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dihydrofolate reductase renders malaria parasites insensitive to
WR99210 but does not affect the intrinsic activity of proguanil. Proc.
Natl. Acad. Sci. U. S. A. 94, 10931 10936
30 Walter, R. et al. (1991) Pyrimethamine-resistantPlasmodiumfalciparum
lack cross-resistance to methotrexate and 2,4-diamino-5-(substituted
benzyl) pyrimidines. Parasitol. Res. 77, 346 –350
31 Cunningham, R.F. et al. (1981) Clinical pharmacokinetics of probene-
cid. Clin. Pharmacokinet. 6, 135 –151
1471-4922/$ - see front matter q2003 Elsevier Ltd. All rights reserved.
Africanized honeybees have unique tolerance to
Varroa mites
Stephen J. Martin
and Luis M. Medina
Laboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield, Western Bank,
Sheffield, S10 2TN, UK
Departamento de Apicultura, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autonoma de Yucatan,
Apartado Postal 4-116, CP 97100, Merida, Yucatan, Mexico
Varroa destructor is an ectoparasitic mite of the adult
honeybee, which parasitizes the bee brood. This mite has
killed millions of honeybee Apis mellifera colonies, world-
wide, eliminating wild populations throughout Europe
and North America [1], and resulting in the loss of billions
of dollars in agricultural production. The Africanized
honeybee (AHB) has a unique tolerance to V. destructor
that is not present in the A. mellifera European honeybee
(EHB), from which the AHB hybrid was derived [2]. This
unexpected tolerance mechanism provides a valuable
insight into the evolution of host parasite interactions.
Varroa mites feed solely on the hemolymph of honey-
bees, and their entire reproductive cycle is completed
within a sealed honeybee brood cell [1].InApis cerana
(the original host of Varroa), mite reproduction occurs only
in the small number of sealed male (drone) honeybee brood
cells. Consequently, mite populations within an A. cerana
colony are low (,800) and no adverse effects are seen. In
A. mellifera EHB colonies, V. destructor also reproduces in
the much more numerous worker brood cells [1], enabling
mite populations to increase up to 2000-fold annually [3],
causing colony death within one year [4]. However, mite
populations in similar-sized AHB colonies stabilize at
1000–3000 mites per colony [3,5], allowing colonies to
survive indefinitely (L.M. Medina, PhD Thesis, University
of Sheffield, 2003), although the resistance mechanism,
until now, has remained elusive.
Varroa kills host colonies indirectly by providing a new
transmission route for a few naturally occurring honeybee
viruses such as the deformed wing virus (DWV) [6,7].
Therefore, for a viral epidemic to kill a honeybee colony
comprising 20 000 honeybees, a minimum number of
vectors (mites) are required. The number of mites required
to sustain a viral epidemic varies with viral virulence and
honeybee longevity because both of these factors affect the
number of honeybees acting as viral reservoirs [6,7].
The daily changes in mite populations reproducing in
simulated A. cerana, AHB and EHB colonies were
investigated using a honeybeemite simulation model
(L.M. Medina, op. cit.)[6]. Mite population growth in EHBs
and AHBs is determined largely by the average number of
mated female mite offspring produced in worker brood
cells per reproductive cycle (Wr). For the Korean haplotype
of V. destructor reproducing in EHB in the UK and South
Africa, the Wr is 0.92, whereas in AHB in Mexico and
Brazil, the Wr is 0.73 and 0.64, respectively [8].By
changing only the value of Wr, the model generated either
a stable mite population in AHB and A. cerana colonies, or
an increasing mite population in EHB colonies [6]
(Figure 1a). The working hypothesis is therefore, at low
mite populations in all colonies, mites reproducing in
drone brood cells, which have a high reproductive success,
contributed mainly to the initial mite population growth.
However, because mites also show a tenfold preference to
reproduce in drone cells (which comprises only 1 5% of all
the honeybee brood), they soon become overcrowded as the
mite population increases. This leads to inter-mite
competition for the limited food and space, causing an
increase in mite mortality [9] and resulting in negative
reproductive success for mites entering these overcrowded
drone cells. Thus, mite population growth in drone brood
cells is limited by a density-dependent mechanism.
