The Year of the Honey Bee (Apis mellifera L.) with Respect to Its Physiology and Immunity: A Search for Biochemical Markers of Longevity
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
QJ1610248
Ministerstvo Zemědělství
2017/19718-0
Sao Paulo Research Foundation
PubMed
31394797
PubMed Central
PMC6723739
DOI
10.3390/insects10080244
PII: insects10080244
Knihovny.cz E-zdroje
- Klíčová slova
- honey bee, immunity, longevity, physiology, seasonal changes,
- Publikační typ
- časopisecké články MeSH
It has been known for many years that in temperate climates the European honey bee, Apis mellifera, exists in the form of two distinct populations within the year, short-living summer bees and long-living winter bees. However, there is only limited knowledge about the basic biochemical markers of winter and summer populations as yet. Nevertheless, the distinction between these two kinds of bees is becoming increasingly important as it can help beekeepers to estimate proportion of long-living bees in hives and therefore in part predict success of overwintering. To identify markers of winter generations, we employed the continuous long-term monitoring of a single honey bee colony for almost two years, which included measurements of physiological and immunological parameters. The results showed that the total concentration of proteins, the level of vitellogenin, and the antibacterial activity of haemolymph are the best three of all followed parameters that are related to honey bee longevity and can therefore be used as its markers.
Zobrazit více v PubMed
Klatt B.K., Holzschuh A., Westphal C., Clough Y., Smit I., Pawelzik E., Tscharntke T. Bee pollination improves crop quality, shelf life and commercial value. Proc. R. Soc. B Biol. Sci. 2013;281:20132440. doi: 10.1098/rspb.2013.2440. PubMed DOI PMC
Klein A.M., Vaissière B.E., Cane J.H., Steffan-Dewenter I., Cunningham S.A., Kremen C., Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007;274:303–313. doi: 10.1098/rspb.2006.3721. PubMed DOI PMC
Potts S.G., Biesmeijer J.C., Kremen C., Neumann P., Schweiger O., Kunin W.E. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 2010;25:345–353. doi: 10.1016/j.tree.2010.01.007. PubMed DOI
Steinhauer N., Kulhanek K., Antúnez K., Human H., Chantawannakul P., Chauzat M.P., vanEngelsdorp D. Drivers of colony losses. Curr. Opin. Insect Sci. 2018;26:142–148. doi: 10.1016/j.cois.2018.02.004. PubMed DOI
Williams G.R., Tarpy D.R., VanEngelsdorp D., Chauzat M.P., Cox-Foster D.L., Delaplane K.S., Neumann P., Pettis J.S., Rogers R.E.L., Shutler D. Colony collapse disorder in context. BioEssays. 2010;32:845–846. doi: 10.1002/bies.201000075. PubMed DOI PMC
vanEngelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier M., Frazier J., Cox-Foster D., Chen Y., et al. Colony collapse disorder: A descriptive study. PLoS ONE. 2009;4:e6481. doi: 10.1371/journal.pone.0006481. PubMed DOI PMC
Danihlík J., Škrabišová M., Lenobel R., Šebela M., Omar E., Petřivalský M., Crailsheim K., Brodschneider R. Does the pollen diet influence the production and expression of antimicrobial peptides in individual honey bees? Insects. 2018;9:79. doi: 10.3390/insects9030079. PubMed DOI PMC
Chauzat M.-P., Carpentier P., Martel A.-C., Bougeard S., Cougoule N., Porta P., Lachaize J., Madec F., Aubert M., Faucon J.-P. Influence of Pesticide Residues on Honey Bee (Hymenoptera: Apidae) Colony Health in France. Environ. Entomol. 2009;38:514–523. doi: 10.1603/022.038.0302. PubMed DOI
Settele J., Bishop J., Potts S.G. Climate Change Impacts on Cold Climates. Treatise Geomorphol. 2016;2:430–459.
Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Predictive markers of honey bee colony collapse. PLoS ONE. 2012;7:e32151. doi: 10.1371/journal.pone.0032151. PubMed DOI PMC
van Dooremalen C., Gerritsen L., Cornelissen B., van der Steen J.J.M., van Langevelde F., Blacquière T. Winter survival of individual honey bees and honey bee colonies depends on level of varroa destructor infestation. PLoS ONE. 2012;7:e36285. doi: 10.1371/journal.pone.0036285. PubMed DOI PMC
Fluri P. Wie alt werden die Arbeitsbienen? Schweiz. Bienen Ztg. 1990;113:620–625.
Mattila H.R., Harris J.L., Otis G.W. Timing of production of winter bees in honey bee (Apis mellifera) colonies. Insectes Soc. 2001;48:88–93. doi: 10.1007/PL00001764. DOI
Seeley T.D., Visscher P.K. Survival of honeybees in cold climates: The critical timing of colony growth and reproduction. Ecol. Entomol. 1985;10:81–88. doi: 10.1111/j.1365-2311.1985.tb00537.x. DOI
Eischen F.A. Overwintering performance of honey bee colonies heavily infested with Acarapis woodi. Apidologie. 1987;18:293–304. doi: 10.1051/apido:19870401. DOI
Bowen-Walker P.L., Martin S.J., Gunn A. Preferential distribution of the parasitic mite, Varroa jacobsoni Oud. on overwintering honeybee (Apis mellifera L.) workers and changes in the level of parasitism. Parasitology. 1997;114:151–157. doi: 10.1017/S0031182096008323. DOI
Guzmán-Novoa E., Eccles L., Calvete Y., Mcgowan J., Kelly P.G., Correa-Benítez A. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie. 2010;41:443–450. doi: 10.1051/apido/2009076. DOI
Highfield A.C., El Nagar A., Mackinder L.C.M., Noël L.M.L.J., Hall M.J., Martin S.J., Schroeder D.C. Deformed wing virus implicated in overwintering honeybee colony losses. Appl. Environ. Microbiol. 2009;75:7212–7220. doi: 10.1128/AEM.02227-09. PubMed DOI PMC
Robinson G.E. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 1992;37:637–665. doi: 10.1146/annurev.en.37.010192.003225. PubMed DOI
Huang Z.Y., Robinson G.E. Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. J. Comp. Physiol. B. 1995;165:18–28. doi: 10.1007/BF00264682. PubMed DOI
Amdam G.V., Aase A.L.T., Seehuus S.C., Fondrk M.K., Norberg K., Hartfelder K. Social reversal of immunosenescence in honey bee workers. Exp. Gerontol. 2005;40:939–947. doi: 10.1016/j.exger.2005.08.004. PubMed DOI PMC
Fluri P., Lüscher M., Wille H., Gerig L. Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees. J. Insect Physiol. 1982;28:61–68. doi: 10.1016/0022-1910(82)90023-3. DOI
Döke M.A., Frazier M., Grozinger C.M. Overwintering honey bees: Biology and management. Curr. Opin. Insect Sci. 2015;10:185–193. doi: 10.1016/j.cois.2015.05.014. PubMed DOI
Fluri P., Wille H., Gerig L., Lüscher M. Juvenile hormone, vitellogenin and haemocyte composition in winter worker honeybees (Apis mellifera) Experientia. 1977;33:1240–1241. doi: 10.1007/BF01922354. DOI
Amdam G.V., Simões Z.L.P., Hagen A., Norberg K., Schrøder K., Mikkelsen Ø., Kirkwood T.B.L., Omholt S.W. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 2004;39:767–773. doi: 10.1016/j.exger.2004.02.010. PubMed DOI
Fluri P., Bogdanov S. Effects of artificial shortening of the photoperiod on honeybee (Apis mellifera) polyethism. J. Apic. Res. 1987;26:83–89. doi: 10.1080/00218839.1987.11100742. DOI
