Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera)

Experimental and Applied Acarology

Volumn 50, Issue 4, 2010, Pages 281-297

  Calderon R A ^a   van Veen, J W ^a   Sommeijer, M J ^b   Sanchez, L A ^a  

^a UNIVERSIDAD NACIONAL   (Costa Rica)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Africanized honey bees; Fertility; Reproductive ability; Resistance mechanisms; Tolerance; Varroa destructor; Viable offspring

Indexed keywords

ACARICIDE; APICULTURE; BROOD REARING; COLONY; FERTILITY; GENETIC VARIATION; HONEYBEE; HOST-PARASITE INTERACTION; LITERATURE REVIEW; MITE; PARASITE INFESTATION; PEST DAMAGE; POPULATION DYNAMICS; REPRODUCTIVE BIOLOGY; REPRODUCTIVE PRODUCTIVITY; RESISTANCE MANAGEMENT; TOLERANCE; TROPICAL ENVIRONMENT; WORKER CASTE;

BRAZIL; EUROPE; NORTH AMERICA;

ACARI; APIS MELLIFERA; APOIDEA; VARROA; VARROA DESTRUCTOR;

ANIMAL; BEE; BRAZIL; FEEDING BEHAVIOR; FEMALE; FERTILITY; GROOMING; MALE; PARASITOLOGY; PHYSIOLOGY; REPRODUCTION; REVIEW; SEXUAL BEHAVIOR; VARROIDAE;

ANIMALS; BEES; BRAZIL; FEEDING BEHAVIOR; FEMALE; FERTILITY; GROOMING; MALE; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; VARROIDAE;

EID: 77950690164     PISSN: 01688162     EISSN: 15729702     Source Type: Journal    
DOI: 10.1007/s10493-009-9325-4     Document Type: Review

References (125)

