Managing the parasitic honey bee mite Tropilaelaps mercedesae through combined cultural and chemical control methods.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
27 Oct 2024
27 Oct 2024
Historique:
received:
14
05
2024
accepted:
11
10
2024
medline:
28
10
2024
pubmed:
28
10
2024
entrez:
28
10
2024
Statut:
epublish
Résumé
The western honey bee (Apis mellifera) is severely impacted by the parasitic Tropilaelaps mercedesae mite, which has the capacity to outcompete Varroa destructor mites (the current leading cause of colony losses) and more rapidly overwhelm colonies. While T. mercedesae is native to Asia, it has recently expanded its geographic range and has the potential to devastate beekeeping worldwide if introduced to new regions. Our research exploited the dependence of T. mercedesae on developing honey bees (brood) by combining a cultural technique (brood break) with U.S. registered chemical products (oxalic acid or formic acid) to manage T. mercedesae infestation. To evaluate this approach, we compared four treatment groups: (1) Brood Break; (2) Brood Break + Formic Acid (FormicPro
Identifiants
pubmed: 39463393
doi: 10.1038/s41598-024-76185-4
pii: 10.1038/s41598-024-76185-4
doi:
Substances chimiques
formic acid
0YIW783RG1
Formates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25677Subventions
Organisme : Animal and Plant Health Inspection Service
ID : USDA-AP23PPQS&T00C067
Organisme : Animal and Plant Health Inspection Service
ID : USDA-AP23PPQS&T00C067
Organisme : Animal and Plant Health Inspection Service
ID : USDA-AP23PPQS&T00C067
Organisme : Animal and Plant Health Inspection Service
ID : USDA-AP23PPQS&T00C067
Organisme : Animal and Plant Health Inspection Service
ID : USDA-AP23PPQS&T00C067
Organisme : Project Apis m.
ID : RA 382
Organisme : Project Apis m.
ID : RA 382
Organisme : Agricultural Research Service
ID : 58-6066-9-042
Organisme : Agricultural Research Service
ID : 58-6066-9-042
Organisme : Agricultural Research Service
ID : 58-6066-9-042
Informations de copyright
© 2024. The Author(s).
Références
Aurell, D., Bruckner, S., Wilson, M., Steinhauer, N. & Williams, G. R. A national survey of managed honey bee colony losses in the USA: results from the Bee Informed Partnership for 2020–21 and 2021–22. J. Apic. Res. 63, 1–14 (2024).
doi: 10.1080/00218839.2023.2264601
Chantawannakul, P., Ramsey, S., vanEngelsdorp, D., Khongphinitbunjong, K. & Phokasem, P. Tropilaelaps mite: an emerging threat to European honey bee. Curr. Opin. Insect Sci. 26, 69–75 (2018).
pubmed: 29764663
doi: 10.1016/j.cois.2018.01.012
De Guzman, L. I., Williams, G. R., Khongphinitbunjong, K. & Chantawannakul, P. Ecology, life history, and management of Tropilaelaps mites. J. Econ. Entomol. 110, 319–332 (2017).
pubmed: 28334185
doi: 10.1093/jee/tow304
Rosenkranz, P., Aumeier, P. & Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119 (2010).
pubmed: 19909970
doi: 10.1016/j.jip.2009.07.016
Mohamadzade Namin, S. et al. Exploring genetic variation and phylogenetic patterns of Tropilaelaps mercedesae (Mesostigmata: Laelapidae) populations in Asia. Front. Ecol. Evol. 12, 1275995 (2024).
doi: 10.3389/fevo.2024.1275995
Bruckner, S. et al. A national survey of managed honey bee colony losses in the USA: results from the Bee Informed Partnership for 2017–18, 2018–19, and 2019–20. J. Apic. Res. 62, 429–443 (2023).
doi: 10.1080/00218839.2022.2158586
Buawangpong, N. et al. Prevalence and reproduction of Tropilaelaps mercedesae and Varroa destructor in concurrently infested Apis mellifera colonies. Apidologie. 46, 779–786 (2015).
doi: 10.1007/s13592-015-0368-8
Ritter, W. & Schneider-Ritter, U. Differences in biology and means of controlling Varroa jacobsoni and Tropilaelaps clareae, two novel parasitic mites of Apis mellifera. in Africanized Honey Bees and Bee Mites 387–395 Halstead Press, (1988).
