475
Views
0
CrossRef citations to date
0
Altmetric
Original research article

Standard methods to estimate strength parameters, flight activity, comb construction, and fitness of Apis mellifera colonies 2.0

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon show all
Received 09 May 2022, Accepted 27 Jan 2024, Published online: 13 May 2024

References

  • Adafruit Industries (n.d.). Retrieved November 1, 2021, from https://www.adafruit.com/
  • Alves, T. S., Pinto, M. A., Ventura, P., Neves, C. J., Biron, D. G., Junior, A. C., DE Paula Filho, P. L., & Rodrigues, P. J. (2020). Automatic detection and classification of honey bee comb cells using deep learning. Computers and Electronics in Agriculture, 170, 105244. https://doi.org/10.1016/j.compag.2020.105244
  • Berry, J. A., & Delaplane, K. S. (2001). Effects of comb age on honey bee colony growth, brood survivorship, and adult mortality. Journal of Apicultural Research, 40(1), 3–8. https://doi.org/10.1080/00218839.2001.11101042
  • Berry, J. A., Owens, W. B., & Delaplane, K. S. (2010). Small-cell comb foundation does not impede varroa mite population growth in honey bee colonies. Apidologie, 41(1), 40–44. https://doi.org/10.1051/apido/2009049
  • Boze, A. (2001). IrfanView 3.36. Information Technology and Libraries, 20, 162–162. Retrieved November 1, 2021, from https://www.irfanview.com/
  • Bradski, G. (2000). The OpenCV Library. Dr. Dobb’s Journal of Software Tools. Retrieved November 1, 2021, from https://opencv.org/
  • Bromenshenk, J. (2015). Infrared: The next generation in colony management. Bee Culture, 143, 1–9. https://www.beeculture.com/infrared-the-next-generation-in-colony-management/
  • Buco, S. M., Rinderer, T. E., Sylvester, H. A., Collins, A. M., Lancaster, V. A., Crewe, R. M., Davis, G. L., & Winfrey, D. (1987). Morphometric differences between South American Africanized and South African (Apis mellifera scutellata) honey bees. Apidologie, 18(3), 217–222. https://doi.org/10.1051/apido:19870301
  • Budge, G. E., Pietravalle, S., Brown, M., Laurenson, L., Jones, B., Tomkies, V., & Delaplane, K. S. (2015). Pathogens as predictors of honey bee colony strength in England and Wales. PLOS One, 10(7), e0133228. https://doi.org/10.1371/journal.pone.0133228
  • Burgett, M., & Burikam, I. (1985). Number of adult honey bees (Hymenoptera: Apidae) occupying a comb: A standard for estimating colony populations. Journal of Economic Entomology, 78(5), 1154–1156. https://doi.org/10.1093/jee/78.5.1154
  • Campbell, J., Mummert, L., & Sukthankar, R. (2008). Video monitoring of honey bee colonies at the hive entrance. Visual Observation & Analysis of Animal & Insect Behavior, ICPR, 8, 1–4.
  • Chabert, S., Requier, F., Chadoeuf, J., Guilbaud, L., Morison, N., & Vaissière, B. E. (2021). Rapid measurement of the adult worker population size in honey bees. Ecological Indicators, 122, 107313. https://doi.org/10.1016/j.ecolind.2020.107313
  • Cobey, S. W., Tarpy, D. R., & Woyke, J. (2013). Standard methods for instrumental insemination of Apis mellifera queens. Journal of Apicultural Research, 52(4), 1–18. https://doi.org/10.3896/IBRA.1.52.4.09
  • Colin, T., Bruce, J., Meikle, W. G., & Barron, A. B. (2018). The development of honey bee colonies assessed using a new semi-automated brood counting method: CombCount. PLOS One, 13(10), e0205816. https://doi.org/10.1371/journal.pone.0205816
  • Cornelissen, B., Blacquière, T., & VAN DER Steen, J. (2009). Estimating honey bee colony size using digital photography. In Proceedings of 41st International Apicultural Congress (p. 48).
