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Journal of Apicultural Research and Bee World 48(1): 11-14 (2009)

© IBRA 2009

DOI 10.3896/IBRA.


A new approach for detecting effective reproductive ability of Varroa destructor (Acari: Varroidae). Roger Strapazzon1, Diego Fagundes Kolling1, Francisco Estevão Carneiro1, Sabrina Alejandra Ramirez1, José Carlos Vieira Guerra Jr1, Geraldo Moretto1*. 1

Departamento de Ciências Naturais, Universidade Regional de Blumenau, 89010-971 Blumenau – SC, Brazil.

Received 22 June 2007, accepted subject to revision 13 June 2008, accepted for publication 12 August 2008. *Corresponding author: Email:

Summary The effective reproductive capacity of Varroa destructor in honey bee colonies is currently calculated on the basis of the number of female deutonymphs found in singly infested worker brood cells at 17-18 days (two to three days before the bee emerges). This calculation presumes that the deutonymphs will reach the adult stage by the time that the adult bee ecloses. Some deutonymphs may not, however, reach the adult phase and there also could be mortality. In order to examine this possibility, we studied mite reproduction in worker brood of Africanized honey bee colonies at 17-18 days and then selected eight colonies in which over 90 % of the infested brood cells contained a single original female mite. The mean proportion of singly infested worker brood cells in these colonies was 96.3 %. Consequently, by subtracting one from the total number of adult female mites found at the time the bee emerged we would be able to estimate the effective reproductive capacity of the original mites, with little error due to the very few cells invaded by more than one original mother mite. Among 377 singly infested worker brood cells analysed at 17-18 days, we found an estimated mean of 1.51 deutonymphs per original female mite. In 250 worker brood cells from the same colonies analysed at bee emergence (two days later) the mean number of new female adult mites was estimated to be 1.07. Thus the effective mite reproductive rate was only 71 % of the original estimate of 1.51. We conclude that the conventional technique of analyzing mite reproduction in 17-18 day old worker brood cells considerably overestimates the actual reproductive rate.

Un nuevo enfoque para la detección de la capacidad reproductiva efectiva de Varroa destructor (Acari: Varroidae). Resumen La capacidad reproductiva efectiva de Varroa destructor en colonias de abejas se calcula actualmente en base al número de deutoninfas hembras encontradas en las celdas de cría de obreras de 17-18 días (de dos a tres días antes de que la abeja eclosione). Este cálculo supone que la deutoninfa llegará a la edad adulta en el momento en que la abeja adulta eclosione. Algunas deutoninfas no podrán, sin embargo, llegar a la fase adulta, y también puede haber mortalidad. Con el fin de examinar esta posibilidad, se estudió la reproducción del ácaro en la cría de obreras de colonias de abejas africanizadas de 17-18 días y luego se seleccionaron ocho colonias en las que más del 90% de las celdas con cría infestada contenían un solo ejemplar del ácaro hembra fundador. La proporción media de celdas de cría de obrera infestadas en estas colonias fue del 96,3%. Por consiguiente, restando uno al número total de hembras maduras encontradas en el momento en que la abeja emerge, podríamos estimar la capacidad reproductiva efectiva de los ácaros fundadores, con un poco de error debido a las escasas celdas invadidas por más de un ácaro fundador. Entre las 377 celdas de cría de obrera infestadas analizadas de 17-18 días, hemos encontrado una media estimada de 1,51 deutoninfas por hembra fundadora. En 250 celdas de cría de obrera de las mismas colonias analizadas tras la eclosión de las abejas (dos días más tarde) el número medio de nuevas hembras adultas de ácaros se estimó en 1,07. Así, la tasa de reproducción efectiva del ácaro fue sólo del 71% de la estimación original de 1,51. Se concluye que la técnica convencional de análisis de la reproducción de Varroa en celdas de cría de obrera de 17-18 días sobrestima considerablemente la tasa de reproducción. Keywords: Varroa destructor, reproductive ability, Apis mellifera, Africanized bees, foundress mites, worker brood emergence.


Strapazzon, Koling, Carneiro, Ramirez, Guerra, Moretto


offspring produced by each female mite is therefore estimated based

Varroa destructor (Anderson and Trueman, 2000) is an ectoparasite

on the number of deutonymphs counted before worker brood

mite responsible for causing serious damages to beekeeping

emergence. In this work, we adopted a different methodology to

worldwide. Severe mortality of honey bee (Apis mellifera L.) colonies

measure the effective reproductive rate by measuring it at two stages

is common in some parts of the world when colonies are not treated

of bee development. The objective of this study was therefore to

against the mite using pesticides. The haplotype of V. destructor is

evaluate the reproductive ability of female V. destructor through the

considered to be an important factor that affects mite virulence. In

analysis of its offspring during the emergence of mite infested

regions of the world where the Korean (K) haplotype is present,

Africanized worker bees.

