korean haplotype is cosmopolite in Argentina.

Keywords Varroa destructor
DNA
Haplotypes
Argentina

Introduction

Several studies about Varroa mite populations demonstrated that the genus comprises at
least four species: Varroa underwoodi, V. rindereri, V. jacobsoni and V. destructor. These
species are morphologically distinct and show clear differences between their DNA
sequences (Anderson and Trueman 2000). In the study of Anderson and Trueman (2000),
18 different mite haplotypes (mites with distinct mitochondrial DNA sequences) were
discovered infesting Apis cerana and/or Apis mellifera, nine of which were members of
V. jacobsoni, six of V. destructor, and the identities of three others were unresolved. Later
on, one more haplotype of V. destructor has subsequently been found infesting A. cerana in
China (Zhou et al. 2004). Nevertheless, although mitochondrial DNA sequencing of
V. destructor revealed several mite haplotypes, only two of them (Korean and Japanese
haplotypes) were capable to infest A. mellifera populations (Anderson and Trueman 2000).
Korean and Japanese haplotype names were chosen regarding to the places where they
were first described as parasites of their original host A. cerana. The Japanese haplotype
first shifted from A. cerana to A. mellifera in Japan last century following the introduction
of A. mellifera (Sakai and Okada 1973) and then, spread on A. mellifera into Brazil
(Anderson and Trueman 2000) and into North America (De Guzman et al. 1999). The
Korean haplotype is cosmopolite. According to De Guzman et al. (1997) and Oldroyd
(1999) reports, the Korean haplotype first switched from A. cerana to A. mellifera near
Vladivostok (north of the Korean Peninsula) following the introduction of A. mellifera
from Ukraine during the late 1950s (Crane 1978). It thereafter spread on A. mellifera into
Europe in the 1960s (Crane 1978), and then around the world, arriving in North America in
1987 (De Guzman et al. 1997; Oldroyd 1999; Sammataro et al. 2000). Latest studies
detected the presence of the Korean haplotype in Argentina (Anderson and Trueman 2000;
Guerra et al. 2010), México, Cuba, Venezuela, Cuba, Chile, Uruguay and Colombia
(Guerra et al. 2010). Varroa destructor and specially the Korean haplotype, represents the
major honey bee pest infesting and destroying millions of commercial beehives around the
world (Beetsma 1994; Sammataro et al. 2000).
In Argentina, V. destructor was first detected in Formosa province in 1976, at the
Argentine-Paraguay frontier. Varroa mite was first introduced in Paraguay when bee-
keepers of this country bought bee queens of A. mellifera from Japan (De Jong et al. 1982)
and thereafter it is believed that Varroa invaded Argentinean territory (Montiel and Piola
1976). Since then, this mite has spread all over Argentina producing a negative impact in
the beekeeping industry (Eguaras and Ruffinengo 2006). At the beginning, this parasite did
not produce big losses in honey bee production but currently, if beekeepers do not use
chemical acaricides, mite populations have devastating effects on beehives (Eguaras and
Ruffinengo 2006). This fact forced beekeepers to use synthetic drugs conscienceless (like
coumaphos and amitraz) producing secondary problems such as mite resistance and
chemical residues in honey and other hive products (Maggi et al. 2009a, 2010, 2011a;
Medici 2010).
Even though the Korean haplotype is the only one that has been reported at present in
Argentina (Anderson and Trueman 2000; Guerra et al. 2010), these conclusions were based