Steinmann N., Corona M., Neumann P., Dainat B. Overwintering is associated with reduced expression of immune genes and higher susceptibility to virus infection in honey bees. PLoS ONE. 2015;10:e0129956. doi: 10.1371/journal.pone.0129956. PubMed DOI PMC
Gätschenberger H., Azzami K., Tautz J., Beier H. Antibacterial Immune Competence of Honey Bees (Apis mellifera) Is Adapted to Different Life Stages and Environmental Risks. PLoS ONE. 2013;8:e66415. doi: 10.1371/journal.pone.0066415. PubMed DOI PMC
Schmid M.R., Brockmann A., Pirk C.W.W., Stanley D.W., Tautz J. Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J. Insect Physiol. 2008;54:439–444. doi: 10.1016/j.jinsphys.2007.11.002. PubMed DOI
Wilson-Rich N., Dres S.T., Starks P.T. The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera) J. Insect Physiol. 2008;54:1392–1399. doi: 10.1016/j.jinsphys.2008.07.016. PubMed DOI
Le Conte Y., Alaux C., Martin J.F., Harbo J.R., Harris J.W., Dantec C., Séverac D., Cros-Arteil S., Navajas M. Social immunity in honeybees (Apis mellifera): Transcriptome analysis of varroa-hygienic behaviour. Insect Mol. Biol. 2011;20:399–408. doi: 10.1111/j.1365-2583.2011.01074.x. PubMed DOI
Simone-Finstrom M., Spivak M. Propolis and bee health: The natural history and significance of resin use by honey bees. Apidologie. 2010;41:295–311. doi: 10.1051/apido/2010016. DOI
Cremer S., Armitage S.A.O., Schmid-Hempel P. Social Immunity. Curr. Biol. 2007;17:693–702. doi: 10.1016/j.cub.2007.06.008. PubMed DOI
Munch D., Kreibich C.D., Amdam G.V. Aging and its modulation in a long-lived worker caste of the honey bee. J. Exp. Biol. 2013;216:1638–1649. doi: 10.1242/jeb.078915. PubMed DOI PMC
Free J.B., Racey P.A. The effect of the size of honeybee colonies on food consumption, brood rearing and the longevity of the bees during winter. Entomol. Exp. Appl. 1968;11:241–249. doi: 10.1111/j.1570-7458.1968.tb02048.x. DOI
Rosenkranz P., Aumeier P., Ziegelmann B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 2010;103:S96–S119. doi: 10.1016/j.jip.2009.07.016. PubMed DOI
Zollner E., Kirs I.K. Uber die quantitative Bestimmung yon Lipoiden (Mikromethode) mittels der vielen natiirliehen Lipoiden (allen bekannten Plasmalipoiden) gemeinsamen Sulfophosphovanillin-Reaktion. Z. Gesamte Exp. Med. 1962;135:545–561. doi: 10.1007/BF02045455. DOI
Kodrík D., Socha R., Šimek P., Zemek R., Goldsworthy G.J. A new member of the AKH/RPCH family that stimulates locomotory activity in the firebug, Pyrrhocoris apterus (Heteroptera) Insect Biochem. Mol. Biol. 2000;30:489–498. doi: 10.1016/S0965-1748(00)00025-4. PubMed DOI
Carroll N., Longley R., Roe J. The Determination of Glycogen in Liver and Muscle by Use of Anthrone Reagent. J. Biol. Chem. 1956;220:583–593. PubMed
Gatschenberger H., Gimple O., Tautz J., Beier H. Honey bee drones maintain humoral immune competence throughout all life stages in the absence of vitellogenin production. J. Exp. Biol. 2012;215:1313–1322. doi: 10.1242/jeb.065276. PubMed DOI
Panzarino O., Hyršl P., Dobeš P., Vojtek L., Vernile P., Bari G., Terzano R., Spagnuolo M., de Lillo E. Rank-based biomarker index to assess cadmium ecotoxicity on the earthworm Eisenia andrei. Chemosphere. 2016;145:480–486. doi: 10.1016/j.chemosphere.2015.11.077. PubMed DOI