Although this occurs in all colony types, it is the normally
overlooked reproductive ability in worker brood cells that
has the crucial role in determining whether the mite
becomes a pest. In A. cerana (Figure 1b), no mite
reproduction occurs in worker brood cells per reproductive
cycle (Wr ¼0) and the mite population stabilizes at a low
level (,800 mites per colony). In AHB (Figure 1c), limited
mite reproduction can occur in worker brood cells
(Wr ¼0.7) and the mite population stabilizes at a higher
level (10003000 mites). However, in EHB (Figure 1d),
mite reproduction in worker brood cells (Wr ¼0.9) is more
than sufficient to compensate for losses as a result of
overcrowding in drone brood cells, allowing the mite
population to increase until the colony dies. The short
adult longevity of AHB (21 days versus 25 180 days for
EHB) as a result of the tropical or sub-tropical climate
Corresponding author: Stephen J. Martin (
Update TRENDS in Parasitology Vol.20 No.3 March 2004
Figure 1. Effect of mite fertility in honeybee worker cells on mite population growth. (a) Predicted growth curves for mite populations in Africanized Apis mellifera (AHB)
(Wr ¼0.7), European A. mellifera (EHB) (Wr ¼0.9) and Apis cerana (Wr ¼0) colonies. The daily relative change in mite number in worker (black line) and drone (red line)
brood in A. cerana (b), AHB (c) and EHB (d) colonies are indicated. The gray region represents the period when the overall mite population is increasing. Data obtained
from S.J. Martin and L.M. Medina (2003) Varroa tolerance in Africanized honeybees explained, Abstract no. 274, XXXVIIIth Apimondia International Apicultural Congress,
held 24– 29 August 2003 in Ljubljana, Slovenia. Abbreviations: AHB, Africanized honeybee; EHB, European honeybee; Wr, average number per reproductive cycle of mated
female mite offspring produced in worker sealed cells.
TRENDS in Parasitology
Daily relative change in mite no.
(worker brood) Daily relative change in mite no.
(worker brood) Daily relative change in mite no.
(worker brood)
Daily relative change in mite no.
(drone brood)
Daily relative change in mite no.
(drone brood)
Daily relative change in mite no.
(drone brood)
Mite population
Increasing Increasing Increasing
Increasing Increasing Increasing
= 0.9
= 0.7
= 0
= 0.9
= 0.7
= 0
Time (years)
Time (years)
Time (years)
Time (years)
Update TRENDS in Parasitology Vol.20 No.3 March 2004 113
indicates that .12 000 mites are needed to kill an AHB
colony [7]. Therefore, although DWV is present in AHB
and A. cerana colonies, mite populations stabilize at levels
well below that required to kill the colony.
It is unlikely that AHB evolved Varroa tolerance after
the AHB hybrid was created as a result of increased
hygienic behaviour or brood attractiveness [10] because
such factors are unlikely to lead to a stabilized mite
population. Instead, tolerance has probably resulted from
pre-existing resistance characteristics fortuitously coming
together in the hybrid. That is a high level of mite offspring
mortality in worker brood and a short life span in the adult
1 Webster, T.C. and Delaplane, K.S. (2001) Mites of the Honey Bee,
Dadant publication, Illinois
2 Martin, S.J. and Kryger, P. (2002) Reproduction of Varroa destructor in
South African honey bees: does cell space influence Varroa male
survivorship? Apidologie (Celle) 33, 51 –61
3Vandame, R. et al. (2000) Levels of compatibility in a new
host – parasite asso ciation: Apis mellifera Varroa jacobsoni.Can.
