Honeybee nutrition is linked to landscape composition

Ecology and Evolution

Volumn 4, Issue 21, 2014, Pages 4195-4206

  Donkersley, Philip ^a   Rhodes, Glenn ^b   Pickup, Roger W ^c   Jones, Kevin C ^a   Wilson, Kenneth ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Apis mellifera; Beebread; Carbohydrate; Countryside Survey; Land use; Nutritional ecology; Protein

Indexed keywords

APIS MELLIFERA; APOIDEA; HEXAPODA; INVERTEBRATA;

EID: 84927694421     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1293     Document Type: Article

References (74)

1. Alaux, C., F. Ducloz, D. Crauser, and Y. Le Conte . 2010. Diet effects on honeybee immunocompetence. Biol. Lett. 6:562-565.
2. Altaye, S. Z., C. W. W. Pirk, R. M. Crewe, and S. W. Nicolson . 2010. Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. J. Exp. Biol. 213:3311-3318.
3. Baayen, R. H. 2007. Analyzing Linguistic Data: a practical introduction to statistics using R. Cambridge Univ. Press, Cambridge.
4. Bates, A. J., J. P. Sadler, A. J. Fairbrass, S. J. Falk, J. D. Hale, and T. J. Matthews . 2011. Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS ONE 6:e23459.
5. Bates, D., M. Maechler, and B. Bolker . 2012. lme4: Linear mixed-effects models using S4 classes. Available via http://lme4.r-forge.r-project.org/.
6. Beckerman, A., O. L. Petchey, and P. J. Morin . 2010. Adaptive foragers and community ecology: linking individuals to communities and ecosystems. Funct. Ecol. 24:1-6.
7. Beekman, M., and F. L. W. Ratnieks . 2000. Long-range foraging by the honey-bee, Apis mellifera L. Funct. Ecol. 14:490-496.
8. Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. H. Stevens, et al. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24:127-135.
9. Breeze, T. D., B. E. Vaissière, R. Bommarco, T. Petanidou, N. Seraphides, L. Kozák, et al. 2014. Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS ONE 9:e82996.
10. Brodschneider, R., and K. Crailsheim . 2010. Nutrition and health in honey bees. Apidologie 41:278-294.
11. Buchmann, S. I. 1986. Vibratile pollination in Solanum and Lycopersicon: a look at pollen chemistry. Pp. 237-252 in W. G. D'Arcy, ed. Solanaceae II: biology and systematics. Columbus Univ. Press, New York, NY.
12. Capri, E., and A. Marchis . 2013. Bee health in Europe - Facts & figures 2013. OPERA Research Centre, Universita Cattolica del Sacro Cuore, Piacenza, Italy.
13. Cheng, Y.-S., Y. Zheng, and J. Van der Gheynst . 2011. Rapid quantitative analysis of lipids using a colorimetric method in a microplate format. Lipids 46:95-103.
14. Cook, S. M., C. S. Awmack, D. A. Murray, and I. H. Williams . 2003. Are honey bees' foraging preferences affected by pollen amino acid composition? Ecol. Entomol. 28:622-627.
15. Cotter, S. C., S. J. Simpson, D. Raubenheimer, and K. Wilson . 2010. Macronutrient balance mediates trade-offs between immune function and life history traits. Funct. Ecol. 25:186-198.
16. Crailsheim, K., and E. Stolberg . 1989. Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L.). J. Insect Physiol. 35:595-602.
17. DeGrandi-Hoffman, G., Y. P. Chen, E. Huang, and M. H. Huang . 2010. The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). J. Insect Physiol. 56:1184-1191.
18. DeGrandi-Hoffman, G., B. Eckholm, and M. Huang . 2013. A comparison of bee bread made by Africanized and European honey bees (Apis mellifera) and its effects on hemolymph protein titers. Apidologie 44:52-63.
19. Dussutour, A., and S. J. Simpson . 2009. Communal nutrition in ants. Curr. Biol. 19:740-744.
20. Dussutour, A., and S. J. Simpson . 2012. Ant workers die young and colonies collapse when fed a high-protein diet. Proc. R. Soc. B Biol. Sci. 279:2402-2408.
21. Gallai, N., J.-M. Salles, J. Settele, and B. E. Vaissière . 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68:810-821.
22. Herbert, E. W., and H. Shimanuki . 1978. Chemical composition and nutritive-value of bee-collected and bee-stored pollen. Apidologie 9:33-40.
23. Hope, D., C. Gries, W. X. Zhu, W. F. Fagan, C. L. Redman, N. B. Grimm, et al. 2003. Socioeconomics drive urban plant diversity. Proc. Natl Acad. Sci. U.S.A. 100:8788-8792.