  • Cunha, A. S., Rose, J., Prior, J., Aumann, H. M., Emanetoglu, N. W., & Drummond, F. A. (2020). A novel non-invasive radar to monitor honey bee colony health. Computers and Electronics in Agriculture, 170, 105241. https://doi.org/10.1016/j.compag.2020.105241
  • Dadant, H. C. (1963). Beekeeping equipment. In R. A. Grout (Ed.), The hive and the honey bee (pp. 219–240). Dadant & Sons.
  • Dainat, B., Dietemann, V., Imdorf, A., & Charrière, J.-D. (2020). A scientific note on the ‘Liebefeld Method’ to estimate honey bee colony strength: Its history, use, and translation. Apidologie, 51(3), 422–427. https://doi.org/10.1007/s13592-019-00728-2
  • Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012). Predictive markers of honey bee colony collapse. PLOS One, 7(2), e32151. https://doi.org/10.1371/journal.pone.0032151
  • de Graaf, D. C., Alippi, A. M., Antúnez, K., Aronstein, K. A., Budge, G., De Koker, D., De Smet, L., Dingman, D. W., Evans, J. D., Foster, L. J., Fünfhaus, A., Garcia-Gonzalez, E., Gregore, A., Human, H., Murray, K. D., Nguyen, B. K., Poppinga, L., Spivak, M., van Engelsdorp, D., Wilkins, S., & Genersch, E. (2013). Standard methods for American foulbrood research. Journal of Apicultural Research, 52(1), 1–28. https://doi.org/10.3896/IBRA.1.52.1.11
  • De la Mora, A., Emsen, B., Morfin, N., Borges, D., Eccles, L., Kelly, P. G., Goodwin, P. H., & Guzman-Novoa, E. (2020). Selective breeding for low and high Varroa destructor growth in honey bee (Apis mellifera) colonies: Initial results of two generations. Insects, 11(12), 864. https://doi.org/10.3390/insects11120864
  • de Miranda, J. R., Bailey, L., Ball, B. V., Blanchard, P., Budge, G. E., Chejanovsky, N., Chen, Y.-P., Gauthier, L., Genersch, E., de Graaf, D. C., Ribière, M., Ryabov, E., De Smet, L., & van der Steen, J. J. M. (2013). Standard methods for virus research in Apis mellifera. Journal of Apicultural Research, 52(4), 1–56. https://doi.org/10.3896/IBRA.1.52.4.22
  • Delaplane, K. S., & Harbo, J. R. (1987). Effect of queenlessness on worker survival, honey gain and defence behaviour in honey bees. Journal of Apicultural Research, 26(1), 37–42. https://doi.org/10.1080/00218839.1987.11100732
  • Delaplane, K. S., & Hood, W. M. (1997). Effects of delayed acaricide treatment in honey bee colonies parasitized by Varroa jacobsoni and a late season treatment threshold for the South-eastern United States. Journal of Apicultural Research, 36(3–4), 125–132. https://doi.org/10.1080/00218839.1997.11100938
  • Delaplane, K. S., & Hood, W. M. (1999). Economic threshold for Varroa jacobsoni Oud. in the South-eastern USA. Apidologie, 30(5), 383–395. https://doi.org/10.1051/apido:19990504
  • Delaplane, K. S., Berry, J. A., Skinner, J. A., Parkman, J. P., & Hood, W. M. (2005). Integrated pest management against Varroa destructor reduces colony mite levels and delays economic threshold. Journal of Apicultural Research, 44(4), 157–162. https://doi.org/10.1080/00218839.2005.11101171
  • Delaplane, K. S., Dag, A., Danka, R. G., Freitas, B. M., Garibaldi, L. A., Goodwin, R. M., & Hormaza, J. I. (2013). Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research, 52(4), 1–28. https://doi.org/10.3896/IBRA/1.52.1.03
  • Delaplane, K. S., Ellis, J. D., & Hood, W. M. (2010). A test for interactions between Varroa destructor (Acari: Varroidae) and Aethina tumida (Coleoptera: Nitidulidae) in colonies of honey bees (Hymenoptera: Apidae). Annals of the Entomological Society of America, 103(5), 711–715. https://doi.org/10.1603/AN09169
  • Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., & Ellis, J. D. (2013). Standard methods for varroa research. Journal of Apicultural Research, 52(1), 1–54. https://doi.org/10.3896/IBRA.1.52.1.09
  • Ducsharm, K., & Eccles, L. (2019). Low-cost infrared thermal imaging technology as a risk management tool. Ontario Bee Journal, 38, 14–17.