J. Zool. 78, 2037 –2044
4 Martin, S.J. et al. (1998) A scientific note on Varroa jacobsoni
Oudemans and the collapse of Apis mellifera colonies in the United
Kingdom. Apidologie (Celle) 29, 369–370
5 Medina, L.M. et al. (2002) Reproduction of Varroa destructor in worker
brood of Africanized honey bee (Apis mellifera). Exp. Appl. Acarol. 27,
6 Martin, S.J. (2001) The role of Varroa and viral pathogens in the
collapse of honey bee colonies: a modelling approach. J. Appl. Ecol. 38,
1082– 1093
7 Sumpter, D. and Martin, S.J. (2004) The dynamics of virus epidemics
in Varroa infested honey bee colonies. J. Anim. Ecol. 73, 51 –63
8 Corre
ˆa-Marques, M.H. et al. (2003) Comparing data on the reproduc-
tion of Varroa destructor.Genet. Mol. Res. 2, 1–6
9 Donze
´, D. and Guerin, P.M. (1997) Time-activity budgets and
space structuring by the different life stages of Varroa jacobsoni in
capped brood of the honey bee Apis mellifera.J. Insect Behav. 10,
10 Guzma
´n-Novoa, E. et al. (1999) Susceptibility of European and
Africanized honey bees (Apis mellifera)toVarroa destructor in Mexico.
Apidologie (Celle) 30, 173–182
1471-4922/$ - see front matter q2004 Elsevier Ltd. All rights reserved.
Free-living endohelminths: the influence of multiple
Neil J. Morley and John W. Lewis
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
In a recent review by Pietrock and Marcogliese [1],an
interpretation of laboratory data on the survival and
infectivity of free-living stages of endohelminths and the
influence of environmental factors, especially toxic pollu-
tants, was undertaken. Although we agree with their
basic interpretations, there has, however, been an over-
simplification of the significance of such data, and the
importance of biotic factors to free-living endohelminths
has been overlooked.
In our recent review of laboratory and field studies on
the transmission of larval digeneans in polluted conditions
[2], we emphasized that the influence of toxicants on
digenean transmission is highly complex, with much of the
observed effects in the laboratory often masked by other
factors in the field. In particular, the mobility of
vertebrates as target and source hosts for free-living
endohelminths can represent a major factor in prevalence,
as demonstrated by Siddall et al., who found that in
laboratory studies the survival of miracidia and cercariae
of Zoogonoides viviparus was reduced in the presence of
sewage sludge [3]. Field studies demonstrated that the
prevalence of Z. viviparus in its molluscan intermediate
host had a reduced gradient in parasitism towards a
sewage dumpsite [4] and appeared to confirm the
laboratory findings. However, the prevalence of Z. viviparus
in the definitive fish host, Hippoglossoides platessoides,
revealed no differences between control and polluted sites
[5]. This fish is highly mobile, and it was considered that
intermixing within its population masked the pollution
effects demonstrated in the intermediate host. Conflicting
results are also apparent in some coastal bird parasite
systems [2], suggesting that caution is necessary when
considering the impact of environmental factors on free-
living helminth ‘transmission success’ under isolated
laboratory conditions.
The influence of biotic factors on free-living endohel-
minths is as important as abiotic factors. The physiological
status of the host can influence the functional biology of
free-living stages. For example, the rate of hatching
of Schistosoma mansoni eggs is related to host age and
intensity of adult worm infections [6], whereas both
the survival and infectivity of cercariae are linked to the
health of the mollusc from which they emerge [7,8]. The
susceptibility of a target host to infection by free-living
stages is often dependent not only on host age [7,9], but
also by the distribution [10] and density [11] of the
target host population. Complex interactions can occur
in multi-species host communities, with hosts of low
susceptibility acting as decoys to reduce the prevalence of
infection in species of high susceptibility [12], and a range
of invertebrates could interfere with the host-finding
process [13].
Therefore, all investigators must avoid implying that
simplified laboratory studies can accurately reflect
Corresponding author: Neil J. Morley (
Update TRENDS in Parasitology Vol.20 No.3 March 2004
... Interestingly, the crossing between Varroa-tolerant African honey bees and susceptible Western honey bees resulted in a hybrid honey bee species known as Africanized honey bees. These bees also possess Varroa resistance traits (30), which must have been a key life history trait to promote their successful spread throughout the Americas (31). Given that Western honey bees are highly susceptible to Varroa, the tolerance and/or resistance traits reported in Africanized honey bees must therefore have originated from their African ancestors. ...
... Male larvae are generally assumed to be more susceptible and have higher mite infestation levels compared with worker larvae (53,54). Furthermore, African and Eastern honey bees have been reported to have higher levels of mite tolerance compared with Western bees (26,30). Our comparative approach therefore allowed us to narrow down on individual molecules or molecular networks that we assume to be part of the innate immune system of honey bees and that can be linked to increased or decreased levels of disease tolerance. ...