24. Jones, E. L., and S. R. Leather . 2012. Invertebrates in urban areas: a review. Eur. J. Entomol. 109:463-478.
25. Keller, I., P. Fluri, and A. Imdorf . 2005. Pollen nutrition and colony development in honey bees - Part II. Bee World 86:27-34.
26. Kleijn, D., and F. van Langevelde . 2006. Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes. Basic Appl. Ecol. 7:201-214.
27. Kleijn, D., R. A. Baquero, Y. Clough, M. Diaz, J. De Esteban, F. Fernandez, et al. 2006. Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol. Lett. 9:243-254.
28. Klein, A.-M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham, C. Kremen, et al. 2007. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274:303-313.
29. Lee, K. P., J. S. Cory, K. Wilson, D. Raubenheimer, and S. J. Simpson . 2006. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. B Biol. Sci. 273:823-829.
30. Lee, K. P., S. J. Simpson, F. J. Clissold, R. Brooks, J. W. O. Ballard, P. W. Taylor, et al. 2008. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc. Natl Acad. Sci. USA. 105:2498-2503.
31. Lees, R. 1971. Laboratory handbooks of methods of food analysis. 2nd ed. Leonard Hill, London.
32. Lussenhop, J. 1977. Urban cemeteries as bird refuges. Condor 79:456-461.
33. Marie-Pierre, C., L. Marion, R. Marie-Pierre, S. Cécile, H. Pascal, and R. C. Magali . 2014. A pan-European epidemiological study on honeybee colony losses 2012-2013. European Union Reference Laboratory for honeybee health (EURL), Anses Honeybee pathology Unit, Sophia Antipolis, France.
34. Martin, S. J., A. C. Highfield, L. Brettell, E. M. Villalobos, G. E. Budge, M. Powell, et al. 2012. Global honey bee viral landscape altered by a parasitic mite. Science 336:1304-1306.
35. McCleary, B. V., V. Solah, and T. S. Gibson . 1994. Quantitative measurement of total starch in cereal flours and products. J. Cereal Sci. 20:51-58.
36. Megazyme. 2006. Total starch assay procedure: (AA/AMG 11/01). Megazyme International Ireland Ltd.; Bray Business Park, Bray, Ireland.
37. Morais, M. M., A. P. Turcatto, R. A. Pereira, T. M. Francoy, K. R. Guidugli-Lazzarini, L. S. Goncalves, et al. 2013. Protein levels and colony development of Africanized and European honey bees fed natural and artificial diets. Genet. Mol. Res. 12:6915-6922.
38. Morgano, M. A., M. C. T. Martins, L. C. Rabonato, R. F. Milani, K. Yotsuyanagi, and D. B. Rodriguez-Amaya . 2012. A comprehensive investigation of the mineral composition of Brazilian bee pollen: geographic and seasonal variations and contribution to human diet. J. Braz. Chem. Soc. 23:727-736.
39. Morton, R. D., C. Rowland, C. Wood, L. Meek, C. Marston, G. Smith, et al. 2011. CS Technical Report No 11/07: Final Report for LCM2007 - the new UK land cover map. NERC/Centre for Ecology & Hydrology (CEH Project Number NEC03259).
40. Naug, D. 2009. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol. Conserv. 142:2369-2372.
41. Nicolson, S. W. 2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool. 46:197-204.
42. Nicolson, S. W., and H. Human . 2013. Chemical composition of the 'low quality' pollen of sunflower (Helianthus annus, Asterarceae). Apidologie 44:144-152.
43. Oliver, R. 2007. Fat bees - part II. Am. Bee J. 148:791-796.
44. Pacini, E., M. Nepi, and J. Vesprini . 2003. Nectar biodiversity: a short review. Plant Syst. Evol. 238:7-21.
45. Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W. E. Kunin . 2010. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25:345-353.
46. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
47. Ricketts, T. H., J. Regetz, I. Steffan-Dewenter, S. A. Cunningham, C. Kremen, A. Bogdanski, et al. 2008. Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11:499-515.
48. Riley, J., U. Greggers, A. Smith, D. Reynolds, and R. Menzel . 2005. The flight paths of honeybees recruited by the waggle dance. Nature 435:205-207.
49. Roulston, T. H., and J. H. Cane . 2000. Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222:187-209.