1. Anderson DL, Fuchs S (1998) Two genetically distinct populations of Varroa jacobsoni with contrasting reproductive abilities on Apis mellifera. J Apic Res 37: 69-78.
2. Anderson DL, Trueman JWH (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 24: 165-189.
3. Arechavaleta-Velasco M, Guzman-Novoa E (2001) Relative effect of four characteristics that restrain the population growth of the mite Varroa destructor in honey bee (Apis mellifera) colonies. Apidologie 32: 157-174.
4. Bailey L, Ball BV (1991) Honey bee pathology, Second edn. Academic Press, London, UK, p 193.
5. Ball BV (1985) Acute paralysis virus isolates from honeybee colonies infested with Varroa jacobsoni. J Apic Res 24: 115-119.
6. Ball BV (1993) The damaging effects of Varroa jacobsoni infestation. In: Proceedings of an IBRA symposium. UK, pp 9-16.
7. Ball BV (1996) Honey bee viruses: a cause for concern. Bee World 77: 117-119.
8. Beetsma J, Zonneveld K (1992) Observations on the initiation and stimulation of oviposition of the varroa mite. Exp Appl Acarol 16: 303-312.
9. Beetsma J, Vries de B, Emani M, Emani V (1989) Effects of Varroa jacobsoni Oud. on colony development, worker bee weight and longevity and brood mortality. In: Cavalloro R (ed) Present status of Varroatosis in Europe and progress in the varroa mite control. Commission of the European communities, Luxemburg, pp 163-170.
10. Beetsma J, Boot W, Calis J (1999) Invasion behavior of Varroa jacobsoni Oud. from bees into brood cells. Apidologie 30: 125-140.
11. Boecking O, Ritter W (1993) Grooming and removal behaviour of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. J Apic Res 32: 127-134.
12. Boecking O, Spivak M (1999) Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 30: 141-158.
13. Boot W (1994) Methyl palmitate does not elicit invasion of honeybee brood cells by varroa mites. Exp Appl Acarol 18: 587-592.
14. Boot W, Calis J, Beetsma J (1991) Invasion of varroa mites into honeybee brood cells; when do brood cells attract varroa mites? In: Proceedings experimental and apply entomology, N. E. V. Amsterdam, pp 154-156.
15. Boot W, Calis J, Beetsma J (1992) Differential periods of varroa mite invasion into worker and drone cells of honey bees. Exp Appl Acarol 16: 295-301.
16. Boot W, Calis J, Beetsma J (1993) Invasion of Varroa jacobsoni into honey bee brood cells: a matter of chance or choice? J Apic Res 32: 167-174.
17. Boot W, van Baalen M, Sabelis M (1995) Why do varroa mites invade worker brood cells of the honey bee despite lower reproductive success? Behav Ecol Sociobiol 36: 283-289.
18. Boot W, Tan NQ, Dien PC, Huan LV, Dung NV, Long LT, Beetsma J (1997) Reproductive success of Varroa jacobsoni in brood of its original host, Apis cerana, in comparison to that of its new host, Apis mellifera (Hymenoptera: Apidae). Bull Entomol Res 87: 119-126.
19. Boot W, Calis J, Beetsma J, Hai DM, Lan NK, Toan TV, Trung LQ, Minh NH (1999) Natural selection of Varroa jacobsoni explains the different reproductive strategies in colonies of Apis cerana and Apis mellifera. Exp Appl Acarol 23: 133-144.
20. Bowen-Walker PL, Martin SJ, Gunn A (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 73: 101-106.
21. Büchler R (1994) Varroa tolerance in honey bees-occurrence, characters and breeding. Bee World 75: 54-70.
22. Büchler R, Drescher W (1990) Variance and hereditability of the capped developmental stage in European Apis mellifera L and its correlation with increased Varroa jacobsoni Oud. infestation. J Apic Res 29: 172-176.
23. Calderón RA, van Veen JW (2008) Varroa destructor (Mesostigmata: Varroidae) in Costa Rica: population dynamics and its influence on the colony condition of Africanized honey bees (Hymenoptera: Apidae). Int J Trop Biol Conserv 56: 1741-1747.
24. Calderón RA, van Veen JW, Arce HG, Esquivel ME (2003a) Presence of deformed wing virus and Kashmir bee virus in Africanized honey bee colonies in Costa Rica infested with Varroa destructor. Bee World 84: 112-116.