... These bees are a hybrid between African and Western honey bees and have been remarkably successful, given they were able to spread throughout South and Central America since they escaped from a laboratory in Brazil in 1957. They are also known for their increased levels of Varroa resistance (30,59). Their ecological success implies that these bees inherited their tolerance traits from their African honey bee ancestors, something that could be studied in the future. ...
Full-text available
Innate immune systems are key defenses of animals and are particular important in species that lack the sophisticated adaptive immune systems as found in vertebrates. Here, we were interested to quantify variation in innate immune responses of insects in hosts that differ in their parasite susceptibility. To do this, we studied immune responses in honey bees, which can host a remarkable number of different parasites, which are major contributors of declining bee health and colony losses. The most significant parasite of honey bees is the mite Varroa destructor, which has infested the majority of global honey bee populations and its control remains a major challenge for beekeepers. However, a number of non-managed honey bees seem able to control Varroa infections, for example the Eastern honey bee Apis ceranae or the African honey bee Apis mellifera scutellata. These bees therefore make interesting study subjects to identify underlaying resistance traits, for example by comparing them to more susceptible bee genotypes such as European honey bees (Apis mellifera). We conducted a series of interlinked experiments and started with behavioral assays to compare the attractiveness of bee larvae to mites using different honey bee genotypes and castes. We found that 6-day old larvae are always most attractive to mites, independently of genotype or castes. In a next step we compared volatile profiles of the most attractive larvae to test whether they could be used by mites for host selection. We found that the abundance of volatile compounds differed between larval ages, but we also found significant differences between genotypes and castes. To further study the expected underlaying physiological differences between potentially resistant and susceptible host larvae, we compared the larval hemolymph proteomes of the three honey bee genotypes and two castes in response to mite exposure. We identified consistent upregulation of immune and stress related genes in Varroa exposed larvae which differed between genotypes and castes but tolerant honey bee genotypes and castes were characterized by stronger immune responses. In summary, we provide first insights into the complex involvement of the innate immune system of honey bees against mite infestations, which could be used for future breeding purposes.
... This confirms that the fertility of V. destructor is not a factor that explains the differential damage of the mite in the two bee populations. However, other studies in populations of bees naturally surviving V. destructor attribute its reduced impact on the colonies to the low fertility of the mite [24,[48][49][50]. On the other hand, differences in the abundance, intensity, and prevalence of V. destructor were found in the colonies of the two groups in both apiaries. ...
Full-text available
In the past few years there has been an increasing interest for the study of honey bee populations that are naturally resistant to the ectoparasitic mite Varroa destructor, aiming to identify the mechanisms that allow the bees to limit the reproduction of the mite. In eastern Uruguay there are still bees resistant to mites that survive without acaricides. In order to determine if the differential resistance to V. destructor was maintained in other environments, a reciprocal transplant experiment was performed between the mite-resistant bee colonies and the mite-susceptible bee colonies from the east and the west of the country, respectively, infesting bees with local mites. In both regions, the mite-resistant colonies expressed a higher hygienic behavior and presented a higher phoretic mites/reproductive mites and mites in drone cells/mites in worker cells ratio than the mite-susceptible colonies. All the mite-susceptible colonies died during fall–winter, while a considerable number of mite-resistant colonies survived until spring, especially in the east of the country. This study shows that the bees in the east of the country maintain in good measure the resistance to V. destructor in other regions and leaves open the possibility that the mites of the two populations have biases in the reproductive behavior.
... This potentially is a key, but currently overlooked part, of the resistance mechanism. Since an empirical model 26 honeybee colonies only when the initial drone cells are present. ...
