Impact of Varroa destructor on honeybee (Apis mellifera scutellata) colony development in South Africa

Experimental and Applied Acarology

Volumn 65, Issue 1, 2015, Pages 89-106

  Strauss, Ursula ^a   Pirk, Christian W W ^a   Crewe, Robin M ^a   Human, Hannelie ^a   Dietemann, Vincent ^a,b  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

Author keywords

Apis mellifera scutellata; Honeybee; Infestation; Mite; Tolerance; Varroa destructor

Indexed keywords

ACARI; APIS MELLIFERA; APIS MELLIFERA SCUTELLATA; VARROA; VARROA DESTRUCTOR;

ACARICIDE;

ANIMAL; BEE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; PARASITOLOGY; PHYSIOLOGY; SEASON; SOUTH AFRICA; TIME; VARROIDAE;

ACARICIDES; ANIMALS; BEES; SEASONS; SOUTH AFRICA; TIME FACTORS; VARROIDAE;

EID: 84916939044     PISSN: 01688162     EISSN: 15729702     Source Type: Journal    
DOI: 10.1007/s10493-014-9842-7     Document Type: Article

References (77)

1. Allsopp M (2006) Analysis of Varroa destructor infestation of southern African honeybee populations. M.Sc. thesis, University of Pretoria
2. Berthoud H, Imdorf A, Haueter M, Radloff SE, Neumann P (2010) Virus infections and winter losses of honey bee colonies (Apis mellifera). J Apic Res 49:60–65
3. Boecking O, Ritter W (1993) Grooming and removal behaviour of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. J Apic Res 32:127–134
4. Branco MR, Kidd NAC, Pickard RS (2006) A comparative evaluation of sampling methods for Varroadestructor (Acari: Varroidae) population estimation. Apidologie 37:452–461
5. Büchler R, Drescher W, Tornier I (1992) Grooming behaviour of Apis cerana, Apis mellifera and Apis dorsata and its effect on the parasitic mites Varroa jacobsoni and Tropilaelaps clareae. Exp Appl Acarol 16:313–319
6. Calatayud F, Verdú MJ (1994) Survival of the mite Varroa jacobsoni Oud. (Mesostigmata: Varroidae) in broodless colonies of the honey bee Apis mellifera L. (Hymenoptera: Apidae). Exp Appl Acarol 18:603–612
7. Calderón RA, van Veen JW, Sommeijer MJ, Sanchez LA (2010) Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp Appl Acarol 50:281–297
8. 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
9. Camazine S, Morse RA (1988) The Africanized honeybee: the epithet “killer bee” is undeserved. Am Sci 76:464–471
10. Carneiro FE, Torres RR, Strapazzon R, Ramirez SA, Guerra JCV, Koling DF, 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
11. Corrêa-Marques MH, De Jong D (1998) Uncapping of worker bee brood, a component of the hygienic behaviour of Africanized honey bees against the mite Varroa jacobsoni Oud. Apidologie 29:283–289
12. Corrêa-Marques MH, Medina ML, Martin SJ, De Jong D (2003) Comparing data on the reproduction of Varroa destructor. Genet Mol Res 2:1–6
13. De Jong D (1988) Varroa jacobsoni does reproduce in worker cells of Apis cerana in South Korea. Apidologie 19:241–244
14. De Jong D, Soares AEE (1997) An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. Am Bee J 137:742–747
15. De Jong D, Goncalves LS, Morse RA (1984) Dependence on climate of the virulence of Varroa jacobsoni. Bee World 65:117–121
16. Delaplane, KS, van der Steen J, Guzman-Novoa E (2013) Standard methods for estimating strength parameters of Apis mellifera colonies. In: Dietemann V, Ellis JD, Neumann P (eds) The COLOSS BEEBOOK, volume I: standard methods for Apis mellifera research. J Apic Res 52(1). doi:10.3896/IBRA.1.52.1.03
17. Dietemann V, Pflugfelder J, Anderson D, Charrière J-D, Chejanovsky N, Dainat B, de Miranda JR, Delaplane K, Dillier F-X, Fuchs S, Gallmann P, Gauthier L, Imdorf A, Koeniger N, Kralj J, Meikle W, Pettis JS, Rosenkranz P, Sammataro D, Smith D, Yañez O, Neumann P (2012) Varroa destructor: research avenues towards sustainable control. J Apic Res 51:125–132
18. Dietemann V, Nazzi F, Martin SJ, Anderson D, Locke B, Delaplane KS, Wauquiez Q, Tannahill C, Frey E, Ziegelmann B, Rosenkranz P, Ellis JD (2013) Standard methods for varroa research. In: Dietemann V, Ellis JD, Neumann P (eds) The COLOSS BEEBOOK, volume II: standard methods for Apis mellifera pest and pathogen research. J Apic Res 52(1). doi:10.3896/IBRA.1.52.1.0
19. Ellis JD (2008) Varroa Mite, Varroa destructor Anderson and Trueman (Acari: Varroidae). In: Capinera JL (ed) Encyclopedia of entomology. Springer, Berlin, pp 4041–4048