25. Calderón RA, Sommeijer MJ, De Ruijter A, van Veen JW (2003b) The reproductive ability of Varroa destructor in worker brood of Africanized and hybrid honey bees in Costa Rica. J Apic Res 42: 65-67.
26. Calderón RA, Zamora LG, van Veen JW, Quesada MV (2007) A comparison of the reproductive ability of Varroa destructor (Mesostigmata: Varroidae) in worker and drone brood of Africanized honey bees (Apis mellifera). Exp Appl Acarol 43: 25-32.
27. Calderón RA, Fallas N, Zamora LG, van Veen JW, Sanchez LA (2009) Behavior of varroa mites in worker brood cells of Africanized honey bees. Exp Appl Acarol. doi: 10. 1007/s10493-009-9266-y.
28. Calderone NW, Kuenen LP (2001) Effect of western honey bee, Apis mellifera L. (Hymenoptera: Apidae), colony, cell type and larval sex on host acquisition by female Varroa destructor (Acari: Varroidae). J Econ Entomol 94: 1022-1030.
29. Calderone NW, Kuenen LP (2003) Differential tending behavior by nurse bees towards worker and drone larvae of the honey bee, Apis mellifera, during the 60 hours prior to capping. Apidologie 34: 543-552.
30. Calderone NW, Lin S (2001) Behavioural responses of Varroa destructor (Acari: Varroidae) to extracts of larvae, cocoons and brood food of worker and drone honey bees, Apis mellifera (Hymentoptera: Apidae). Physiol Entomol 26: 241-350.
31. Calis J, Fries I, Ryrie SC (1999) Population modeling of Varroa jacobsoni Oud. Apidologie 30: 111-124.
32. Camazine S (1986) Differential reproduction of the mite, Varroa jacobsoni (Mesostigmata: Varroidae), on Africanized and European honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 79: 801-803.
33. Camazine S (1988) Factors affecting the severity of Varroa jacobsoni infestations on European and Africanized honey bees. In: Needham R, Page R, Delfinado-Baker M, Bowman C (eds), Africanized honey bees and bee mites. pp 445-451.
34. Carneiro F, Torres R, Strapazzon R, Ramirez S, Guerra J, Koling D, Moretto G (2007) Changes in the reproductive ability of the mite Varroa destructor (Anderson and Trueman) in Africanized honey bees (Apis mellifera L.) (Hymenoptera: Apidae) colonies in Southern Brazil. Neotrop Entomol 36: 949-952.
35. Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res 70: 33-80.
36. Chen YP, Pettis J, Collins A, Feldlaufer MF (2006) Prevalence and transmission of honey bee viruses. Appl Environ Microbiol 72: 606-611.
37. Correa-Marquez MA, Medina L, Martin S, De Jong D (2003) Comparing data on the reproduction of Varroa destructor. Genet Mol Res 2: 1-6.
38. De Guzman L, Rinderer TE, Frake A (2007) Growth of Varroa destructor populations in Russian honey bee (Hymenoptera: Apidae) colonies. Ann Entomol Soc Am 100: 187-195.
39. De Jong D (1984) Current knowledge and open questions concerning reproduction in the honey bee mite Varroa jacobsoni. In: Engels W (ed), Advances in invertebrate reproduction. Elsevier, Amsterdam, 125 pp.
40. De Jong D (1997) Varroa and other parasites of brood. In: Morse R, Flottum K (eds) Honey bee pest, predators, and diseases, Third edn. A. I. Root Company, Ohio, USA, pp 280-327.
41. De Jong D, Morse RA (1988) Utilization of raised brood cells of the honey bee, Apis mellifera (Hymenoptera: Apidae), by the mite, Varroa jacobsoni (Acarina: Varroidae). Entomol Gen 14: 103-106.
42. De Jong D, De Jong PH, Goncalves LS (1982a) Weight loss and other damage to developing worker honey bees (Apis mellifera) due to infestation with Varroa jacobsoni. J Apic Res 20: 254-257.
43. De Jong D, Morse R, Eickwort G (1982b) Mite pests of honey bees. Annu Rev Entomol 27: 229-252.
44. De Jong D, Goncalves LS, Morse RA (1984) Dependence on climate of the virulence of Varroa jacobsoni. Bee World 65: 117-121.
45. de Ruijter A (1987) Reproduction of Varroa jacobsoni during successive brood cycles of the honeybee. Apidologie 18: 321-326.
46. de Ruijter A, Calis J (1988) Distribution of Varroa jacobsoni female mites in honey bee worker brood cells of normal and manipulated depth (Acarina: Varroidae). Entomol Gen 14: 107-109.
47. Donzé G, Guerin P (1994) Behavioral attributes and parental care of varroa mites parasiting honeybee brood. Behav Ecol Sociobiol 34: 305-319.