Full-text available
The Varroa destructor ectoparasitic mite has spread globally and in conjunction with Deformed Wing Virus has killed millions of honeybee (Apis mellifera) colonies. This has forced Northern hemisphere beekeepers into using miticides to avoid mass colony losses. However, in many Southern hemisphere countries widespread treatment did not occur since miticides were prohibitively expensive, or a centralised choice was made not to treat, both allowing natural selection to act. The Varroa mite initially caused high losses before mite-resistance appeared in the honeybee populations. Initially, mite-resistance was only associated with African and Africanised honeybees. Although recently, several isolated mite-resistant European honeybee populations have appeared. Here we studied the mite-resistance in Cuba and found high rates of recapping of infested worker cells (77%), high removal of mites (80%) and corresponding low mite fertility (r = 0.77). These are all traits found in all naturally evolved Varroa-resistant populations. We can confirm Cuba has the world’s largest European mite-resistant population with 220,000 colonies that have been treatment-free for over two decades and illustrating the power of natural selection. Cuban honeybees are also highly productive, 40–70 kg of honey produced annually, and are mild mannered. Cuba is an excellent example of what is possible when honeybees are allowed to adapt naturally to Varroa with minimal human interference.
... The results of this study add to the notion of Africanized bee resistance to V. destructor parasitism, which has been documented in a number of studies [32,34,35,38,39,59,60]. The higher relative resistance of Africanized bees to V. destructor is apparently due in part to a lower attractiveness of Africanized bee brood to being parasitized by the mite [34], to lower rates of reproduction of the mite in the brood of Africanized bees [40,61,62], to frequent colony swarming and evasion [63], or to greater expression of mechanisms of social immunity such as hygienic and grooming behavior, compared to bees of European descent [33,[36][37][38]42,[64][65][66]. ...
Full-text available
This study was conducted to analyze the effect of genotype and climate on the resistance of honey bee (Apis mellifera) colonies to parasitic and viral diseases. The prevalence and intensity of parasitism by Varroa destructor, or infection by Nosema spp., and four honey bee viruses were determined in 365 colonies of predominantly European or African ancestry (descendants of A. m. scutellata) in subtropical and temperate regions of Mexico. Varroa destructor was the most prevalent parasite (95%), whilst N. ceranae was the least prevalent parasite (15%). Deformed wing virus (DWV) and black queen cell virus (BQCV) were the only viruses detected, at frequencies of 38% and 66%, respectively. Varroa destructor was significantly more prevalent in colonies of European ancestry (p < 0.05), and the intensity of parasitism by V. destructor or infection by DWV and BQCV was also significantly higher in colonies of European descent than in African descent colonies (p < 0.01), although no genotype–parasite associations were found for N. ceranae. Additionally, significant and positive correlations were found between V. destructor and DWV levels, and the abundance of these pathogens was negatively correlated with the African ancestry of colonies (p < 0.01). However, there were no significant effects of environment on parasitism or infection intensity for the colonies of both genotypes. Therefore, it is concluded that the genotype of honey bee colonies, but not climate, influences their resistance to DWV, BQCV, and V. destructor.
... In the same way as the other infestation parameters, mite fertility also presented great variation between regions, but low levels were generally found. This result was expected considering the direct relationship between infestation levels and reproductive potential, as observed in several studies (Martin, 1994;Martin & Medina, 2004;Rosenkranz et al., 2010). These variations and low levels found in AHB are generally attributed to high levels of offspring mortality, including the only male produced by the first laid egg (Mondragon et al., 2006). ...
Full-text available
The mite Varroa destructor is one of the most studied parasites in apiculture, and its genotype variation is a key factor for the severity of infestation in bee colonies. Here we report the genetic and reproductive profile of mites from 14 Brazilian states with different geographic and climatic conditions. We performed PCR to amplify a fragment of the COI gene and differentiate the haplotypes using restriction enzymes. The K haplotype was widely prevalent in the studied sites, while the J haplotype was found only in four municipalities. We also observed both haplotypes (J and K) coexisting in the same colony, a fact unprecedented in Brazil. Infestation levels were low (0.33 to 15.3%). The reproductive potential showed wide variation (0 to 1.5), indicating that even with the massive presence of K haplotype, environmental and biotic factors related to Africanized honeybees may be responsible for maintaining the mite under low levels in Brazil.
... An apparently harmless symbiont to one species can become a severe parasite when crossing over to a different species. An interesting example is the mite V. destructor that spread from a resistant host, A. cerana, to the susceptible A. mellifera causing major colony losses worldwide (Martin and Medina 2004). ...
