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Apidologie

, Volume 49, Issue 5, pp 573–580 | Cite as

A honey bee (Apis mellifera) colony’s brood survival rate predicts its in vitro-reared brood survival rate

  • Ashley N. Mortensen
  • James D. Ellis
Original article
  • 93 Downloads

Abstract

Rearing honey bee, Apis mellifera L., larvae in vitro is a popular risk assessment tool because many uncontrollable factors (e.g., weather conditions, food availability) that bias field studies can be eliminated in the laboratory. However, modern in vitro rearing techniques suffer variable survival rates and OECD guidelines specify a minimum of 70% survival to adult emergence in the untreated negative controls for the test to be considered valid. We hypothesized that the colony from which larvae are sourced for in vitro-rearing risk assessments may affect the survival percentage of those larvae in vitro. To test this hypothesis, we compared the survival rates of brood reared in vitro to that of brood reared by their parental colony to determine if source colony affects brood survival in vitro. Colony-reared and in vitro-reared brood survival percentages were calculated for each of the 14 colonies. There was not a statistically detectable difference in the survival percentage to adult emergence of colony-reared and in vitro-reared bees. Furthermore, the colony-reared brood survival percentage at day 11 (prepupal stage) was predictive of the survival percentage to adult emergence of in vitro-reared bees. We suggest that the 11-day brood survival percentage should be used when selecting suitable colonies for use as source colonies for in vitro-rearing risk assessments. Based on our results, colonies with brood survival percentages of ≥ 80% are suitable colonies from which to source larvae for in vitro-rearing risk assessments.

Keywords

Apis mellifera honey bee in vitro brood rearing 

Notes

Acknowledgements

We are grateful to Daniel Schmehl and Hudson Tomé for their help with troubleshooting the in vitro rearing protocol, Cameron Jack for assistance in rearing honey bee larvae, Brandi Simmons and Emily Helton for ordering and preparing project supplies, Logan Cutts and Liana Teigan for managing healthy honey bee colonies, Vince Alderman for his diligent construction of project tools, and Edzar van Santen for statistical consultation.

Author contributions

ANM and JDE conceived this research; ANM performed experiments and wrote the paper; and JDE and ANM participated in the revisions of the paper. All authors read and approved the final manuscript.

Funding information

Funding for this project was provided by the USDA National Institute of Food and Agriculture Multistate Project (1005822) and the National Honey Board.