48. Donzé G, Guerin P (1997) Time-activity budgets and spacing structure by the different life stages of Varroa jacobsoni in capped brood of the honey bee, Apis mellifera. J Insect Behav 10: 371-393.
49. Eischen F (1997) Hygienic behavior and varroa. Am Bee J 137: 574-575.
50. Evans JD, Pettis J (2005) Colony-level effects of immune responsiveness in honey bees, Apis mellifera. Evolution 59: 2270-2274.
51. Evans JD, Aronstein K, Chen YP, Hetru C, Imler J, Jiang H, Kanost M, Thompson G, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15: 645-656.
52. Fries I, Huazhen W, Wei S, Chen SJ (1996) Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana and Apis mellifera ligustica. Apidologie 27: 3-11.
53. Fuchs S (1992) Choice in Varroa jacobsoni Oud. between honey bee drone or worker brood cells for reproduction. Behav Ecol Sociobiol 31: 429-435.
54. Garrido C, Rosenkranz P, Stürmer M, Rübsam R, Büning J (2000) Toluidine blue staining as a rapid measure for initiation of oocyte growth and fertility in Varroa jacobsoni Oud. Apidologie 31: 559-566.
55. Garrido C, Rosenkranz P, Paxton RJ, Goncalves LS (2003) Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34: 535-541.
56. Ghandi A, Hoopingarner R (2003) Reproductive biology of Varroa jacobsoni Oud. in worker and drone brood of the honey bee Apis mellifera L. under Michigan conditions. Pak J Biol Sci 6: 756-761.
57. Goetz B, Koeninger N (1992) Structural features trigger capping of brood cells in honey bees. Apidologie 23: 211-216.
58. Goetz B, Koeninger N (1993) The distance between larva and cell opening triggers brood cell invasion by Varroa jacobsoni. Apidologie 24: 67-72.
59. Grandi-Hoffman G, Page R, Martin J, Fondrk K (2002) Can the frequency of reduced Varroa destructor fecundity in honey bee (Apis mellifera) pupae be increased by selection? Apidologie 33: 563-570.
60. Guzman-Novoa E, Sanchez AA, Page RE, Garcia PT (1996) Susceptibility of European and Africanized honeybees (Apis mellifera L.) and their hybrids to Varroa jacobsoni Oud. Apidologie 27: 93-103.
61. Guzman-Novoa E, Vandame R, Arechavaleta M (1999) Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico. Apidologie 30: 173-182.
62. Hänel H (1986) Effect of juvenile hormone (III) from the host Apis mellifera (Insecta: Hymenoptera) on the neurosecretion of the parasitic mite Varroa jacobsoni (Acari: Mesostigmata). Exp Appl Acarol 2: 257-271.
63. Hänel H, Koeniger N (1986) Possible regulation of the reproduction of the honey bee mite Varroa jacobsoni (Mesostigmata: Acari) by a host's hormone: juvenile hormone III. J Insect Physiol 32: 791-798.
64. Harbo JR, Harris JW (2005) Suppressed mite reproduction explained by the behaviour of adult bees. J Apic Res 44: 21-23.
65. Harbo JR, Hoopingarner RA (1997) Honey bees (Hymenoptera: Apidae) in the United States that express resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol 90: 893-898.
66. Harris JW, Harbo JR (2000) Changes in reproduction of Varroa destructor after honey bee queens were exchanged between resistant and susceptible colonies. Apidologie 31: 689-699.
67. Hung AC, Adams JR, Shimanuki H (1995) Bee parasitic mite syndrome (II): the role of varroa mite and viruses. Am Bee J 135: 702-704.
68. Ibrahim A, Reuter G, Spivak M (2003) Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie 38: 67-76.
69. Ifantidis MD (1988) Some aspects of the process of Varroa jacobsoni entrance into honey bee (Apis mellifera) brood cells. Apidologie 19: 387-396.
70. Korpela S, Aarthus A, Fries I, Hansen H (1993) Varroa jacobsoni Oud. in cold climates: population growth, winter mortality and influence on survival of honey bee colonies. J Apic Res 31: 157-164.
71. Kraus B (1994) Factors influencing host choice of the honey bee parasite Varroa jacobsoni Oud. Exp Appl Acarol 18: 435-443.
72. Kuenen LP, Calderone NW (1997) Transfers of varroa mites from newly emerged bees: preferences for age- and function-specific adult bees. J Insect Behav 10: 213-228.
73. Kuenen LP, Calderone NW (2000) Varroa mite infestations in elevated honey bee brood cells: effects of context and caste. J Insect Behav 13: 201-215.