... At the same time, a lack of correlation between elevation and Varroa levels suggests that the mite has managed to adapt to the environmental conditions of the highlands since there were IRs with slight variations at the three altitude tiers. However, a genetic component could also influence the bees since the IRs found were lower than those found in populations of European genotype and similar to those of African origin [45,46]. ...
Full-text available
The aim of this research was to analyze the relationship among hygienic behavior (HB), Varroa destructor infestation, and honey production in the central highlands of Ecuador. Overall, 75 honey bee colonies were evaluated before, during, and after production at three altitude levels (2600–2800, 2801–3000, and >3000 m.a.s.l.). The hygienic behavior percentage of the colonies was determined by the pin-killing method, and the colonies were classified into three groups: high HB (>85%), mid HB (60.1–85%), and low HB (≤60%). Varroa infestation was diagnosed as well, and honey production was evaluated only during production. HB was high and heterogeneous, averaging 80% ± 9.7%. Its highest expression was observed at lower altitudes. The infestation degree was low (3.47% ± 1.56%), although the mite was detected in all colonies upon sampling. A negative correlation was observed between HB and Varroa infestation in the first sampling (−0.49 **), suggesting that the high- and mid-altitude HB colonies underwent the lowest infestation rates, regardless of sampling. The correlations between HB and production were significant (0.26 *), indicating a positive effect of HB on production, meaning that colonies with high HB obtained the highest honey production (25.08 ± 4.82 kg/hive). The HB of bees showed an inverse relationship with altitude and it tended to reduce the effect of Varroa infestation, favoring honey production and, thus, suggesting the feasibility of selecting colonies with high HB.
... The current selection methods include hygienic behavior and grooming, length of post-Capping stage, brood attractiveness and low mite fecundity. Martin and Medina ( 2004 ) reported tolerance to V. destructor in the Africanized honeybee that is not present in the A. mellifera from which the AHB hybrid was derived. Medina ( 2003 ) in an extensive study reported that mite reproduction (<800/ colony) in A. cerana occurs only in the small number of sealed male (drone) honeybee brood cells with no adverse effects on colony development. ...
... The Asian honeybee Apis cerana , the original host of V. destructor , is resistant to the parasitic mite (Peng et al. 1987). "Africanized honeybees" are hybrids of an African and a European subspecies of the western honeybee Apis mellifera and are assumed to have become tolerant to Varroa by restricting the size of the mite population (Martin and Medina 2004). However, most subspecies of A. mellifera exhibit weaker grooming and broodremoval behavior than A. cerana and have no effective resistance against Varroa (Peng et al. 1987; (Kralj et al. 2007;Kralj and Fuchs 2004;Yang and Cox-Foster 2007). ...
This datasheet on Apis mellifera scutellata covers Identity, Overview, Distribution, Dispersal, Diagnosis, Biology & Ecology, Environmental Requirements, Natural Enemies, Impacts, Uses, Prevention/Control, Management, Further Information.
Full-text available
The knowledge generated from several studies conducted in Mexico on the susceptibility of European and Africanized honey bees to Varroa jacobsoni is reviewed and compared with the situation in Brazil. There is evidence of genotypic variation for mite population growth, and for tolerance to the mite in honey bee colonies located in Mexico. However, Mexican honey bees seem to be relatively less tolerant to the parasite than bees in Brazil. The main difference is that mite fertility rates in Mexico are higher than those reported from Brazil. Hypotheses for why the situation is different in Mexico than in Brazil are discussed. (C) Inral/DIB/ACIB/Elsevier, Paris.
Full-text available
We investigated the relationships between the honey bee, Apis mellifera, and the parasitic mite Varroa jacobsoni in Mexico. In an 18-month survey of European honey bees (EHB) and Africanized honey bees (AHB), we showed that EHB were highly compatible with V. jacobsoni, while AHB were not as compatible. Furthermore, mite infertility ("parasite infectivity" factor), suspected to be the main factor of low AHB/V. jacobsoni compatibility in Brazil, was not observed in Mexico. The "intrinsic rate of natural increase" of mites did not differ significantly between host subspecies, indicating that the cause of low compatibility appears only at high parasite densities. The "carrying capacity" was twice as high in EHB as in AHB, indicating that the cause of low compatibility is possibly linked to honey bees' behavior. We hypothesize that the reason why V. jacobsoni is highly fertile on Mexican AHB (whereas it has low fertility on Brazilian AHB) may be that different strains of V. jacobsoni exist in the two countries.