Woyke, J. Length of successive stages in the development of the mite tropilaelaps clareae in relation to honeybee brood age. J. Apic. Res. 26, 110–114 (1987).
doi: 10.1080/00218839.1987.11100746
Rath, W., Delfinado-Baker, M. & Drescher, W. Observations on the mating behavior, sex ratio, phoresy and dispersal of Tropilaelaps clareae (Acari: Laelapidae). J. Acarology. 17, 201–208 (1991).
doi: 10.1080/01647959108683907
Khongphinitbunjong, K., Neumann, P., Chantawannakul, P. & Williams, G. R. The ectoparasitic mite tropilaelaps mercedesae reduces western honey bee, Apis mellifera, longevity and emergence weight, and promotes deformed wing virus infections. J. Invertebr. Pathol. 137, 38–42 (2016).
pubmed: 27126517
doi: 10.1016/j.jip.2016.04.006
Khongphinitbunjong, K., De Guzman, L. I., Tarver, M. R., Rinderer, T. E. & Chantawannakul, P. Interactions of Tropilaelaps mercedesae, honey bee viruses and immune response in Apis mellifera. J. Apic. Res. 54, 40–47 (2015).
doi: 10.1080/00218839.2015.1041311
Jack, C. J. & Ellis, J. D. Integrated pest management control of Varroa destructor (Acari: Varroidae), the most damaging pest of (Apis mellifera L. (Hymenoptera: Apidae)) colonies. J. Insect Sci. 21, 6 (2021).
pubmed: 34536080
pmcid: 8449538
doi: 10.1093/jisesa/ieab058
Traynor, K. S. et al. Varroa destruator: a complex parasite, crippling honey bees worldwide. Trends Parasitol. 36, 592–606 (2020).
pubmed: 32456963
doi: 10.1016/j.pt.2020.04.004
Woyke, J. Infestation of honeybee (Apis mellifera) colonies by the parasitic mites Varroa jacobsoni and tropilaelaps clareae in South Vietnam and results of chemical treatment. J. Apic. Res. 26, 64–67 (1987).
doi: 10.1080/00218839.1987.11100738
Woyke, J. Tropilaelaps clareae females can survive for four weeks when given open bee brood of Apis mellifera. J. Apic. Res. 33, 21–25 (1994).
doi: 10.1080/00218839.1994.11100845
Woyke, J. Comarative population dynamics of Tropilaelaps clareae and Varroa jacobsoni mites on honey bees. J. Apic. Res. 26, 196–202 (1987).
doi: 10.1080/00218839.1987.11100759
Häußermann, C. K., Ziegelmann, B. & Rosenkranz, P. Spermatozoa capacitation in female Varroa destructor and its influence on the timing and success of female reproduction. Exp. Appl. Acarol. 69, 371–387 (2016).
pubmed: 27209572
doi: 10.1007/s10493-016-0051-4
Pettis, J. S., Rose, R. & Chaimanee, V. Chemical and cultural control of Tropilaelaps mercedesae mites in honeybee (Apis mellifera) colonies in Northern Thailand. PLoS One. 12, e0188063 (2017).
pubmed: 29125881
pmcid: 5681254
doi: 10.1371/journal.pone.0188063
Khongphinitbunjong, K., De Guzman, L. I., Burgett, M. D., Rinderer, T. E. & Chantawannakul, P. Behavioral responses underpinning resistance and susceptibility of honeybees to Tropilaelaps mercedesae. Apidologie. 43, 590–599 (2012).
doi: 10.1007/s13592-012-0129-x
Koeniger, N. & Muzaffar, N. Lifespan of the parasitic honeybee mite, Tropilaelaps Clareae, on Apis Cerana, Dorsata and Mellifera. J. Apic. Res. 27, 207–212 (1988).
doi: 10.1080/00218839.1988.11100804
Rinderer, T. E. et al. Extended survival of the parasitic honey bee mite Tropilaelaps clareae on adult workers of Apis mellifera and Apis dorsata. J. Apic. Res. 33, 171–174 (1994).