Jančaříková G., Houser J., Pavel D., Demo G., Hyršl P., Wimmerová M. Characterization of novel bangle lectin from Photorhabdus asymbiotica with dual sugar-binding specificity and its effect on host immunity. PLoS Pathog. 2017;13:e1006564. doi: 10.1371/journal.ppat.1006564. PubMed DOI PMC
Yang W., Tian Y., Han M., Miao X. Longevity extension of worker honey bees (Apis mellifera) by royal jelly: Optimal dose and active ingredient. PeerJ. 2017;5:e3118. doi: 10.7717/peerj.3118. PubMed DOI PMC
Medina R.G., Paxton R.J., De Luna E., Fleites-Ayil F.A., Medina Medina L.A., Quezada-Euán J.J.G. Developmental stability, age at onset of foraging and longevity of Africanized honey bees (Apis mellifera L.) under heat stress (Hymenoptera: Apidae) J. Therm. Biol. 2018;74:214–225. doi: 10.1016/j.jtherbio.2018.04.003. PubMed DOI
Shehata S.M., Townsend G.F., Shuel R.W. Seasonal Physiological Changes in Queen and Worker Honeybees. J. Apic. Res. 1981;20:69–78. doi: 10.1080/00218839.1981.11100475. DOI
Erler S., Moritz R.F.A. Pharmacophagy and pharmacophory: Mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera) Apidologie. 2016;47:389–411. doi: 10.1007/s13592-015-0400-z. DOI
Frias B.E.D., Barbosa C.D., Lourenço A.P. Pollen nutrition in honey bees (Apis mellifera): Impact on adult health. Apidologie. 2016;47:15–25. doi: 10.1007/s13592-015-0373-y. DOI
Casteels P., Ampe C., Riviere L., van Damme J., Elicon C., Fleming M., Jacobs F., Tempst P. Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera) Eur. J. Biochem. 1990;187:381–386. doi: 10.1111/j.1432-1033.1990.tb15315.x. PubMed DOI
Evans J.D., Aronstein K., Chen Y.P., Hetru C., Imler J.L., Jiang H., Kanosi M., Thompson G.J., Zou Z., Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 2017;15:645–656. doi: 10.1111/j.1365-2583.2006.00682.x. PubMed DOI PMC
Danihlík J., Aronstein K., Petřivalský M. Antimicrobial peptides: A key component of honey bee innate immunity. J. Apic. Res. 2015;54:123–136. doi: 10.1080/00218839.2015.1109919. DOI
Azzami K., Ritter W., Tautz J., Beier H. Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses. Arch. Virol. 2012;157:689–702. doi: 10.1007/s00705-012-1223-0. PubMed DOI PMC
González-Santoyo I., Córdoba-Aguilar A. Phenoloxidase: A key component of the insect immune system. Entomol. Exp. Appl. 2012;142:1–16. doi: 10.1111/j.1570-7458.2011.01187.x. DOI
Lourenço A.P., Zufelato M.S., Gentile Bitondi M.M., Paulino Simões Z.L. Molecular characterization of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. Insect Biochem. Mol. Biol. 2005;35:541–552. doi: 10.1016/j.ibmb.2005.01.013. PubMed DOI
Szymas B., Jedruszuk A. The influence of different diets on haemocytes of adult worker honey bees, Apis mellifera. Apidologie. 2003;34:97–102. doi: 10.1051/apido:2003012. DOI
Segerstrom S.C. Stress, energy, and immunity: An ecological view. Curr. Dir. Psychol. Sci. 2007;16:326–330. doi: 10.1111/j.1467-8721.2007.00522.x. PubMed DOI PMC
Shattuck-Heidorn H., Reiches M.W., Prentice A.M., Moore S.E., Ellison P.T. Energetics and the immune system: Trade-offs associated with non-acute levels of CRP in adolescent Gambian girls. Evol. Med. Public Health. 2017;2017:27–38. doi: 10.1093/emph/eow034. PubMed DOI PMC
Lochmiller R.L., Deerenberg C. Trade-offs in evolutionary immunology: Just what is the cost of immunity? Oikos. 2000;88:87–98. doi: 10.1034/j.1600-0706.2000.880110.x. DOI