Full-text available
Apis mellifera / Varroa jacobsoni / virus/ colony death / Great Britain The mechanism by which the Varroa jacob-soni mite causes the Apis mellifera colony to col-lapse is still not understood. Some apparently healthy colonies are able to support large mite populations while others containing a much lower mite population collapse. One possible explana-tion is the impact of various diseases, particu-larly certain viruses. Acute paralysis virus (APV) has been associated with colony death in mite infested colonies in Germany [3], Russia [4] and the USA [6]. The aim of this preliminary study was to investigate the role of the mite population and other diseases in the collapse of A. mellifera colo-nies in the UK. Eight naturally infested A. mellifera colonies fitted with screened floors had their debris col-lected weekly and the number of sealed brood and adult bees estimated monthly, until they col-lapsed. Samples of dead bees and live brood were collected at irregular intervals and sent to Brenda Ball at IACR-Rothamsted to be tested against antisera to ten bee viruses [3]. The colonies were also checked for signs of other common bee diseases. Four colonies survived one full summer, one colony survived two summers while three colo-nies survived three summers. All colonies died during the winter within 4 years of becoming infected (table I). The signs of colony collapse, which were similar in all cases, were a decline in the adult bee population eventually resulting in only a few bees (< 200) and the queen. No, or very few, dead bees were found in the hive. The mean number of bees and sealed brood produced during the year did not differ signifi-cantly from the year preceding either colony col-lapse or survival. Also, during the year prior to collapse, colonies appeared to function normally, producing comparable honey yields to colonies treated with Bayvarol®. The number of mites (cumulated total, peak and monthly means) in the debris was found to be a poor indicator of colony survivorship in the following year. The total yearly natural mite drop ranged from 10 000 to 40 000 (mean = 20 000 ± s.e. = 3 800, n = 7) in colonies which lived the following year and from 10 000 to 60 000 (mean = 29 000 ± s.e. = 6 000, n = 8) in those that col-lapsed in the following year. This corresponds to estimated peak mite populations of 2 500 to 15 000 in surviving colonies and 2 600 to 16 000 mites in collapsing colonies, as indicated by a mite model [8]. Other bee diseases (foulbrood, chalkbrood, Nosema apis, Amoeba and the para-site Acarapis woodi) were either not detected or at insignificant levels.
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Summary 1. When the parasitic mite Varroa jumped species from the eastern to the western honey bee, millions of infested bee colonies died. Recent work has revealed that the probable cause of this collapse is that mites provide a new route of transmission, by acting as a vector, for certain bee viruses. 2. Using a mathematical model parameterized by recently collected data on bee viruses, we investigate the relationship between the mite load in a colony and the possibility of a virus epidemic occurring within a bee colony. 3. The model suggests that the balance of coexistence between mite, virus and bee in the eastern honey bee, has been lost in the western bee host, not simply because of the new transmission route, but also because mite populations in western honey bee colonies has exceeded a critical epidemic threshold. We quantify the critical epidemic mite load for two well-studied bee viruses, acute paralysis virus and deformed wing virus, through the colony's yearly life cycle. 4. As well as providing practical insights into mite control strategies, the model allows us to disentangle the relative importance of different bee and mite behaviours in virus spread. We consider the evolutionary aspects of the new route of virus transmission, looking in particular at how changes to social organization might bring about collective resistance.