References

  1. Al-Lawati H, Bienefeld K (2009) Maternal Age Effects on Embryo Mortality and Juvenile Development of Offspring in the Honey Bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 102, (5):881-888. doi: https://doi.org/10.1603/008.102.0514 'CrossRefGoogle Scholar
  2. Alix A, Chauzat MP, Duchard S, Lewis G, Maus C, Miles MJ, Pilling E, Thompson HM, Wallner K (2010) Environmental risk assessment scheme for plant protection products Chapter 10: Honeybees–Proposed scheme. Julius-Kühn-Archiv. 423, 27Google Scholar
  3. Asencot M, Lensky Y (1984) Juvenile hormone induction of “queenliness” on female honey bee (Apis mellifera L.) larvae reared on worker jelly and on stored royal jelly. Comp. Biochem. Physiol. B 78, 109–117.CrossRefGoogle Scholar
  4. Aupinel P, Fortini D, Dufour H, Tasei J, Michaud B, Odoux J, et al. (2005) Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. B. Istectol. 58, 107–111.Google Scholar
  5. Aupinel P, Fortini D, Michaud B, Medrzycki P, Padovani E, et al. (2010) Honey bee brood ring-test: method for testing pesticide toxicity on honeybee brood in laboratory conditions. Julius-Kühn-Archiv 423, 96–102.Google Scholar
  6. Breed MD, Rogers KB (1991) The behavioral genetics of colony defense in honeybees: genetic variability for guarding behavior. Behav. Genet. 21, 295–303. doi:  https://doi.org/10.1007/BF01065821 CrossRefPubMedGoogle Scholar
  7. Brouwers EVM (1984) Glucose/fructose ratio in the food of honeybee larvae during caste differentiation. J. Apic. Res. 23, 94–101.CrossRefGoogle Scholar
  8. Buttstedt A, Ihling CH, Pietzsch M, Moritz RFA (2016) Royalactin is not a royal making of a queen. Nature 537:E10–E12.CrossRefGoogle Scholar
  9. Chauzat M-P, Faucon J-P, Martel A-C, Lachaize J, Cougoule N, et al. (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol. 99, 253–262.CrossRefGoogle Scholar
  10. Crailsheim K, Brodschneider R, Aupinel P, Behrens D, Genersch E, et al. (2013) Standard methods for artificial rearing of Apis mellifera larvae. J. Apic. Res. 52, 1–16. doi:  https://doi.org/10.3896/IBRA.1.52.1.05 CrossRefGoogle Scholar
  11. De Souza DA, Wang Y, Kaftanoglu O, De Jong D, Amdam GV, et al. (2015) Morphometric identification of queens, workers and intermediates in in vitro reared honey bees (Apis mellifera). PLoS ONE 10, e0123663. doi:  https://doi.org/10.1371/journal.pone.0123663 CrossRefPubMedGoogle Scholar
  12. Delaplane KS, van der Steen J, Guzman-Novoa E (2013) Standard methods for estimating strength parameters of Apis mellifera colonies. J. Apic. Res. doi:  https://doi.org/10.3896/IBRA/1.52.1.03
  13. Florida Department of Agriculture and Consumer Services (FDACS) (2013) Best management practices for maintaining European honey bee colonies. http://www.freshfromflorida.com/content/download/71084/1640892/08492.pdf. Accessed on 11 October 2017
  14. Hendriksma HP, Härtel S, Steffan-Dewenter I (2011) Honey bee risk assessment: new approaches for in vitro larvae rearing and data analyses. Methods Ecol. Evol. 2, 509–517.CrossRefGoogle Scholar
  15. Higes M, Martín-Hernández R, Botías C, Bailón EG, González-Porto AV, Barrios L, et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10, 2659–2669. doi:  https://doi.org/10.1111/j.1462-2920.2008.01687.x CrossRefPubMedGoogle Scholar
  16. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204.PubMedPubMedCentralGoogle Scholar
  17. Human H, Brodschneider R, Dietemann V, Dively G, Ellis JD, et al. (2013) Miscellaneous standard methods for Apis mellifera research. J. Apic. Res. 52, 1–53. doi:  https://doi.org/10.3896/IBRA.1.52.4.10 CrossRefGoogle Scholar
  18. Ibrahim A, Spivak M (2006) The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor. Apidologie 37, 31.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Lebuhn G, Droege S, Connor EF, Gemmill-Herren B, Potts SG, et al. (2013) Detecting insect pollinator declines on regional and global scales. Conserv. Biol. 27, 113–120. doi:  https://doi.org/10.1111/j.1523-1739.2012.01962.x CrossRefPubMedGoogle Scholar
  21. Lynch M, Walsh B (1997) Genetics and analysis of quantitative traits. Sinauer Associates Incorporated, SunderlandGoogle Scholar