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on mites sampled in apiaries from a specific site of Argentina (Buenos Aires province).
In this way, virulence variations of V. destructor observed in Argentina could be attributed
to the presence of both haplotypes (Korean and Japanese haplotype). Recently studies
demonstrated that there was a change in frequency from Japanese to Korean haplotypes in
Brazil and currently, Japanese haplotype only is found in particular sites of the Brazilian
territory (Strapazzon et al. 2009; Guerra et al. 2010). Also, Maggi et al. (2009b) found
three morphotypes of V. destructor infesting colonies of A. mellifera in Argentina and they
hypothesized the presence of more than one haplotype. Equally, there are some others
factors that are related to a low impact on bees, such as the mite tolerance of African bees
and their hybrids (Medina and Martin 1999) and/or climatic conditions (Moretto et al.
1991), seem to be important factors in the population dynamics of the mite V. destructor.
Due to all these reasons, the study of mites from other regions of Argentina could reveal
the presence of the Japanese genotype, especially considering sites near to Brazil, where
Japanese haplotype was already detected (De Jong and Goncalves 1981; De Guzman et al.
1997). The importation of European queens from USA, Europe and elsewhere by
Argentinean beekeepers and the proximal geographical contact with Brazil (natural swarm
dispersion) represents two possible ways for this genotype to arrive into Argentinean
territory. As a consequence, more effort research is needed to assess the genetic distri-
bution of Varroa in Argentina. The hypothesis that more than one haplotype of V. de-
structor could be present in Argentina is also supported for other reasons: (a) Eguaras and
Ruffinengo (2006) reported that parasite virulence changed (become more virulent) since
its first detection in Formosa province, (b) the fact that Varroa mites enter to Argentina
from Paraguay through bees imported from Japan (De Jong and Goncalves 1981; De Jong
et al. 1982; De Guzman et al. 1997) (where Japanese haplotype was early reported,
Anderson and Trueman (2000) and De Guzman et al. 1997), (c) that in the bordering
country of Brazil Japanese and Korean haplotypes have been early detected (De Guzman
et al. 1997) and currently only Korean haplotype is present (Guerra et al. 2010 and
Strapazzon et al. 2009) suggesting a possible haplotype shift towards new niches as might
be the Argentine territory and d) the presence of morphotypes V. destructor in Argentina
(Maggi et al. 2009b). In this way, studies of the genetic profile of Varroa populations
infecting A. mellifera in Argentina can provide further insights into this host-parasite
relationship. Here, we continued with studies reported by Maggi et al. (2009a, b) and
present the first description of the genetic structure of V. destructor populations from
apiaries located in different provinces of Argentina, in order to determine the presence of
different haplotypes.

Materials and methods

The study was carried out between January 2006 and December 2009. Phoretic Varroa
mites were collected from honey bee workers belonging to apiaries located in different
geographical areas of Argentina (Entre Rı́os, Buenos Aires, Corrientes, Rı́o Negro, Santa
Cruz and Neuquén provinces) (Fig. 1). For each apiary, at least five colonies of A.
mellifera were sampled following the protocol established by De Jong (2005). At least 100
mites were collected in each apiary and they were finally pooled for DNA analysis. In this
study we sampled six of the twelve mite populations that were analyzed. The degree of
virulence of Varroa sampled were established by beekeepers comments, who confirmed to
us a variation in the virulence degree among the populations studied: mites from south-
ern Argentina (Morphotype 1: mites from Rı́o Negro and Santa Cruz provinces) were

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Fig. 1 Geographical sites of

Argentina where Varroa mites
were collected: 1 = Entre Rı́os
province, 2 = Buenos Aires
province, 3 = Corrientes
province, 4 = Rı́o Negro
province, 5 = Santa Cruz 1
province (Site a), 6 = Santa Cruz
2 province (Site b) and
7 = Neuquén province

more virulent than those from central and northern (Morphotype 2: mites from Entre Rı́os,
Buenos Aires, Corrientes and Neuquén provinces).

DNA extraction and analysis

Twenty female mites from each sampling site (a pool of mites for each apiary) were used
to carry out the genetic analysis. For DNA extraction nondestructive method was used
(Cruikshank et al. 2001) via Quiagen DNeasy Tissue Kit. Extracted DNA was stored at
-20°C. Samples of crude DNA were used to amplify CO-I gene using COXF and COXRa
primers developed by Anderson and Fuchs (1998). PCR cycling conditions were the fol-
lowing: an initial denaturation for 5 min at 94°C followed by 35 cycles of denaturation at
948c for 1 min, annealing at 42°C for 1 min and 20 s of elongation at 64°C for 2 min, was
applied. An extra elongation step at 64°C for 10 min also was performed. PCR reaction
products were electrophoresed on 2% agarose gels using molecular weight marker to

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identify bands (size ladder 100 bp, InvitrogenÒ). Amplified fragments by COXF y COXRa
primers were purified and sequenced.
To confirm the identity of DNA sequences, GeneBank, EMBL and DDBJ data bases,
using FASTA program were used. DNA sequences from different mite populations were
compared using ClustalW (http://www.ebi.ac.uk/clustalw/), in order to identify which V.
destructor haplotype was present in samples collected in this study. DNA sequences were
compared to those published by Anderson and Trueman (2000) in Genbank for Korean
(AF106899) and Japanese haplotypes (AF106897). A sample of amplified material was
sent to Laboratorio de Secuenciación Pro-Papa EEA INTA Balcarce to confirm obtained
results and to detect nucleotide sequences variations. PCR products were sequenced in both
directions.