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1. The ecto-parasitic mite Varroa destructor is a serious world-wide pest of the honeybee Apis mellifera and has being linked with the death of millions of colonies, although its role in colony death has remained elusive. 2. A simulation model was developed to explain the link between the mite and collapse of the host bee colony, given that colony death does not always occur. We investigated the effects of two pathogens, deformed wing virus (DWV) and acute paralysis virus (APV), vectored by the mite, on the host colony. 3. Two previously published simulation models, a bee and a mite, were combined and adapted for use in temperate climates with a variety of bee diseases. The model was constructed using Modelmaker ® software, which allows the progression of a disease in the host colony to be followed daily. 4. The population dynamics generated by the model were similar to those observed in a natural honeybee colony. When DWV- or APV-transmitting mites were introduced into the colony, its adult worker bee population collapsed either during winter or spring for DWV, or autumn to spring for APV. This corresponds well with field observations
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The ability of Varroa destructor to reproduce in the African honey bee Apis mellifera scutellata was studied. In addition, the effects of space within the brood cell and short brood developmental time on mite reproduction, was investigated using A. m. scutellata cells parasitised by a A. m. capensis worker pseudo-clone. In A. m. scutellata worker cells Varroa produced 0.9 fertilised females per mother mite which is the same as found in susceptible European honey bees, but greater than the 0.4 produced in cells containing the pseudo-clone. Low mite reproductive success in cells containing pseudo-clone was mainly as a result of increased mite mortality. This was caused by male protonymphs and some mothers becoming trapped in the upper part of the cell due to the pseudo-clone being 8% larger than their host and not due to their short developmental time. Therefore, mite populations in South African A. m. scutellata and A. m. capensis honey bees are expected to increase to levels observed in Europe and USA.
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Reproduction and population growth of Varroa destructor was studied in ten naturally infested, Africanized honey bee (AHB) (Apis mellifera) colonies in Yucatan, Mexico. Between February 1997 and January 1998 monthly records of the amount of pollen, honey, sealed worker and drone brood were recorded. In addition, mite infestation levels of adult bees and worker brood and the fecundity of the mites reproducing in worker cells were determined. The mean number of sealed worker brood cells (10,070 +/- 1,790) remained fairly constant over the experimental period in each colony. However, the presence and amount of sealed drone brood was very variable. One colony had drone brood for 10 months and another for only 1 month. Both the mean infestation level of worker brood (18.1 +/- 8.4%) and adult bees (3.5 +/- 1.3%) remained fairly constant over the study period and did not increase rapidly as is normally observed in European honey bees. In fact, the estimated mean number of mites fell from 3,500 in February 1997 to 2,380 in January 1998. In May 2000 the mean mite population in the study colonies was still only 1,821 mites. The fertility level of mites in this study was much higher (83-96%) than in AHB in Brazil (25-57%). and similar to that found in EHB (76-94%). Mite fertility remained high throughout the entire study and was not influenced by the amount of pollen, honey or worker brood in the colonies.
The genetic and phenotypic characterization of a new Arabidopsis mutant, de-etiolated-3, (det3), involved in light-regulated seedling development is described. A recessive mutation in the DET3 gene uncouples light signals from a subset of light-dependent processes. The det3 mutation causes dark-grown Arabidopsis thaliana seedlings to have short hypocotyls, expanded cotyledons, and differentiated leaves, traits characteristic of light-grown seedlings. Despite these morphological changes, however, the det3 mutant does not develop chloroplasts or show elevated expression of nuclear- and chloroplastencoded light-regulated mRNAs. The det3 mutation thus uncovers a downstream branch of the light transduction pathways that separates leaf development from chloroplast differentiation and light-regulated gene expression. In addition, light-grown det3 plants have reduced stature and apical dominance, suggesting that DET3 functions during growth in normal light conditions as well. The genetic interactions between mutations in det1, det2, and det3 are described. The phenotypes of doubly mutant strains suggest that there are at least two parallel pathways controlling light-mediated development in Arabidopsis.
Varroa jacobsoni reproduces in honey bee brood cells. Here the behavioral activity and use of space by infestingVarroa females and progeny were quantified in transparent artificial brood cells. The time-activity budget of both infesting and developing mites converged toward a stable pattern which was established during the bee prepupal stage of the infesting mites and the protonymphal stage of mite progeny. The pattern was such that infesting females and offspring eventually divided their activity between the fecal accumulation on the cell wall, which served as the rendezvous site for newly molted individuals, and the feeding site prepared on the pupa by the foundress. Other parts of the cell wall were used for oviposition and molting, away from the fecal accumulation on which activity of mobile stages was concentrated. Space structuring and the time-activity budget inVarroa probably evolved to enhance the number of fertilized females produced within the capped brood, where space and time are limiting factors. These behavioral adaptations parallel those of other mite species which show group behavior within cavities.