50. Sapan, C. V., R. L. Lundblad, and N. C. Price . 1999. Colorimetric protein assay techniques. Biotechnol. Appl. Biochem. 29:99-108.
51. Schmidt, J. O., and A. Hanna . 2006. Chemical nature of phagostimulants in pollen attractive to honeybees. J. Insect Behav. 19:521-532.
52. Schmidt, J. O., S. C. Thoenes, and M. D. Levin . 1987. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann. Entomol. Soc. Am. 80:176-183.
53. Schmidt, L. S., J. O. Schmidt, H. Rao, W. Y. Wang, and L. G. Xu . 1995. Feeding preference and survival of young worker honey bees (Hymenoptera: Apidae). Fed rape, sesame, and sunflower pollen. J. Econ. Entomol. 88:1591-1595.
54. Seeley, T. D. 1986. Social foraging by honeybees - how colonies allocate foragers among patches of flowers. Behav. Ecol. Sociobiol. 19:343-354.
55. Simpson, S. J., and D. Raubenheimer . 2012. The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton Univ. Press, Princeton, NJ.
56. Singh, R. P., and P. N. Singh . 1996. Amino acid and lipid spectra of larvae of honey bee (Apis cerana Fabr) feeding on mustard pollen. Apidologie 27:21-28.
57. Somerville, D. C. 2001. Nutritional value of bee collected pollen. A report for Australian Government Rural Industrial Research & Development Corporation, RIRDC Publication Australia No. 01/047. Project No. DNA-134A. Available via https://rirdc.infoservices.com.au/downloads/01-047.
58. Steffan-Dewenter, I., and T. Tscharntke . 2000. Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122:288-296.
59. Steffan-Dewenter, I., U. Münzenberg, C. Bürger, C. Thies, and T. Tscharntke . 2002. Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421-1432.
60. Steffan-Dewenter, I., S. G. Potts, and L. Packer . 2005. Pollinator diversity and crop pollination services are at risk. Trends Ecol. Evol. 20:651-652.
61. Tscharntke, T., I. Steffan-Dewenter, A. Kruess, and C. Thies . 2002. Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecol. Appl. 12:354-363.
62. Tscharntke, T., A. M. Klein, A. Kruess, I. Steffan-Dewenter, and C. Thies . 2005. Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecol. Lett. 8:857-874.
63. Van der Planck, M., B. Leroy, B. Wathelet, R. Wattiez, and D. Michez . 2013. Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie, 45:192-204.
64. Vásquez, A., and T. C. Olofsson . 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apic. Res. 48:189-195.
65. Vergnes, A., I. Le Viol, and P. Clergeau . 2012. Green corridors in urban landscapes affect the arthropod communities of domestic gardens. Biol. Conserv. 145:171-178.
66. Visscher, P. K., and T. D. Seeley . 1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63:1790-1801.
67. Visscher, P., R. Morse, and T. Seeley . 1985. Honey bees choosing a home prefer previously occupied cavities. Insectes Soc. 32:217-220.
68. Waddington, K. D. 1983. Floral visitation sequences by bees: models and experiments. Pp. 461-473. in C. E. Jones and R. J. Little, eds. Handbook of experimental pollination biology. Scientific and Academic Editions, New York, NY.
69. Ward, K. N., J. L. Coleman, K. Clinnin, S. Fahrbach, and O. Rueppell . 2008. Age, caste, and behavior determine the replicative activity of intestinal stem cells in honeybees (Apis mellifera L.). Exp. Gerontol. 43:530-537.
70. Woodcock, B. A., M. Edwards, J. Redhead, W. R. Meek, P. Nuttall, S. Falk, et al. 2013. Crop flower visitation by honeybees, bumblebees and solitary bees: behavioural differences and diversity responses to landscape. Agric. Ecosyst. Environ. 171:1-8.
71. Wright, G. A. 2011. Appetitive learning: memories need calories. Curr. Biol. 21:R301-R302.
72. Wright, G. A., J. A. Mustard, S. M. Kottcamp, and B. H. Smith . 2007. Olfactory memory formation and the influence of reward pathway during appetitive learning by honey bees. J. Exp. Biol. 210:4024-4033.
73. Wright, G. A., A. F. Choudhary, and M. A. Bentley . 2009. Reward quality influences the development of learned olfactory biases in honeybees. Proc. R. Soc. B Biol. Sci. 276:2597-2604.
74. Zuur, A. F. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, NY.