  • Dynes, T. L., Berry, J. A., Delaplane, K. S., Brosi, B. J., & DE Roode, J. C. (2019). Reduced density and visually complex apiaries reduce parasite load and promote honey production and overwintering survival in honey bees. PLOS One, 14(5), e0216286. https://doi.org/10.1371/journal.pone.0216286
  • Ellis, J. D., Delaplane, K. S., & Hood, W. M. (2001). Efficacy of a bottom screen device, Apistan, and Apilife VAR in controlling Varroa destructor. American Bee Journal, 141, 813–816.
  • Faulkner, A. L., & Chavez, C. (2017). Adobe photoshop CC classroom in a book: The official training workbook from adobe (2018 Release). Adobe Press.
  • Forsgren, E., Budge, G. E., Charrière, J. D., & Hornitzky, M. A. (2013). Standard methods for European foulbrood research. Journal of Apicultural Research, 52(1), 1–14. https://doi.org/10.3896/IBRA.1.52.1.12
  • Giray, T. G.-N. E., Aron, C. W., Zelinsky, B., Fahrbach, S. E., & Robinson, G. E. (2000). Genetic variation in worker temporal polyethism and colony defensiveness in the honey bee, Apis mellifera. Behavioral Ecology, 11(1), 44–55. https://doi.org/10.1093/beheco/11.1.44
  • Greco, M. K. (2010). Imaging techniques for improved bee management. ALP Technical-Scientific Information Series, 534, 38.
  • Gris, A. (2002). Efecto de las diferencias en población entre colonias de abejas (Apis mellifera L.) con una y dos reinas en el comportamiento productivo y de pecoreo de sus obreras [MSc thesis]. National University of Mexico.
  • Guzman-Novoa, E. (2007). Elemental genetics and breeding for the honey bee. University of Guelph. Aylmer Press.
  • Guzman-Novoa, E., Correa-Benítez, A., Montaño, L. G. E., & Guzmán-Novoa, G. (2011). Colonization, impact, and control of Africanized honey bees in Mexico. Revista Veterinaria México, 42(2), 149–178.
  • Guzman-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P. G., & Correa-Benítez, A. (2010). Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie, 41(4), 443–450. https://doi.org/10.1051/apido/2009076
  • Guzman-Novoa, E., Hunt, G. J., Page, J. R. R. E., & Fondrk, M. K. (2002). Genetic correlations among honey bee (Hymenoptera: Apidae) behavioral characteristics and wing length. Annals of the Entomological Society of America, 95(3), 402–406. https://doi.org/10.1603/0013-8746(2002)095[0402:GCAHBH]2.0.CO;2
  • Guzman-Novoa, E., Morfin, N., De la Mora, A., Macías-Macías, J. O., Tapia-González, J. M., Contreras-Escareño, F., Medina-Flores, C. A., Correa-Benítez, A., & Quezada-Euán, J. J. G. (2020). The process and outcome of the Africanization of honey bees in Mexico: Lessons and future directions. Frontiers in Ecology and Evolution, 8, 608091. https://doi.org/10.3389/fevo.2020.608091
  • Harbo, J. R. (1983). Effect of population size on worker survival and honey loss in broodless colonies of honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environmental Entomology, 12(5), 1559–1563. https://doi.org/10.1093/ee/12.5.1559
  • Harbo, J. R. (1986). Effect of population size on brood production, worker survival and honey gain in colonies of honey bees. Journal of Apicultural Research, 25(1), 22–29. https://doi.org/10.1080/00218839.1986.11100687
  • Harbo, J. R. (1988). Effect of comb size on population growth of honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology, 81(6), 1606–1610. https://doi.org/10.1093/jee/81.6.1606
  • Harbo, J. R. (1993). Worker-bee crowding affects brood production, honey production, and longevity of honey bees (Hymenoptera: Apidae). Journal of Economic Entomology, 86(6), 1672–1678. https://doi.org/10.1093/jee/86.6.1672
  • Hepburn, H. R. (1983). Comb construction by the African honey bee, Apis mellifera adansonii. Journal of the Entomological Society of South Africa, 46, 87–101.
