Relationship Between Hygienic Behavior and Varroa destructor Mites in Colonies Producing Honey or Royal Jelly


  • Maria Claudia Colla Ruvolo-Takasusuki Universidade Estadual de Maringá Departamento de Biotecnologia Genética e Biologia Celular
  • Vagner Alencar Toledo Universidade Estadual de Maringá
  • Denise Alves Lopes Universidade Estadual de Maringá



bee breeding, heritability, genetic correlation, phenotypic correlation, Bayesian inference


Genetic and phenotypic parameters for hygienic behavior, invasion and infestation rates, total and effective reproduction of Varroa destructor in Africanized honeybee colonies producing honey (20 hives) or royal jelly (30 mini-hives) were analyzed. The significance of monthly fixed effects, type of product (honey and royal jelly) and their interactions were verified through generalized linear model procedures. Software WinBugs (Bayesian Inference Using Gibbs Sampling) with Bayesian inference was employed for (co)variance estimates. The average values for colonies producing honey or royal jelly were 74.38 and 71.40% for hygienic behavior in 24 hours; infestation rates 8.30 and 11.40%; invasion rates 9.50 and 7.50%; total reproduction 1.02 and 0.55%; effective reproduction was 0.62 and 0.33%, respectively. The additive genetic variance for invasion (0.16), total reproduction (0.25) and effective reproduction (0.94) rates of the mite were higher than estimates for hygienic behavior in 24 hours (0.05) and infestation rate (0.04). Mean heritability for hygienic behavior, infestation and invasion rates, total and effective reproduction of the mite were .58, 0.54, 0.56, 0.63 and 0.61, respectively. The genetic correlation of -0.48 for hygienic behavior with total reproduction rate of Varroa destructor shows that hygienic behavior may be the most interesting trait for selection. Besides a heritability of high magnitude, when combined with the total reproduction rate of the mite, it has a high and antagonistic correlation. Consequently, in cases of high infestation of Varroa destructor, the selection for hygienic behavior would decrease the reproduction rate of the mite.


Download data is not yet available.

Author Biography

Maria Claudia Colla Ruvolo-Takasusuki, Universidade Estadual de Maringá Departamento de Biotecnologia Genética e Biologia Celular

Associate professor at the State University of Maringa, Department of Biotechnology, Genetics and Cell Biology.
Develop research in Population genetics of social insects (bees), gene expression in bees and pollination.


Arathi, H.S., I. Burns & M. Spivak 2000. Ethology of hygienic behaviour in honey bee Apis

mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology


Bienefeld, K., K. Ehrhardt & F. Reinhardt 2007. Genetic evaluation in the honey bee

considering queen and worker effects – A BLUP- Animal Model approach. Apidologie


Boecking, O. & W. Ritter 1993. Grooming and removal behaviour of Apis mellifera in Tunisia

against Varroa jacobsoni. Journal of Apicultural Research 32:127-134.

Boecking, O., K. Bienefeld & W. Drescher 2000. Heritability of the varroa-specific hygienic

behavior in honey bees (Hymenoptera: Apidae). Journal Animal Breeding and Genetics


Calderon, R.A., J.W. Van Veen, M.J. Sommeijer & L.A. Sanchez 2010. Reproductive biology

of Varroa destructor in Africanized honey bees (Apis mellifera). Experimental and Applied

Acarology 50:281-297.

Carneiro, F.E., R.R. Torres, R. Strapazzon, S.A. Ramirez, J.C. Jr. Guerra, D.F. Koling & G.

Moretto 2007. Changes in the reproductive ability of the mite Varroa destructor (Anderson

& Trueman) in Africanized honey bees (Apis mellifera L.) colonies in southern Brazil.

Neotropical Entomology 36:949-952.

Costa-Maia, F.M. Aspectos geneticos da producao de mel e comportamento higienico em

abelhas Apis mellifera africanizadas. 2009. 77f. Thesis (PhD in Animal Science) - UEM,

Universidade Estadual de Maringa, Maringa.

De Jong, D. & L.S. Goncalves 1981. The Varroa problem in Brazil. American Bee Journal


Doolittle, G.M. 1889. Scientific queen-rearing as practically applied. Chicago: Illinois,


Falconer, D.S. 1987. Introducao a genetica quantitativa. Vicosa, MG: UFV, 279p.

Geweke, J. 1992. Evaluating the accuracy of sampling-based approaches to the calculation

of posterior moments. Bayesian Stat 4:625-631.

Gilliam, M., S. Taber & G.V. Richardson, 1983. Hygienic behavior of honey bees in relation

to chalkbrood disease. Apidologie 14:29-39.

Gramacho, K.P. Estudo do comportamento higienico em Apis mellifera, como subsidio a

programas de selecao e melhoramento genetico em abelhas. 1995. 103f. Dissertation

(Master’s degree in entomology). Faculdade de Filosofia, Ciencias e Letras de Ribeirao

Preto, Ribeirao Preto.

Harbo, J.R. & J.W. Harris 1999. Heritability in honey bees (Hymenoptera: Apidae) of

characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae).

Journal of Economic Entomology 92:262-265.