Results

Two of the three V. destructor morphotypes reported by Maggi et al. (2009b) were ana-
lyzed in this study. Table 1 detail the morphometric measures of each mite population used
in this research (data extracted from Maggi et al. 2009b). With regard to DNA analysis,
COXF and COXRa primers amplified a 458 base pair (±10 base pair) fragment from the
extracted DNA obtained for each mite population studied. This fragment was ±10 bases
pair different from the previous one published by Anderson and Fuchs (1998) for V.
jacobsoni, using the same primers. Besides these sequence length variations, the amplified
DNA sequences had enough informative sites to confirm mite species and haplotypes of the
Varroa mite populations analyzed in this study.
All DNA sequences obtained from different mite populations in Argentina were 98%
concordant with the sequences reported for Korean haplotype (Gene Bank NCBI).
Sequences corresponding to COI fragment collected from mites in Buenos Aires, Cor-
rientes, Rı́o Negro, Entre Rı́os, Santa Cruz and Neuquén, share 98% of similitude with
Korean Haplotype (AF106899) reported by Anderson and Trueman (2000). If mite popu-
lations studied here are compared genetically, we can affirm the following statements:
(a) mites from the Buenos Aires province showed the highest sequence variation in their
COI fragment; (b) mites from Corrientes, Rio Negro and Entre Rios were more related
among them and c) mites from Santa Cruz (population 1 and 2) are more similar to Neuquén
(being mites from Santa Cruz 1 equal to mites from Neuquén). Table 2 shows DNA
sequences obtained for each sample and the comparison with Anderson and Trueman (2000)
for Korean and Japanese haplotypes. All mites within a site shared identical sequences.

Table 1 Mean of each variable studied (millimeters) belonging to the morphotypes of Varroa destructor
from Argentina studied in this research (data published by Maggi et al. 2009b)
WDS LDS WMS LMS WGS LGS WAS LAS

Morphotype 1 1.757 1.178 0.358 0.449 0.729 0.565 0.258 0.146

Morphotype 2 1.711 1.128 0.351 0.449 0.716 0.562 0.265 0.155

WDS width of dorsal shield, LDS length of dorsal shield, WGS width of genital shield, LGS length of genital
shield, WMS width of metapodal shield, LMS length of metapodal shield, WAS width of anal shield, LAS
length of anal shield
Morphotype 1: mites from Rı́o Negro ? Santa Cruz
Morphotype 2: mites from Buenos Aires ? Neuquén ? Corrientes ? Entre Rı́os

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Discussion

In this work, we studied several samples of mites from Argentina which showed different
virulence against A. mellifera. As a result, we cover an extensive territory of the country
from north to south. Another examples for these kind of studies are those carried out in
China (Zhou et al. 2004), Indonesia and Java (Anderson and Trueman 2000) and in Spain
(Muñoz et al. 2008). However, we could not find the Japanese haplotype in samples

Table 2 Mitochondrial DNA (CO-I genes) from holotype Varroa jacobsoni (Java haplotype), holotype of
V. destructor (Korea haplotype) and the obtained in the present study in Argentina

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Table 2 continued

Bold letters indicate the variable regions between sequences

studied. Contrary, our results confirm that sequences under study for the COI fragment
share a 98% similitude with the Korean haplotype in each one of the mite populations
studied. However, we were able to detect genetic variations in the COI fragment among the
studied populations. For example, mites from Buenos Aires province showed the highest