  • Hernandez, J., Maisonnasse, A., Cousin, M., Beri, C., Le Quintrec, C., Bouetard, A., Castex, D., Decante, D., Servel, E., Buchwalder, G., Brunet, F., Feschet-Destrella, E., DE Bellescize, K., Kairo, G., Frontero, L., Pédehontaa-Hiaa, M., Buisson, R., Pouderoux, T., Aebi, A., & Kretzschmar, A. (2020). ColEval: Honey bee COLony Structure EVALuation for field surveys. Insects, 11(1), 41. https://doi.org/10.3390/insects11010041
  • Human, H., Brodschneider, R., Dietemann, V., Dively, G., Ellis, J. D., Forsgren, E., Fries, I., Hatjina, F., Hu, F.-L., Jaffé, R., Jensen, A. B., Köhler, A., Magyar, J. P., Özkýrým, A., Pirk, C. W. W., Rose, R., Strauss, U., Tanner, G., Tarpy, D. R., … Zheng, H.-Q. (2013). Miscellaneous standard methods for Apis mellifera research. Journal of Apicultural Research, 52(4), 1–53. https://doi.org/10.3896/IBRA.1.52.4.10
  • Imdorf, A., & Gerig, L. (2001). Course in determination of colony strength. Swiss Federal Dairy Research Institute, Liebefeld CH-3003 Bern Switzerland (after L Gerig, 1983. Lehrgang zur Erfassung der Volksstärke). Schweiz Bienen-Zeitung, 106, 199–204.
  • Imdorf, A., Buehlmann, G., Gerig, L., Kilchenmann, V., & Wille, H. (1987). Überprüfung der Schätzmethode zur ermittlung der Brutfläche und der anzahl Arbeiterinnen in freifliegenden Bienenvölkern. Apidologie, 18(2), 137–146. https://doi.org/10.1051/apido:19870204
  • Jeker, L., Schmid, L., Meschberger, T., Candolfi, M., Pudenz, S., & Magyar, J. P. (2012). Computer-assisted digital image analysis and evaluation of brood development in honey bee combs. Journal of Apicultural Research, 51(1), 63–73. https://doi.org/10.3896/IBRA.1.51.1.08
  • Jensen, A. B., Aronstein, K., Flores, J. M., Vojvodic, S., Palacio, M. A., & Spivak, M. (2013). Standard methods for fungal brood disease research. Journal of Apicultural Research, 52(1), 1–20. https://doi.org/10.3896/IBRA.1.52.1.13
  • Jevtić, G., Mladenović, M., Andjelković, B., Nedić, N., Sokolović, D., & Štrbanović, R. (2009). The correlation between colony strength, food supply and honey yield in honey bee colonies. Biotechnology in Animal Husbandry, 25(5-6-2), 1141–1147.