  22. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, et al. (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306. doi:  https://doi.org/10.1126/science.1220941 CrossRefPubMedGoogle Scholar
  23. Medrzycki P, Giffard H, Aupinel P, Belzunces LP, Chauzat M-P, et al. (2013) Standard methods for toxicology research in Apis mellifera. J. Apic. Res. 52, 1–60. doi:  https://doi.org/10.3896/IBRA.1.52.4.14 CrossRefGoogle Scholar
  24. Meixner MD, Pinto MA, Bouga M, Kryger P, Ivanova E, et al. (2013) Standard methods for characterising subspecies and ecotypes of Apis mellifera. J. Apic. Res. 52, 1–28. doi:  https://doi.org/10.3896/IBRA.1.52.4.05 CrossRefGoogle Scholar
  25. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5, e9754. doi:  https://doi.org/10.1371/journal.pone.0009754 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nettle D (2006) The evolution of personality variation in humans and other animals. Am. Psychol. 61, 622–631. doi:  https://doi.org/10.1037/0003-066X.61.6.622 CrossRefPubMedGoogle Scholar
  27. Neumann P, Carreck NL (2010) Honey bee colony losses. J. Apic. Res. 49, 1–6. doi:  https://doi.org/10.3896/IBRA.1.49.1.01 CrossRefGoogle Scholar
  28. OECD (2015) Honey Bee (Apis mellifera) Larval Toxicity Test, Repeated Exposure. OECD DRAFT GUIDANCE DOCUMENTGoogle Scholar
  29. Peng Y-S, Jay SC (1977) Larval rearing by worker honey bees lacking their mandibular glands: I. Rearing by small numbers of worker bees. Can. Entomol. 109, 1175–1180.CrossRefGoogle Scholar
  30. Peng Y-SC, Mussen E, Fong A, Montague MA, Tyler T (1992) Effects of chlortetracycline of honey bee worker larvae reared in vitro. J. Invertebr. Pathol. 60, 127–133.CrossRefGoogle Scholar
  31. Pirk CWW, de Miranda JR, Kramer M, Murray TE, Nazzi F, Shutler D, et al. (2013) Statistical guidelines for Apis mellifera research. J. Apic. Res. 52, 1–24. doi:  https://doi.org/10.3896/IBRA.1.52.4.13 CrossRefGoogle Scholar
  32. Rembold H, Lackner B (1981) Rearing of honeybee larvae in vitro - effect of yeast extract on queen differentiation. J. Apic. Res. 20, 165–171.CrossRefGoogle Scholar
  33. Scheiner R, Abramson CI, Brodschneider R, Crailsheim K, Farina WM, et al. (2013) Standard methods for behavioural studies of Apis mellifera. J. Apic. Res. 52, 1–58. doi:  https://doi.org/10.3896/IBRA.1.52.4.04 CrossRefGoogle Scholar
  34. Schmehl DR, Tomé HVV, Mortensen AN, Martins GF, Ellis JD (2016) Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. J. Apic. Res. 55, 113–129. doi:  https://doi.org/10.1080/00218839.2016.1203530 CrossRefGoogle Scholar
  35. Sheppard WS (1989) A history of the introduction of honey bee races into the United Sates: Part II. Am. Bee J. 129, 664–667.Google Scholar
  36. Silva IC, Message D, Cruz CD, Campos LAO, Sousa-Majer MJ (2009) Rearing Africanized honey bee (Apis mellifera L.) brood under laboratory conditions. Genet. Mol. Res. 8, 623–629.CrossRefGoogle Scholar
  37. Spivak M, Gilliam M (1998) Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa. Bee World 79, 124–134. doi:  https://doi.org/10.1080/0005772X.1998.11099394 CrossRefGoogle Scholar
  38. Steinhauer NA, Rennich K, Wilson ME, Caron DM, Lengerich EJ, et al. (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. doi:  https://doi.org/10.3896/IBRA.1.53.1.01 CrossRefGoogle Scholar
  39. Vandenberg JD, Shimanuki H (1987) Technique for rearing worker honeybees in the laboratory. J. Apic. Res. 26, 90–97. doi:  https://doi.org/10.1080/00218839.1987.11100743 CrossRefGoogle Scholar
  40. vanEngelsdorp D, Speybroeck N, Evans JD, Nguyen BK, Mullin C, et al. (2010) Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis. J. Econ. Entomol. 103, 1517–1523. doi:  https://doi.org/10.1603/EC09429 CrossRefPubMedGoogle Scholar
  41. Wittmann D, Engels W (1981) Development of test procedures for insecticide-induced brood damage in honeybees. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 3, 187–190.Google Scholar
  42. Woyke J (1963) Rearing and viability of diploid drone larvae. J. Apic. Res. 2, 77–84.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Honey Bee Research and Extension Laboratory, Entomology & Nematology DepartmentUniversity of FloridaGainesvilleUSA
  2. 2.The New Zealand Institute for Plant & Food Research LimitedHamiltonNew Zealand

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