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sequence variation. This fact deserves attention from a view point of genetic interaction
between host and parasite. Warrit et al. (2006) investigated the genetic diversity, bioge-
ography, and coevolution in Varroa mites and their host, A. cerana F in the Thai-Malay
Peninsula. They showed a strong geographic pattern in the distribution of the Mainland and
Sundaland lineages of A. cerana in Thailand, and in the distribution of Varroa species and
mitochondrial haplotypes. Taking into account this research (Warrit et al. 2006) and our
results, it could be probable that genetic variation of mites studied here were correlated
with different ecotypes of bees. This hypothesis should be tested in future research,
because we did not characterized genetically the lineage of A. mellifera used in our work.
Thereby, we are able to conclude that Korean haplotype is cosmopolite in Argentina and
consequently we extend its geographical distribution (before this study, the Korean hap-
lotype only was reported for Buenos Aires province). In addition, we sampled two of the
three morphotypes reported by Maggi et al. (2009b) and we were able to confirm that
all mite population belonged to the same haplotype despite these ones showed differ-
ent virulence against A. mellifera. Therefore, we discard a relationship among morpho-
types, haplotypes and virulence. It is possible that Varroa morphotypes reported by Maggi
et al. (2009b) could be explained as a result of morphometric correlations between
coexisting populations of V. destructor and A. mellifera (e.g., larger bees could sup-
port larger mites) or could be the result of local and current conditions: Maggi et al.
(2011b) reported that mite survival could be affected by mite size when an acaricide
treatment is applied. Thus, morphotypes reported by Maggi et al. (2009b) could have
originated as a result of different intensities of acaricide use (selection pressures). Thus,
mite sizes reported in each geographical place (morphotypes) could be those best
adapted to face particular acaricide treatments applications (local and current conditions).
With regard to the different virulences of Varroa populations studied here, a possible
explanation for this phenomenon is the degree of climatic conditions where sampling was
carried out and the ecotypes of bees infested by the mites. Rio Negro and Santa Cruz
provinces are characterized by an extreme cold winter; which leads (in the absence of
an acaricide treatment) to the death of bee colonies due they do not have enough bee
brood population to support Varroa parasitic loads. In the case of Rio Negro province also
exists a high influx of beehives from other zones of Argentina, which are brought to this
area for their development in spring. This continuous influx of beehives, probably leads to
a poor coevolution between native ecotypes of Rı́o Negro and their Varroa populations.
Nevertheless, more studies should be conducted in areas near to the frontier with Paraguay
and Brazil. Guerra et al. (2010) reported that Japanese haplotype was displaced from Brazil
by the Korean one, restricting its distribution to specific sites of the Brazilian country. As a
result, it is possible that Japanese haplotype was able to find ecological niches in geo-
graphical sites of Argentina near to Brazil.
Today, Argentine beekeeping is characterized by different population dynamics
of V. destructor. It is important to note that still exist areas in our country in which bee
colonies do not need acaricide treatments against Varroa. The results presented in this
study suggest that the Korean haplotype is cosmopolite in our country and probably,
the Japanese haplotype is not present or it is confined to endemic areas of Argentina. In
this way, if the Korean haplotype is the only one present in Argentina, another possible
explanation to the different virulence of Varroa observed in honeybees from Argentina
(not studied in this research) is the presence/absence of Africanized bees. The study
conducted by De Santis and Cornejo (1986) showed the occurrence of these bees in three
different northeast provinces of Argentina (Formosa, Misiones and Corrientes), although
its presence has also been reported in Rı́o Negro province (39 8S) (Dietz et al. 1985).

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It is already known that Africanized bees are more tolerant against mite populations than
European ones. The study conducted by Warrit et al. (2006) postulated that populations of
Varroa on different host populations are genetically differentiated, and may be adapted to
specific characteristics of their local host populations. In this way different haplotypes may
be correlated with differences in the mite’s ability to utilize specific host populations and
species. Taking into account this background, different outcomes can result when tolerance
against V. destructor is measured among several geographical places involving different
kind of bees (European or Africanized bees). In addition, it is possible that Varroa mites
become more virulent against Argentinean bees last years, due to a geographical retraction
of Africanized bees, result of the massive importation of European queens produced in
the last time. Currently in Argentina, different outcrosses and recombination processes
between Africanized honeybee and the previous European introduced bee, allowed the
formation of local ecotypes with morphological, behavioral and physiological proper
features (Basualdo et al. 2001). These authors reported a massive introduction of queen
honeybees from Buenos Aires province (where Apis mellifera ligustica was the main
introduced subspecies) to the northeast and northwest of the country. Thus, the European
gene frequency in Africanized saturated regions might be higher than those previously
reported (Basualdo et al. 2001) affecting Varroa virulence.
In this research we sampled mite populations only from European bees; future studies
should be conducted in areas where both genotypes of bees are present. The results
obtained from these types of studies would generate new tools to be incorporated into an
integrated pest management of mite populations in Argentina.

Acknowledgments The authors would like to thank the Universidad Nacional de Mar del Plata (UNMDP),
Consejo Nacional de Investigaciones Cientı́ficos y Técnicas (CONICET), Prof. Ives Le Conte for their help
and criticism and to Nancy Garcı́a, Manuel Darı́oMathot, JuanMange, Pablo Pérez, Natalia Messina, Fer-
nando Mariani, Pedro Bailac, José Ernesto Nuñez Camelino, Cristiansen, Jose Luis Carlachiani, Freddy
Alemán, Santiago Plischuk, and Campo & Abejas for their help in the sampling.

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