20. Fletcher DJC (1975) New perspectives in the causes of absconding in the African bee (Apis mellifera adansonii L.). Part 1. S Afr Bee J 47:11–14
21. Fletcher DJC (1978) The African bee, Apis mellifera adansonii, in Africa. Annu Rev Entomol 23:151–171
22. Francis RM, Nielsen SL, Kryger P (2013) Varroa-virus interaction in collapsing honey bee colonies. PLoS One 8:e57540
23. Francoy TM, Wittmann D, Steinhage V, Drauschke M, Müller S, Cunha DR, Nascimento AM, Figueiredo VLC, Simões ZLP, De Jong D, Arias MC, Gonçalves LS (2009) Morphometric and genetic changes in a population of Apis mellifera after 34 years of Africanization. Genet Mol Res 8:709–717
24. Frazier M, Muli E, Conklin T, Schmehl D, Torto B, Frazier J, Tumlinson J, Evans JD, Raina S (2010) A scientific note on Varroa destructor found in East Africa; threat or opportunity? Apidologie 41:463–465
25. Fries I, Raina S (2003) American foulbrood and African honey bees (Hymenoptera: Apidae). J Econ Entomol 96:1641–1646
26. Fries I, Huazhen W, Wei S, Jin CS (1996) Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie 27:3–11
27. Fries I, Imdorf A, Rosenkranz P (2006) Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie 37:564–570
28. Garrido C, Rosenkranz P, Paxton RJ, Gonçalves LS (2003) Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34:535–541
29. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352
30. Gerig L (1983) Lehrgang zur erfassung der volksstärke. Schweiz. Bienen-Zeitung 106:199–204
31. Guerra JCV, Gonçalves LS, De Jong D (2000) Africanized honey bees (Apis mellifera L.) are more efficient at removing worker brood artificially infested with the parasitic mite Varroa jacobsoni Oudemans than are Italian bees or Italian/Africanized hybrids. Genet Mol Biol 23:89–92
32. Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer, Berlin
33. Imdorf A, Maquelin C (1993) Volksschätzung im zeitigen Frühjahr, Schweiz. Bienenztg 116:392–395
34. Kerr WE (1967) The history of the introduction of African bees to Brazil. S Afr Bee J 39:3–5
35. Koeniger N, Koeniger G, Delfinado-Baker M (1983) Observations on mites of the Asian honeybee species (Apis cerana, Apis dorsata, Apis florea). Apidologie 14:197–204
36. Kraus FB, Franck P, Vandame R (2007) Asymmetric introgression of African genes in honeybee populations (Apis mellifera L.) in Central Mexico. Heredity 99:233–240
37. Le Conte Y, de Vaublanc G, Crauser D, Jeanne F, Rousselle JC, Bécard J-M (2007) Honey bee colonies that have survived Varroa destructor. Apidologie 38:566–572
38. Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41:353–363
39. Locke B, Fries I (2011) Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie 42:533–542
40. Locke B, Le Conte Y, Crauser D, Fries I (2012) Host adaptations reduce the reproductive success of Varroa destructor in two distinct European honey bee populations. Ecol Evol 2:1144–1150
41. Martin SJ (1998) A population model for the ectoparasitic mite Varroa jacobsoni in honey bee (Apis mellifera) colonies. Ecol Model 109:267–281
42. Martin SJ, Kryger P (2002) Reproduction of Varroa destructor in South African honey bees: does cell space influence Varroa male survivorship? Apidologie 33:51–61
43. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powell M, Nikaido S, Schroeder DC (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336:1304–1306
44. Mcnally LC, Schneider SS (1992) Seasonal cycles of growth, development and movement of the African honey bee, Apis mellifera scutellata, in Africa. Insectes Soc 39:167–179
45. Medina LM, 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
46. Medina LM, Martin SJ, Espinosa-Montaño L, Ratnieks FLW (2002) Reproduction of Varroa destructor in worker brood of Africanized honey bees (Apis mellifera). Exp Appl Acarol 27:79–88
47. Michener CD (1973) The Brazilian honeybee. Bioscience 23:523–527
48. Mondragón 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
49. Mondragón 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
50. Moritz RFA (1985) Heritability of the postcapping stage in Apis mellifera and its relation to varroatosis resistance. J Hered 76:267–270
51. Moritz RFA, Hänel H (1984) Restricted development of the parasitic mite Varroa jacobsoni Oud. in the Cape honey bee, Apis mellifera capensis Esch. Z Angew Entomol 97:91–95