infestation levels are higher than in other regions where the Japan / Thailand (J) haplotype is present (Delfinado-Baker, 1988). The variability among the effects caused by V. destructor infestation in different parts of the world seems also to be related to the bee

Materials and methods

subspecies and climatic conditions. For instance, bee subspecies

The study was carried out during the summer of 2007 in eight

clearly has an effect on the parasite development as African bees and

Africanized honey bee colonies in the experimental apiary of the

their hybrids are more tolerant to the mite than European bee races

Departamento de Ciências Naturais, Universidade Regional de

(De Jong et al., 1984; Moretto et al., 1991; Medina and Martin, 1999). Blumenau, state of Santa Catarina, Brazil. Since it is not possible to The tolerance of A. mellifera races to V. destructor seems to be

distinguish foundress female mites from their adult offspring at

related to the reproductive success of the mite female in worker

worker bee emergence, the first step of this study was to obtain

brood cells. The number of offspring per adult female mite

Africanized bee colonies with at least 90 % of worker brood cells

parasitizing worker brood cells is higher in European bees than in

invaded by a single female mite. This was estimated by determining

African bees and their hybrids (Camazine, 1986; Moretto et al., 1991). the number of adult female mites recorded in 17-18 day-old worker In South and Central America, fecundity of adult female mites is

brood. In these bee colonies with most worker brood cells invaded by

reduced on Africanized A. mellifera compared to that observed with

a single female mite, other emerging worker brood cells were again

mites on European A. mellifera in Europe (Rosenkranz and Engels,

analysed two days later in order to evaluate the number of

1994; Medina and Martin, 1999; Calderón et al., 2003). The

deutonymph and adult mites (foundress female and adult offspring).

reproductive ability of V. destructor female in worker brood cells also

Brood cells that were partially uncapped by the emerging bee, with

appears to be dependent on the season; female mites produce more

bee antennae seen poking out through the cell capping were manually

offspring during times of pollen production than at any other season

uncapped with forceps and the number of mites (adults and

of the year (Moretto et al., 1997).

deutonymphs) recorded.

Despite the introduction of V. destructor into Brazil over thirty

The average number of offspring generated by each adult female

years ago, low levels of infestation have generally been found, and

mite invading worker bee brood cells was thus estimated through the

unlike the experience in other regions in the world, the mite has not

expression: Y = Y2 – Y1, where: Y = average number of offspring

caused serious damage to apiculture. The low reproductive ability in

generated by each adult female mite; Y1 = average number of adult

worker brood cells has generally been considered as the main factor

female mites recorded in 17-18 day old worker brood cells; Y2 =

of tolerance of Africanized bees to the mite, but Garrido et al. (2003)

average number of adult mites (foundress and offspring) per brood

found a significant increase on the reproductive ability of female V.

cell at the moment when worker bees emerged.

destructor. These authors observed that the fertility rate of females in

Comparison of the number of deutonymphs and adult mites

worker brood cells of Africanized bee under the climatic conditions of

between those on 17-18 day old pupae and on emerging workers was

Ribeirão Preto, state of São Paulo was similar to that found in worker

determined by the t Student test. Differences in the percentage of

brood cells of European bees worldwide.

female mites without deutonymphs were analysed using the Chi-

Most of the results on the reproductive ability of female V.

square test.

destructor conducted so far were obtained by recording the number of mite offspring in worker brood at the pupal stage, which is characterized by dark eyes and recently pigmented body. At this


stage, all mite offspring can be differentiated from the foundress

A total of 406 adult female mites were found in the 392 worker brood

female mites. Offspring reaching the deutonymph phase by this bee

cells examined at the 17-18 day old stage. Fifteen cells (3.4 %) were

brood stage may reach adulthood before the worker bee emerges

excluded from the study because the foundress mites were dead.

giving an estimate of the effective reproduction rate. The number of

Among the remaining 377 cells infested with live mites, 363 (96.3 %)

Reproductive ability of Varroa destructor


and 14 (3.7 %) were infested with one and two adult varroa females,

who found 1.01 descendents per mite female on European honey

respectively, resulting in an average invasion rate of 1.04 mites per

bees from the United Kingdom.