doi: 10.1080/00218839.1994.11100866
Roberts, J. M. K., Schouten, C. N., Sengere, R. W., Jave, J. & Lloyd, D. Effectiveness of control strategies for Varroa jacobsoni and Tropilaelaps mercedesae in Papua New Guinea. Exp. Appl. Acarol. 80, 399–407 (2020).
pubmed: 32072354
doi: 10.1007/s10493-020-00473-7
Woyke, J. Further investigations into control of the parasite bee mite Tropilaelaps clareae without medication. J. Apic. Res. 24, 250–254 (1985).
doi: 10.1080/00218839.1985.11100681
Berry, J. A., Braman, S. K., Delaplane, K. S. & Bartlett, L. J. Inducing a summer brood break increases the efficacy of oxalic acid vaporization for Varroa destructor (Mesostigmata: Varroidae) control in Apis mellifera (Hymenoptera: Apidae) colonies. J. Insect Sci. 23, 14 (2023).
pubmed: 38055946
pmcid: 10699866
doi: 10.1093/jisesa/iead085
Büchler, R. et al. Summer brood interruption as integrated management strategy for effective Varroa control in Europe. J. Apic. Res. 59, 764–773 (2020).
doi: 10.1080/00218839.2020.1793278
Gregorc, A., Alburaki, M., Werle, C., Knight, P. R. & Adamczyk, J. Brood removal or queen caging combined with oxalic acid treatment to control varroa mites (Varroa destructor) in honey bee colonies (Apis mellifera). Apidologie. 48, 821–832 (2017).
doi: 10.1007/s13592-017-0526-2
Kulhanek, K., Garavito, A. & vanEngelsdorp, D. Accelerated Varroa destructor population growth in honey bee (Apis mellifera) colonies is associated with visitation from non-natal bees. Sci. Rep. 11, 7092 (2021).
pubmed: 33782493
pmcid: 8007729
doi: 10.1038/s41598-021-86558-8
NOD Apiary Products. FormicPro® pesticide label (2017).
Underwood, R. M. & Currie, R. W. Effect of concentration and exposure time on treatment efficacy against Varroa mites (Acari: Varroidae) during indoor winter fumigation of honey bees (Hymenoptera: Apidae) with formic acid. J. Econ. Entomol. 98, 1802–1809 (2005).
pubmed: 16539097
doi: 10.1093/jee/98.6.1802
Steube, X., Beinert, P. & Kirchner, W. H. Efficacy and temperature dependence of 60% and 85% formic acid treatment against Varroa destructor. Apidologie. 52, 720–729 (2021).
doi: 10.1007/s13592-021-00859-5
Underwood, R. M. et al. A longitudinal experiment demonstrates that honey bee colonies managed organically are as healthy and productive as those managed conventionally. Sci. Rep. 13, 6072 (2023).
pubmed: 37055462
pmcid: 10100614
doi: 10.1038/s41598-023-32824-w
Camphor, E. S. W., Hashmi, A. A., Ritter, W. & Bowen, I. D. Seasonal changes in mite (Tropilaelaps Clareae) and honeybee (Apis mellifera) populations in apistan treated and untreated colonies. Apiacta. 40, 34–44 (2005).
Raffique, M. K., Mahmood, R., Aslam, M. & Sarwar, G. Control of tropilaelaps clareae mite by using formic acid and thymol in honey bee Apis mellifera L. colonies. Pakistan J. Zool. 44, 1129–1135 (2012).