74. Le Conte Y, Arnold G, Trouiller J, Masson C, Chappe B, Ourisson G (1989) Attraction of the parasitic mite varroa to the drone larvae of honey bees by simple aliphatic esters. Science 245: 638-639.
75. Martin SJ (1994) Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Exp Appl Acarol 18: 87-100.
76. Martin SJ (2001a) The role of varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38: 1082-1093.
77. Martin SJ (2001b) Biology and life history of varroa mites. In: Webster TC, Delaplane KS (eds) Mites of the honey bee. Dadant publication, USA, pp 131-148.
78. Martin SJ, Kemp D (1997) Average number of reproductive cycles performed by Varroa jacobsoni in honey bees (Apis mellifera) colonies. J Apic Res 36: 113-123.
79. Martin SJ, Medina L (2004) Africanized honeybees have unique tolerance to varroa mites. Trends Parasitol 20: 112-114.
80. Martin SJ, Holland K, Murray M (1997) Non-reproduction in the honeybee mite Varroa jacobsoni. Exp Appl Acarol 21: 539-549.
81. Medina L, Martin SJ (1999) A comparative study of Varroa jacobsoni reproduction in worker cells of honey bees (Apis mellifera) in England and Africanized bees in Yucatan, Mexico. Exp Appl Acarol 23: 659-667.
82. Medina L, Martin SJ, Espinosa LM, Ratnieks LF (2002) Reproduction of Varroa destructor in worker brood of Africanized honey bees (Apis mellifera). Exp Appl Acarol 27: 79-88.
83. Message D, Goncalves L (1995) Effect of the size of worker brood cells of Africanized honey bees on infestation and reproduction of the ectoparasite Varroa jacobsoni Oud. Apidologie 26: 381-386.
84. Milani N, Vedova G, Nazzi F (2004) (Z)-8-Heptadecene reduces the reproduction of Varroa destructor in brood cells. Apidologie 35: 265-273.
85. Mobus B, Bruyn C (1993) The new varroa handbook. Arc & Throstle Press, Todmorden, Scotland, p 160.
86. Mondragon L, Spivak M, Vandame R (2005) A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico. Apidologie 36: 345-358.
87. Mondragon L, Martin SJ, Vandame R (2006) Mortality of mite offspring: a major component of Varroa destructor resistance in a population of Africanized bees. Apidologie 37: 67-74.
88. Moretto G (1997) Defense of Africanized bee workers against the mite Varroa jacobsoni in Southern Brazil. Am Bee J 137: 746-747.
89. Moretto G, Leonidas J (2001) Infestation and distribution of the mite Varroa jacobsoni in Africanized honey bees (Apis mellifera) colonies. Interciencia 26: 393-396.
90. Moretto G, Leonidas J (2003) Infestation and distribution of the mite Varroa destructor in colonies of Africanized bees. Braz J Biol 63: 83-86.
91. Moretto G, Mello JL (1999) Varroa jacobsoni infestation of adult Africanized and Italian bees (Apis mellifera) in mixed colonies in Brazil. Genet Mol Biol 22: 321-323.
92. Moretto G, Goncalves L, De Jong D (1991) Africanized bees are more efficient at removing Varroa jacobsoni, preliminary data. Am Bee J 131: 434.
93. Moretto G, Pillati A, De Jong D, Goncalves L, Cassini F (1995) Reduction of varroa infestations in the state of Santa Catarina, in Southern Brazil. Am Bee J 135: 498-500.
94. Morse R, Goncalves L (1979) Varroa disease a threat to world beekeeping. Bee Cult 107: 179-181.
95. Oldroyd BP (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends Evol Ecol 14: 312-315.
96. Peng YS, Fang Y, Xu S, Ge L (1987) The resistance mechanism of the Asian honey bee Apis cerana Fabr. to an ectoparasitic mite, Varroa jacobsoni Oudemans. J Invertebr Pathol 49: 54-60.
97. Piccirillo G, De Jong D (2003) The influence of brood comb cell size on the reproductive behavior of the ectoparasitic mite Varroa destructor in Africanized honey bee colonies. Genet Mol Res 2: 36-42.
98. Rath W (1993) Aspects of pre-adaptation in Varroa jacobsoni while shifting from its original host Apis cerana to Apis mellifera. In: Conner L, Rinderer T, Sylvester H (eds) Asian apiculture. Wicwas Press, Cheshire, pp 417-426.
99. Rath W, Drescher W (1990) Response of Apis cerana Fabr. colonies toward brood infested with Varroa jacobsoni Oud. and infestation rate of colonies in Thailand. Apidologie 21: 311-321.