Heidelberger, P. & P. Welch 1983. Simulation run length control in the presence of an initial

transient. Operations Research 31:1109-1144.

Junkes, L., J.C.V. Guerra Jr. & G. Moretto 2007. Varroa destructor mite mortality rate according

to the amount of worker broods in Africanized honey bee (Apis mellifera L.) colonies.

Acta Scientiarum Animal Science 29:305-308.

Lee K.V., R.D. Moon, E.C. Burkness, W.D. Hutchison & J. Spivak 2010. Practical Sampling

Plans for Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae)

Colonies and Apiaries. Journal of Economic Entomology 103:1039-1050.

Message, D. 2006. Devemos utilizar produtos quimioterapicos para controlar doencas

e parasitoses das abelhas africanizadas? In: Nogueira-Couto, R.H. & L.A. Couto.

Apicultura: manejo e produtos. Jaboticabal: Funep, p.147-156.

Momot, J.P. & W.C. Rothenbuhler 1971. Behaviour genetics of nest cleaning in honeybees

VI. Interactions of age and genotype of bees, and nectar flow. Journal of Apicultural

Research 10:11-21.

Moretto, G., L.S. Goncalves & D. De Jong 1993. Heritability of Africanized and European

honey bee defensive behavior against the mite Varroa jacobsoni. Revista Brasileira de

Genetica 16:71-76.

Moretto, G., L.S. Goncalves, D. De Jong & M.Z. Bichuette 1991. The effects of climate and

bee race on Varroa jacobsoni Oud. infestation in Brazil, Apidologie 22:197-203.

Moretto, G. & L.J. Mello 2001. Infestation and distribution of the mite Varroa jacobsoni in

Africanized honey bee (Apis mellifera) colonies. Interciencia 26:394-396.

Morse, R.A. & L.S. Goncalves 1979. Varroa disease, a threat to world beekeeping. Bee

Culture 107:179-181.

Newton, D.C., G.C. Cantowell & E.P. Bourquin 1975. Removal of freeze-killed brood as

an index of nest cleaning behavior in honeybee colonies (Apis mellifera L.). American

Bee Journal 115:388-406.

Nogueira-Couto, R.H. Producao de alimento e cria de colmeias de Apis mellifera infestadas

com Varroa jacobsoni, em regioes canavieiras. 1991. 131f. Thesis (Livre Docencia

em Apicultura) - Universidade Estadual Paulista, Faculdade de Ciencias Agrarias e

Veterinarias, Jaboticabal.

R Development Core Team. 2009. R: A language and environment for statistical computing.

R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL

Rinderer, T.E. 1977. A new approach to honey bee breeding at the Baton Rouge USDA,

Laboratory. American Bee Journal 117:146-147.

Rothenbuhler, W.C. 1964. Behavior genetics of nest cleaning in honey bees IV. Responses of F1

and backcross generations to disease-killed brood. American Zoologist 4:111-123.

Spiegelhalter, D.J., A.P. Dawid, S.L. Lauritzen & R.G. Cowell 1993. Bayesian analysis in

expert systems. Statistical Sciences 8:219-283.

Spivak, M. & D.L. Downey 1998. Field assays for hygienic behavior in honey bees

(Hymenoptera: Apidae). Journal of Economic Entomology 91(1):64-70.

Spivak, M. & M. Gilliam 1993. Facultative expression of hygienic behavior of honey bees

in relation to disease resistance. Journal of Apicultural Research 32:147-157.

Stort, A.C., L.S. Goncalves, O. Malaspina & F.A. Moura Duarte 1981. Study on sineacar

effectiveness in controlling Varroa jacobsoni. Apidologie 12:289-297.

Taber, S. 1982. Bee behavior: Breeding for disease resistance. American Bee Journal 122:823-

Terada, Y., C.A. Garofalo & S.F. Sakagami 1975. Age-survival curves for workers of two

eusocial bees (Apis mellifera and Plebeia droryana) in a subtropical climate, with notes

on worker polytheism in P. droryana. Journal of Apicultural Research 14:161-170.

Toledo, V.A.A. & G.F. Mouro 2005. Producao de geleia real com abelhas africanizadas

selecionadas carnicas e hibridas. Revista Brasileira de Zootecnia 34:2085-2092.

Toledo, V.A.A. & R.H. Nogueira-Couto 1996. Infestacao de colonias hibridas de abelhas

Apis mellifera pelo acaro Varroa jacobsoni. ARS Veterinaria 12:104-112.

Winston, M.L. The biology of the honey bee. London: Harvard University, 1987. 281p.

Winston, M.L. & S.J. Katz 1981. Longevity of cross-fostered honey bee workers (Apis mellifera)

of European and Africanized races. Canadian Journal of Zoology 59:1571-1574.

Winston, M.L., O.R. Taylor & G.W. Otis 1983. Some differences between temperate and

tropical African and South American honeybees. Bee World 64:12-21.




How to Cite

Ruvolo-Takasusuki, M. C. C., Toledo, V. A., & Lopes, D. A. (2014). Relationship Between Hygienic Behavior and Varroa destructor Mites in Colonies Producing Honey or Royal Jelly. Sociobiology, 59(1), 251–274.




Most read articles by the same author(s)