  • Kale, D. J., Tashakkori, R., & Parry, R. M. (2015). Automated beehive surveillance using computer vision. IEEE SoutheastCon (pp. 1–3). https://doi.org/10.1109/SECON.2015.7132991
  • Khoury, D. S., Barron, A. B., & Myerscough, M. R. (2013). Modelling food and population dynamics in honey bee colonies. PLOS One, 8(5), e59084. https://doi.org/10.1371/journal.pone.0059084
  • Lecocq, A., Kryger, P., Vejsnæs, F., & Bruun Jensen, A. (2015). Weight watching and the effect of landscape on honey bee colony productivity: Investigating the value of colony weight monitoring for the beekeeping industry. PLOS One, 10(7), e0132473. https://doi.org/10.1371/journal.pone.0132473
  • Lee, K. V., Goblirsch, M., Mcdermott, E., Tarpy, D. R., & Spivak, M. (2019). Is the brood pattern within a honey bee colony a reliable indicator of queen quality? Insects, 10(1), 12. https://doi.org/10.3390/insects10010012
  • Lee, P. C., & Winston, M. L. (1987). Effects of reproductive timing and colony size on the survival, offspring colony size and drone production in the honey bee (Apis mellifera). Ecological Entomology, 12(2), 187–195. https://doi.org/10.1111/j.1365-2311.1987.tb00997.x
  • Lozano, A., Hernando, M. D., Uclés, S., Hakme, E., & Fernández-Alba, A. R. (2019). Identification and measurement of veterinary drug residues in beehive products. Food Chemistry, 274, 61–70. https://doi.org/10.1016/j.foodchem.2018.08.055
  • MATLAB (2010). MATLAB version 7.10.0 (R2010a). The MathWorks Inc. Retrieved November 1, 2021, from https://www.mathworks.com/products/matlab.html
  • Mattila, H. R., & Seeley, T. D. (2007). Genetic diversity in honey bee colonies enhances productivity and fitness. Science, 317(5836), 362–364. https://doi.org/10.1126/science.1143046
  • Mayack, C., & Naug, D. (2009). Energetic stress in the honey bee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology, 100(3), 185–188. https://doi.org/10.1016/j.jip.2008.12.001
  • Meikle, W. G., Holst, N., Colin, T., Weiss, M., Carroll, M. J., Mcfrederick, Q. S., & Barron, A. B. (2018). Using within-day hive weight changes to measure environmental effects on honey bee colonies. PLOS One, 13(5), e0197589. 23 https://doi.org/10.1371/journal.pone.0197589
  • Microchip Technology (2021). ATSAMD21G18A. Retrieved November 1, 2021, from https://www.digikey.ca/en/supplier-centers/microchip-technology
  • Microsoft Corporation (2018). Microsoft Excel. Retrieved November 1, 2021, from https://office.microsoft.com/excel
  • Mid-Atlantic Apiculture Research and Extension Consortium (n.d.). Package bees. Retrieved December 2, 2021, from https://canr.udel.edu/maarec/package-bees/
  • Morales, M. M., Ramos, M. J. G., Vázquez, P. P., Galiano, F. J. D., Valverde, M. G., López, V. G., Flores, J. M., & Fernández-Alba, A. R. (2020). Distribution of chemical residues in the beehive compartments and their transfer to the honey bee brood. Science of the Total Environment, 710, 136288. https://doi.org/10.1016/j.scitotenv.2019.136288
  • Nightingale, J. M., Esaias, W. E., Wolfe, R. E., Nickeson, J. E., & Ma, P. L. A. (2008). Assessing honey bee equilibrium range and forage supply using satellite-derived phenology. In IGARSS 2008 – 2008 IEEE International Geoscience and Remote Sensing Symposium, Boston, MA (pp. III-763–III-766). https://doi.org/10.1109/IGARSS.2008.4779460
  • Odemer, R. (2021). Approaches, challenges and recent advances in automated bee counting devices: A review. Annals of Applied Biology, 180(1), 73–89. https://doi.org/10.1111/aab.12727
  • Odoux, J.-F., Aupinel, P., Gateff, S., Requier, F., Henry, M., & Bretagnolle, V. (2014). ECOBEE: A tool for long-term honey bee colony monitoring at the landscape scale in West European intensive agroecosystems. Journal of Apicultural Research, 53(1), 57–66. https://doi.org/10.3896/IBRA.1.53.1.05