Wheeler D.E., Kawooya J.K. Purification and characterization of honey bee vitellogenin. Arch. Insect Biochem. Physiol. 1990;14:253–267. doi: 10.1002/arch.940140405. PubMed DOI
Seehuus S.-C., Norberg K., Krekling T., Fondrk K., Amdam G.V. Immunogold Localization of Vitellogenin in the Ovaries, Hypopharyngeal Glands and Head Fat Bodies of Honeybee Workers, Apis mellifera. J. Insect Sci. 2009;7:52. doi: 10.1673/031.007.5201. PubMed DOI PMC
Amdam G.V., Norberg K., Omholt S.W., Kryger P., Lourenço A.P., Bitondi M.M.G., Simões Z.L.P. Higher vitellogenin concentrations in honey bee workers may be an adaptation to life in temperate climates. Insectes Soc. 2005;52:316–319. doi: 10.1007/s00040-005-0812-2. DOI
Aurori C.M., Buttstedt A., Dezmirean D.S., Mărghitaş L.A., Moritz R.F.A., Erler S. What is the main driver of ageing in long-lived winter honeybees: Antioxidant enzymes, innate immunity, or vitellogenin? J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2014;69:633–639. doi: 10.1093/gerona/glt134. PubMed DOI
Corona M., Velarde R.A., Remolina S., Moran-Lauter A., Wang Y., Hughes K.A., Robinson G.E. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA. 2007;104:7128–7133. doi: 10.1073/pnas.0701909104. PubMed DOI PMC
Pinto L.Z., Bitondi M.M.G., Simões Z.L.P. Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen. J. Insect Physiol. 2000;46:153–160. doi: 10.1016/S0022-1910(99)00111-0. PubMed DOI
Cardoso-Júnior C.A., Guidugli-Lazzarini K.R., Hartfelder K. DNA methylation affects the lifespan of honey bee (Apis mellifera L.) workers—Evidence for a regulatory module that involves vitellogenin expression but is independent of juvenile hormone function. Insect Biochem. Mol. Biol. 2018;92:21–29. doi: 10.1016/j.ibmb.2017.11.005. PubMed DOI
Amdam G.V., Norberg K., Hagen A., Omholt S.W. Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. USA. 2003;100:1799–1802. doi: 10.1073/pnas.0333979100. PubMed DOI PMC
Trenczek T., Engels W. Occurrence of vitellogenin in drone honeybees (Apis mellifica) Int. J. Invertebr. Reprod. Dev. 1986;10:307–311. doi: 10.1080/01688170.1986.10510254. DOI
Trenczek T., Zillikens A., Engels W. Developmental patterns of vitellogenin haemolymph titre and rate of synthesis in adult drone honey bees (Apis mellifera) J. Insect Physiol. 1989;35:475–481. doi: 10.1016/0022-1910(89)90054-1. DOI
Piulachs M.D., Guidugli K.R., Barchuk A.R., Cruz J., Simões Z.L.P., Bellés X. The vitellogenin of the honey bee, Apis mellifera: Structural analysis of the cDNA and expression studies. Insect Biochem. Mol. Biol. 2003;33:459–465. doi: 10.1016/S0965-1748(03)00021-3. PubMed DOI
Kunert K., Crailsheim K. Seasonal changes in carbohydrate, lipid and protein content in emerging worker honeybees and their mortality. J. Apic. Res. 1988;27:13–21. doi: 10.1080/00218839.1988.11100775. DOI
Amdam G.V., Omholt S.W. The regulatory anatomy of honeybee lifespan. J. Theor. Biol. 2002;216:209–228. doi: 10.1006/jtbi.2002.2545. PubMed DOI
De Souza D.A., Kaftanoglu O., De Jong D., Page R.E., Amdam G.V., Wang Y. Differences in the morphology, physiology and gene expression of honey bee queens and workers reared in vitro versus in situ. Biol. Open. 2018;7:bio036616. doi: 10.1242/bio.036616. PubMed DOI PMC
Otis G., Wheeler D.E., Buck N.A., Mattila H.R. Storage proteins in winter honey bees. APIACATA. 2004;38:352–357.