infested cell. The average number of deutonymphs found in these

In this study, 30.8 % of female mites infesting Africanized worker

cells was 1.51 ± 0.45 per adult female mite. At least one deutonymph brood cells did not produce mature females. This value is less than was observed in 78 % of the brood cells analysed. Among the 250

half when compared to data from Africanized honey bee worker brood

brood cells infested with V. destructor and analysed at bee

cells from Costa Rica (Calderón et al., 2003). The discrepancy

emergence, an average of 2.11 ± 0.37 and 0.78 ± 0.39 adult mites

between these studies could be attributed to the fact that in the Costa

and deutonymphs were found, respectively. Thus, 58 % of the

Rica study the reproductive ability of female mites was analysed on

deutonymphs produced become adult mites. We found a statistically

worker broods about to emergence (19-20 day old brood) and some

significant (P < 0.0001) difference between the number of adult mites deutonymphs could still become adult individuals before worker bees on the two brood stages. With the emerging worker bees, each

emergence, whilst in our study we analysed the final number of

infested brood cell had on average 1.07 more adult females than with adults. the 17-18 day old brood. The number of deutonymphs found at bee

Female mites analysed from 17-18 day old worker brood in this

emergence was half that found for the 17-18 day old brood (t = 6.4;

study produced on average 1.51 deutonymphs, approximately twice

P< 0.0001).

the number found in other studies on Africanized bee colonies

In the 17-18 day old worker brood, no deutonymphs were

(Moretto et al., 1997; Correa-Marques et al., 2003). When the

recorded in 23.3 % of the cells analysed (females that effectively did

number of deutonymphs and adult offspring in emerging workers was

not contribute to reproduction). A single female mite was found in

considered, it was concluded that 58 % of the deutonymphs produced

30.8 % (n=77) of the cells of emerging bees analysed. However,

became adult mites before emergence.

among these cells infested with a single mite, 45 (18 % of the total number of infested cells) had no deutonymphs. No significant

Until the turn of the century, differences in the mite reproductive potential were considered to be the only factor responsible for

difference was found in the percentage of mites without deutonymphs different mite population sizes between Africanized and European between 17-18 day old brood and bee emergence (χ2 = 2.51;

bees (Martin and Medina, 2004). However, this has not been

P = 0.46).

corroborated at the climatic conditions of the Itajaí River Valley, state of Santa Catarina. The number of offspring obtained per adult female


mite in worker brood cells of Africanized honey bees found in this

This strategy allows a more realistic estimation of the reproductive

United Kingdom, although the infestation level of V. destructor in

success of V. destructor. Because of the difficulty of differentiating

Africanized bee colonies remains the same as in the past. According to

study was similar to that found for European honey bees from the

foundress mites from their adult offspring at the time of emergence of Garrido et al. (2003), the possible reason for the increase of the

A. mellifera worker brood, the reproductive success of female mites is reproductive rate of female mites in Africanized bees is the switch of generally estimated based on the number of deutonymphs found in worker brood bees at the final pupal phase (Camazine, 1986; Medina

the haplotype of V. destructor that recently occurred in Brazil. Despite similarities in the reproductive rate of the mite in the

and Martin, 1999; Mondragón et al., 2006). With our approach it was Africanized bees found in our study and in European bees studied possible to distinguish foundress mites from their offspring. As this

elsewhere (Correa-Marques et al., 2003), the infestation level of the

study was conducted with bee colonies where most of infested worker parasite in Africanized bee colonies remains low. For instance brood (96.7 %) was infested by a single female mite, all adult mites

infestation of adult bees in the Itajaí River Valley was approximately

found at worker bee emergence were considered as offspring, except

2 % (Carneiro et al., 2007). The size of the population of V.

for one adult, which would represent the foundress female. The reproductive success of female V. destructor based on the

destructor in A. mellifera bee colonies must therefore not depend exclusively on the reproductive success of females, and other factors

number of deutonymphs has revealed different reproductive rates

such as hygienic and grooming behaviour, must play an important

according to the honey bee race. In Africanized honey bee colonies,

role in the development of the pest population (Guerra et al., 2000;

the average number of offspring per adult mite female has generally

Mondragón et al., 2005).

been found to range from 0.6 to 0.8 per reproductive cycle, while in European honey bee colonies, each female generally produces approximately one adult offspring (Moretto et al., 1996; Medina and Martin, 1999). In this study, we found 1.07 adult offspring from each female mite on the emergence of Africanized honey bee workers. This rate of reproduction is similar to that found by Martin (1994),


Strapazzon, Koling, Carneiro, Ramirez, Guerra, Moretto


GUERRA, J C V Jr; GONÇALVES, L S; DE JONG D, (2000) Africanized honey bees (Apis mellifera L.) are more efficient at removing

The authors thanks Dr. Sidney Luiz Stürmer for his comments and

worker brood artificially infested with the parasitic mite Varroa

English revision and we would like to thank both referees for

jacobsoni Oudemans than are Italian bees or Italian / Africanized

important suggestions to improve the quality of this paper.

hybrids. Genetics and Molecular Biology 23(1): 89-92. MARTIN, S J (1994) Ontogenesis of the mite Varroa jacobsoni Oud.

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