  • Organism for Economic Cooperation and Development (2007). Guidance document on the honey bee (Apis mellifera L.) brood test under semi-field conditions. In Series on testing and assessment, guidance document on the honey bee (Apis mellifera) brood test under semi-field conditions. OECD Publishing. Retrieved July 24, 2023, from https://doi.org/10.1787/9789264085510-en
  • Russell, S., Barron, A. B., & Harris, D. (2013). Dynamic modelling of honey bee (Apis mellifera) colony growth and failure. Ecological Modelling, 265, 158–169. https://doi.org/10.1016/j.ecolmodel.2013.06.005
  • Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675. https://doi.org/10.1038/nmeth.208
  • Shaw, J. A., Nugent, P. W., Johnson, J., Bromenshenk, J. J., Henderson, C. B., & Debnam, S. (2011). Long-wave infrared imaging for non-invasive beehive population assessment. Optics Express, 19(1), 399–408. https://doi.org/10.1364/OE.19.000399
  • Sinia, A., & Guzman-Novoa, E. (2018). Evaluation of the entomopathogenic fungi Beauveria bassiana GHA and Metarhizium anisopliae UAMH 9198 alone or in combination with thymol for the control of Varroa destructor in honey bee (Apis mellifera) colonies. Journal of Apicultural Research, 57(2), 308–316. https://doi.org/10.1080/00218839.2018.1430983
  • Skinner, J. J., Parkman, J. P., & Studer, M. D. (2001). Evaluation of honey bee miticides, including temporal and thermal effects on formic acid gel vapours, in the central south-eastern USA. Journal of Apicultural Research, 40(3–4), 81–89. https://doi.org/10.1080/00218839.2001.11101055
  • Smith, M. L., Ostwald, M. M., Loftus, J. C., & Seeley, T. D. (2014). A critical number of workers in a honey bee colony triggers investment in reproduction. Die Naturwissenschaften, 101(10), 783–790. https://doi.org/10.1007/s00114-014-1215-x
  • Strange, J. P., & Sheppard, W. S. (2001). Optimum timing of miticide applications for control of Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) in Washington state, USA. Journal of Economic Entomology, 94(6), 1324–1331. https://doi.org/10.1603/0022-0493-94.6.1324
  • Struye, M. H., Mortier, H. J., Arnold, G., Miniggio, C., & Borneck, R. (1994). Microprocessor-controlled monitoring of honey bee flight activity at the hive entrance. Apidologie, 25(4), 384–395. https://doi.org/10.1051/apido:19940405
  • Szabo, T. I. (1977). Effect of colony size and ambient temperature on comb building and sugar consumption by honey bees. Journal of Apicultural Research, 16(4), 174–183. https://doi.org/10.1080/00218839.1977.11099884
  • Taha, E. K. A. (2014). Seasonal variation of foraging activity, pollen collection and growth of honey bee colonies in Al-Ahsa, Saudi Arabia. Bulletin of the Entomological Society of Egypt, 91, 163–175.
  • Tashakkori, R., & Ghadiri, A. (2015, April 1–7). Image processing for honey bee hive health monitoring. SoutheastCon 2015, Fort Lauderdale FL, USA. IEEE. https://doi.org/10.1109/SECON.2015.7133029
  • Tashakkori, R., Hamza, A. S., & Crawford, M. B. (2021). Beemon: An IoT-based beehive monitoring system. Computers and Electronics in Agriculture, 190, 106427. https://doi.org/10.1016/j.compag.2021.106427
  • Torres, D. J., Ricoy, U. M., & Roybal, S. (2015). Modeling honey bee populations. PLOS One, 10(7), e0130966. https://doi.org/10.1371/journal.pone.0130966
  • UNIBRAIN (2021). Retrieved November 1, 2021, fom https://www.unibrain.com/products/fire-i-digital-camera/
  • van Dooremalen, C., Cornelissen, B., Poleij-Hok-Ahin, C., & Blacquière, T. (2018). Single and interactive effects of Varroa destructor, Nosema spp., and imidacloprid on honey bee colonies (Apis mellifera). Ecosphere, 9(8), e02378. https://doi.org/10.1002/ecs2.2378
  • WSC Regexpert (2021). Software for honey bee trials. Retrieved May 22, 2023, from https://wsc-regexperts.com/en/software-and-databases/software/honeybee-brood-colony-assessment-software/
  • Yoshiyama, M., Kimura, K., Saitoh, K., & Iwata, H. (2011). Measuring colony development in honey bees by simple digital analysis. Journal of Apicultural Research, 50(2), 170–172. https://doi.org/10.3896/IBRA.1.50.2.109

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.