Switanek M., Crailsheim K., Truhetz H., Brodschneider R. Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci. Total Environ. 2017;579:1581–1587. doi: 10.1016/j.scitotenv.2016.11.178. PubMed DOI
Nielsen A., Reitan T., Rinvoll A.W., Brysting A.K. Effects of competition and climate on a crop pollinator community. Agric. Ecosyst. Environ. 2017;246:253–260. doi: 10.1016/j.agee.2017.06.006. DOI
Dalmon A., Peruzzi M., Le Conte Y., Alaux C., Pioz M. Temperature-driven changes in viral loads in the honey bee Apis mellifera. J. Invertebr. Pathol. 2019;160:87–94. doi: 10.1016/j.jip.2018.12.005. PubMed DOI
Huang Z. Pollen nutrition affects honey bee stress resistance. Terr. Arthropod Rev. 2012;5:175–189. doi: 10.1163/187498312X639568. DOI
Fine J.D., Shpigler H.Y., Ray A.M., Beach N.J., Sankey A.L., Ahmed-Casch A., Huang Z.Y., Astrauskaite I., Chao R., Zhao H., et al. Quantifying the effects of pollen nutrition on honey bee queen egg laying with a new laboratory system. PLoS ONE. 2018;13:e0203444. doi: 10.1371/journal.pone.0203444. PubMed DOI PMC
Nürnberger F., Härtel S., Steffan-Dewenter I. The influence of temperature and photoperiod on the timing of brood onset in hibernating honey bee colonies. PeerJ. 2018;6:e4801. doi: 10.7717/peerj.4801. PubMed DOI PMC
Medrzycki P., Sgolastra F., Bortolotti L., Bogo G., Tosi S., Padovani E., Porrini C., Sabatini A.G. Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides. J. Apic. Res. 2010;49:52–59. doi: 10.3896/IBRA.1.49.1.07. DOI
Inouye D.W. Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology. 2008;89:353–362. doi: 10.1890/06-2128.1. PubMed DOI
Williams C.M., Henry H.A.L., Sinclair B.J. Cold truths: How winter drives responses of terrestrial organisms to climate change. Biol. Rev. 2015;90:214–235. doi: 10.1111/brv.12105. PubMed DOI
Schenk M., Krauss J., Holzschuh A. Desynchronizations in bee–plant interactions cause severe fitness losses in solitary bees. J. Anim. Ecol. 2018;87:139–149. doi: 10.1111/1365-2656.12694. PubMed DOI
Langowska A., Zawilak M., Sparks T.H., Glazaczow A., Tomkins P.W., Tryjanowski P. Long-term effect of temperature on honey yield and honeybee phenology. Int. J. Biometeorol. 2017;61:1125–1132. doi: 10.1007/s00484-016-1293-x. PubMed DOI PMC
Phytochemical S-methyl-L-cysteine sulfoxide from Brassicaceae: a key to health or a poison for bees?
Unusual functions of insect vitellogenins: minireview
1H NMR Profiling of Honey Bee Bodies Revealed Metabolic Differences between Summer and Winter Bees
The Effect of Foraging on Bumble Bees, Bombus terrestris, Reared under Laboratory Conditions