52. Moritz RFA, Härtel S, Neumann P (2005) Global invasions of the western honey bee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12:289–301
53. Page RE (1998) Blessing or curse? Varroa mite impacts Africanized bee spread and beekeeping. Calif Agric 52:9–13
54. 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
55. Pirk CWW, Human H, Crewe RM, vanEngelsdorp D (2014) A survey of managed honey bee colony losses in the Republic of South Africa—2009 to 2011. J Apic Res 53:35–42
56. Rath W (1999) Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie 30:97–110
57. Rath W, Drescher W (1990) Response of Apis cerana Fabr. towards brood infested with Varroa jacobsoni Oud., and infestation rate of colonies in Thailand. Apidologie 21:311–321
58. Rosenkranz P (1999) Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30:159–172
59. Rosenkranz P, Engels W (1994) Infertility of Varroa jacobsoni females after invasion into Apis mellifera worker brood as a tolerance factor against varroatosis. Apidologie 25:402–411
60. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:96–119
61. Schneider SS, DeGrandi-Hoffman G, Smith DR (2004) The African honey bee: factors contributing to a successful biological invasion. Annu Rev Entomol 49:351–376
62. Seeley TD (2007) Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38:19–29
63. Shabanov M, Nedyalkov S, Toshkov AL (1978) Varroatosis—a dangerous parasitic disease on bees. Am Bee J 118:402-403, 407
64. Sheppard WS, Smith DR (2000) Identification of African-derived bees in the Americas: A survey of methods. Ann Entomol Soc Am 93:159–176
65. Sheppard WS, Soares AEE, De Jong D, Shimanuki H (1991) Hybrid status of honey bee populations near the historic origin of Africanization in Brazil. Apidologie 22:643–652
66. Solignac M, Cornuet J, Vautrin D, Le Conte Y, Anderson D, Evans JD, Cros-Arteil S, Navajas M (2005) The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honey bee (Apis mellifera), are two partly isolated clones. Proc R Soc Biol Sci Ser B 272:411–419
67. Spleen AM, Lengerich EJ, Rennich K, Caron DM, Rose R, Pettis JS, Henson M, Wilkes JT, Wilson ME, Stitzinger J, Lee K, Andree M, Snyder R, vanEngelsdorp D (2013) A national survey of managed honey bee 2011-2012 winter colony losses in the United States: results from the Bee Informed Partnership. J Apic Res 52:44–53
68. Steinhauer NA, Rennich K, Wilson ME, Caron DM, Lengerich EJ, Pettis JS, Rose R, Skinner JA, Tarpy DR, Wilkes JT, van Engelsdorp D (2014) A national survey of managed honey bee 2012–2013 annual colony losses in the USA: results from the Bee Informed Partnership. J Apic Res 53:1–18
69. Strauss U, Human H, Gauthier L, Crewe RM, Dietemann V, Pirk CWW (2013) Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). J Invertebr Pathol 114:45–52
70. Swart DJ (2001) Specialized management. In: Johannsmeier MF (ed) Beekeeping in South Africa, plant protection handbook no. 14. Agricultural Research Council, Pretoria, pp 85–94
71. Tribe GD, Allsopp M (2001) Life history of the honeybee colony. In: Johannsmeier MF (ed) Beekeeping in South Africa, plant protection handbook no. 14. Agricultural Research Council, Pretoria, pp 17–26
72. van Dooremalen C, Stam E, Gerritsen L, Cornelissen B, van der Steen J, van Langevelde F, Blacquière T (2013) Interactive effect of reduced pollen availability and Varroa destructor infestation limits growth and protein content of young honey bees. J Insect Physiol 59:487–493
73. Vandame R, Colin ME, Otero-Colina G (1999) Africanized honey bees tolerance to Varroa in Mexico: mite infertility is not the main tolerance factor. Apiacta 1:12–20
74. Vandame R, Morand S, Colin ME, Belzunces LP (2002) Parasitism in the social bee Apis mellifera: quantifying costs and benefits of behavioral resistance to Varroa destructor mites. Apidologie 33:433–445
75. Visscher PK, Vetter RS, Baptista FC (1997) Africanized bees, 1990–1995: initial rapid invasion has slowed in the US. Calif Agric 51:22–25
76. Whitfield CW, Behura SK, Berlocher SH, Clark AG, Spencer Johnston J, Sheppard WS, Smith DR, Suarez AV, Weaver D, Tsutsui ND (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642–645
77. Winston ML (1992) The biology and management of Africanized honey bees. Annu Rev Entomol 37:173–193