Laigo, F. M. & Morse, R. A. The mite tropilaelaps clareae in Apis dorsata colonies in the Philippines. Bee World. 49, 116–118 (1968).
doi: 10.1080/0005772X.1968.11097211
Jack, C. J., De Bem Oliveira, I., Kimmel, C. B. & Ellis, J. D. Seasonal differences in Varroa destructor population growth in western honey bee (Apis mellifera) colonies. Front. Ecol. Evol. 11, 1102457 (2023).
doi: 10.3389/fevo.2023.1102457
Dynes, T. L., Berry, J. A., Delaplane, K. S., Brosi, B. J. & de Roode, J. C. Reduced density and visually complex apiaries reduce parasite load and promote honey production and overwintering survival in honey bees. PLoS One. 14, e0216286 (2019).
pubmed: 31120911
pmcid: 6532956
doi: 10.1371/journal.pone.0216286
Guzman-Novoa, E. et al. Standard methods to estimate strength parameters, flight activity, comb construction, and fitness of Apis mellifera colonies 2.0. J. Apic. Res. 1–22 https://doi.org/10.1080/00218839.2024.2329853 (2024).
Maucourt, S., Fournier, V. & Giovenazzo, P. Comparison of three methods to multiply honey bee (Apis mellifera) colonies. Apidologie. 49, 314–324 (2018).
doi: 10.1007/s13592-017-0556-9
Altman, D. G. The revised CONSORT Statement for reporting randomized trials: explanation and elaboration. Ann. Intern. Med. 134, 663 (2001).
pubmed: 11304107
doi: 10.7326/0003-4819-134-8-200104170-00012
Moher, D. et al. CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials. BMJ. 340, c869–c869 (2010).
pubmed: 20332511
pmcid: 2844943
doi: 10.1136/bmj.c869
Molineri, A. et al. Risk factors for the presence of deformed wing virus and Acute bee paralysis virus under temperate and subtropical climate in Argentinian bee colonies. Prev. Vet. Med. 140, 106–115 (2017).
pubmed: 28460743
doi: 10.1016/j.prevetmed.2017.02.019
Giacobino, A. et al. Risk factors associated with the presence of Varroa destructor in honey bee colonies from east-central Argentina. Prev. Vet. Med. 115, 280–287 (2014).
pubmed: 24794646
doi: 10.1016/j.prevetmed.2014.04.002
Kernan, W. N., Viscoli, C. M., Makuch, R. W. & Brass, L. M. Horwitz, R. I. Stratified Randomization for clinical trials. J. Clin. Epidemiol. 52, 19–26 (1999).
pubmed: 9973070
doi: 10.1016/S0895-4356(98)00138-3
Hurlbert, S. H. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187–211 (1984).
doi: 10.2307/1942661
Jack, C. J., Van Santen, E. & Ellis, J. D. Determining the dose of oxalic acid applied via vaporization needed for the control of the honey bee (Apis mellifera) pest Varroa destructor. J. Apic. Res. 60, 414–420 (2021).
doi: 10.1080/00218839.2021.1877447
Jack, C. J., Van Santen, E. & Ellis, J. D. Evaluating the efficacy of oxalic acid vaporization and brood interruption in controlling the honey bee pest Varroa destructor (Acari: Varroidae). J. Econ. Entomol. 113, 582–588 (2020).
pubmed: 31909423
doi: 10.1093/jee/toz358
Sabahi, Q., Gashout, H., Kelly, P. G. & Guzman-Novoa, E. Continuous release of oregano oil effectively and safely controls Varroa destructor infestations in honey bee colonies in a northern climate. Exp. Appl. Acarol. 72, 263–275 (2017).
pubmed: 28748336
pmcid: 5547185
doi: 10.1007/s10493-017-0157-3
Pettis, J. S. et al. A rapid survey technique for Tropilaelaps Mite (Mesostigmata: Laelapidae) detection. J. Econ. Entomol. 106, 1535–1544 (2013).
pubmed: 24020263
doi: 10.1603/EC12339
R Core Team. R: A Language and Environment for Statistical Computing (R foundation for Statistical Computing, 2022).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear mixed-effects models using lme4. J. Stat. Soft. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Wickham, H. ggplot2: Elegant Graphics for data Analysis (Spinger-, 2016).
Wickham, H., Francois, R., Henry, L. & Muller, K. & Vaughan, D. dplyr: A grammar of data manipulation. R package version 1.1.0 (2023).
Lenth, R. V. & emmeans Estimated marginal means, aka least-squares means. R package version 1.8.7 (2023).
Hartig, F. & DHARMa Residual diagnostics for hierarchial (multi-level / mixed) regression models. (2022).