100. Rehm S, Ritter W (1989) Sequence of the sexes in the offspring of Varroa jacobsoni and the resulting consequences for the calculation of the development period. Apidologie 20: 339-343.
101. Rickli M, Guerin PM, Diehl PA (1992) Palmitic acid released from honeybee worker larvae attracts the parasitic mite Varroa jacobsoni on a servosphere. Naturwissenschaften 79: 320-322.
102. Rickli M, Diehl PA, Guerin PM (1994) Cuticle alkanes of honeybee larvae mediate arrestment of bee parasite Varroa jacobsoni. J Chem Ecol 20: 2437-2453.
103. Ritter W, De Jong D (1984) Reproduction of Varroa jacobsoni O. in Europe, the middle East and tropical South America. Zeitschrift fur Angewandte Entomologie 98: 55-57.
104. Rosenkranz P (1990) Host factors in the control of the reproduction of the parasitic bee mite Varroa jacobsoni in colonies of Apis mellifera. PhD Thesis, Tübingen, Germany, 149 pp.
105. Rosenkranz P (1999) Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30: 159-172.
106. Rosenkranz P, Rachinsky P, Strambi A, Strambi C, Ropstorf P (1990) Juvenile hormone titer in capped worker brood of Apis mellifera and reproduction in the bee mite Varroa jacobsoni. Gen Comp Endocrinol 78: 189-193.
107. Rosenkranz P, Tewarson NC, Rachinsky A, Strambi A, Strambi C, Engels W (1993) Juvenile hormone titer and reproduction of Varroa jacobsoni in capped brood stages of Apis cerana indica in comparison to Apis mellifera ligustica. Apidologie 24: 375-382.
108. Ruttner F (1977) Report on the cause of varroa infection. Die Biene 13: 353-354.
109. Ruttner F, Marx H, Marx G (1984) Observations about a possible adaptation of Varroa jacobsoni to Apis mellifera L. in Uruguay. Apidologie 15: 43-62.
110. Sammataro D (1996) Mechanisms of bee resistance/tolerance to varroa mites. Am Bee J 136: 567-568.
111. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 45: 519-548.
112. Shimanuki H, Calderone NW, Knox DA (1994) Parasitic mite syndrome: the symptoms. Am Bee J 134: 827-828.
113. Spivak M (1996) Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie 27: 245-260.
114. Spivak M, Gilliam M (1998) Hygienic behavior of honey bees and its application for control of brood diseases and varroa. Bee World 79: 169-186.
115. Spivak M, Reuter GS (1998) Performance of hygienic colonies in a commercial apiary. Apidologie 29: 285-296.
116. Sumpter DJ, Martin SJ (2004) The dynamics of virus epidemics in varroa-infested honey bee colonies. J Anim Ecol 73: 51-63.
117. Szabo T, Walker T, Mueller A (1996) Grooming behavior as a varroa resistance characteristic in honey bee colonies. Am Bee J 136: 515-517.
118. Tewarson N, Singh A, Engels W (1992) Reproduction of Varroa jacobsoni in colonies of Apis cerana indica under natural and experimental conditions. Apidologie 23: 161-171.
119. Trouiller J, Arnold G, Le Conte Y, Masson C (1991) Temporal pheromonal and kairomonal secretion in the broods of honeybees. Naturwissenshaften 78: 368-370.
120. Trouiller J, Arnold G, Chappe B, Le Conte Y, Mason C (1992) Semiochemical basis of infestation of honey bee brood by Varroa jacobsoni. J Chem Ecol 18: 2041-2053.
121. Trouiller J, Arnold G, Chappe B, Le Conte Y, Billion A, Mason C (1994) The kairomonal esters attractive to the Varroa jacobsoni mite in the queen brood. Apidologie 25: 314-321.
122. Vandame R, Colin ME, Otero-Colina G (1999) Africanized honeybees tolerance to varroa in Mexico: mite infertility is not the main tolerance factor. Apiacta 34: 1-5.
123. Vandame R, Colin ME, Morand S, Otero-Colina G (2000) Levels of compatibility in a new host-parasite association: Apis mellifera/Varroa jacobsoni. Can J Zool 78: 2037-2044.
124. Vandame R, Morand S, Colin ME, Belzunces LP (2002) Parasitism in the social bee Apis mellifera: quantifying costs and benefits of behavioural resistance to varroa mites. Apidologie 33: 433-455.
125. Webster TC (2001) Methods for detection of Varroa jacobsoni in honey bee colonies. In: Webster TC, Delaplane KS (eds) Mites of the honey bee. Dadant and Sons, Hamilton, IL.