Het effect van nutriëntenvervuiling op voedselkwaliteit van de bestuiver Bombus terrestris.

Eva Hulsmans Tobias Ceulemans
Bijen gaan achteruit, niet enkel door een tekort aan voedsel in het landschap, maar eventueel ook via een verminderde kwaliteit van dit voedsel als gevolg van nutriëntenvervuiling. Dit wordt hier experimenteel aangetoond.

Overbemesting van planten kan leiden tot slechtere voedselkwaliteit voor bestuivers

Zo’n 90% van alle wilde planten en meer dan twee derde van de landbouwgewassen hangen af van bestuivers voor de productie van hun zaden en vruchten. De meeste bestuivers zijn insecten, waarvan de belangrijkste groep bijen zijn. Er zijn ongeveer 30.000 soorten bijen, waaronder de welgekende honingbij, naast andere sociale of solitaire bijen en hommels, die allemaal afhankelijk zijn van pollen en nectar als enige voedselbron. Ondanks hun belangrijke rol gaan bijen wereldwijd achteruit waarbij een afname van bijenpopulaties intussen is vastgesteld op elk continent. Er zijn verschillende mogelijke oorzaken voor deze achteruitgang. Ten eerste kunnen competitie met invasieve soorten en een grote variëteit aan ziektes en parasieten inheemse bestuivers bedreigen. Ook de klimaatsverandering kan ervoor zorgen dat de interactie tussen plant en bestuiver verstoord wordt. Tot slot kan de grootschalige landgebruiksverandering van de afgelopen decennia, waarbij grote stukken semi-natuurlijk land naar een intensief landbouwlandschap worden omgevormd, een grote impact hebben. Dit zorgt er namelijk voor dat diversiteit aan plantensoorten achteruitgaat en dat er minder en kleinere stukjes habitat voor de bijen en hun voedselplanten overblijven. Dit alles leidt ertoe dat er minder voedsel en nestgelegenheid is voor de bijen. Door het sterk toegenomen gebruik van pesticiden en meststoffen in de landbouw sinds de Industriële Revolutie, zijn de overgebleven stukjes habitat dan ook nog eens van mindere habitatkwaliteit. Deze hebben immers niet alleen rechtstreeks toxische effecten op de bestuivers, maar kunnen ook de planten beïnvloeden die de voedselbron zijn van bijen. Bemesting van planten kan er namelijk voor zorgen dat de samenstelling van nectar en pollen, waarvan bijen zo afhankelijk zijn, verandert. Zulke samenstellingsveranderingen, voornamelijk van suikers en aminozuren, kunnen op hun beurt een effect hebben op het bloembezoek door bestuivers. Aangezien nectar en pollen de enige voedselbron van bijen zijn, kunnen veranderingen in hun samenstelling mogelijk ook een invloed hebben op de voedselkwaliteit voor deze bestuivers. In deze studie onderzochten wij het effect van een veranderde voedselsamenstelling na bemesting op Aardhommelkolonies. We vonden dat hommels die zich voeden met nectar en pollen van bemeste planten meer dode larven en minder levende werksters in hun nesten hadden. Bij de chemische analyse van de nectar en pollen zagen we dat hun suiker– en aminozuursamenstelling inderdaad veranderd was. In de pollen, wat de grootste bron is van aminozuren voor bijen, vonden we minder van de belangrijke aminozuren glycine en arginine. Daarbovenop vonden we minder glucose in de nectar, de voornaamste suikerbron van bijen. Glucose is een van de suikers die verkozen wordt door Aardhommels. Wij vermoeden dat een verminderd aandeel van deze suiker en de aangehaalde aminozuren in de voedselbronnen van deze hommels leidde tot de slechtere toestand van zijn kolonies. Deze resultaten zijn een van de eerste aanwijzingen dat bestuivers negatief beïnvloed worden door veranderingen in voedselkwaliteit na overbemesting. Dit kan belangrijke gevolgen hebben voor het behoud van bestuivers in een omgeving waar overbemesting alom aanwezig is.

Bibliografie

Abrol, D. P. (2011). Pollination Biology: Biodiversity conservation and agricultural production.
Pollination Biology: Biodiversity Conservation and Agricultural Production, 1–792.
Adams, A. A. W. (1955). Succisa Pratensis Moench. Journal of Ecology, 43(2), 709–718.
Addiscott, T. M., & Thomas, D. (2000). Tillage, mineralization and leaching: Phosphate. Soil and
Tillage Research, 53(3-4), 255–273.
Albrecht, M., Schmid, B., Hautier, Y., Mueller, C. B., & Müller, C. B. (2012). Diverse pollinator
communities enhance plant reproductive success. Proceedings of the Royal Society B: Biological
Sciences, 279(1748), 4845–4852.
Allen-Wardell, G., & Others. (1998). The potential consequences of pollinator declines on the
conservation of biodiversity and stability of fruit crop yields. The Forgotten Pollinators
Campaign, 12(1), 8–17.
Alston, D. G., Tepedino, V. J., Bradley, B. a, Toler, T. R., Griswold, T. L., & Messinger, S. M. (2007).
Effects of the insecticide phosmet on solitary bee foraging and nesting in orchards of Capitol
Reef National Park, Utah. Environmental Entomology, 36(4), 811–816.
Armbruster, W.S. 1984. The role of resin in angiosperm pollination: ecological and chemical
considerations. Amer. J. Bot., 71(8): 1149-1160.
Atsumura, C. M., Okoyama, J. Y., & Ashitani, I. W. (2004). Invasion Status and Potential Ecological
Impacts of an Invasive Alien Bumblebee , Bombus terrestris L . (Hymenoptera: Apidae)
Naturalized in Southern Hokkaido, Japan. Global Environmental Research, 8(1), 51–66.
Auerswald, L., Schneider, P., & Gäde, G. (1998). Utilisation of subrstrates during tethered flight with
and without lift generation in the african fruit beetle Pachnoda sinuata (Cetoniinae). The Journal
of Experimental Biology, 201, 2333–2342.
Baker, I., & Baker, H. G. (1976). Analysis of amino acids in nectar. Phytochem. Bull, 9(3), 4-7.
Ball, D. W. (2007). The Chemical Composition of Honey. Chemistry for Everyone, 84(10), 1643–1646.
Barrett, S. C. H. (2002). The Evolution of Plant Sexual Diversity. Nature Reviews Genetics, 3(4), 274–
284.
Bertazzini, M., Medrzycki, P., & Forlani, G. (2010). Amino acid content and nectar choice by forager
honeybees ( Apis mellifera L .). Amino Acids, 39, 315–318.
Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., … Kunin, W.
E. (2006). Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the
Netherlands. Science, 313(July), 351–354.
Blomqvist, M. M. 2005. Restoration of plant species diversity of ditch banks. Ecological constraints
and opportunities. Ph.D-thesis, Leiden University, the Netherlands.
Bobbink, R. B., Hicks, K. H., Galloway, J. G., Spranger, T. S., Alkemade, R. A., Ashmore, M. A., … De
Vries, W. (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity:
a synthesis. Ecological Applications, 20(1), 30–59.
Bobbink, R., Hornung, M., Roelofs, J. G. M., Hornungt, M., & Roelofst, J. G. M. (1998). The Effects of
Air-Borne Nitrogen Pollutants on Species Diversity in Natural and Semi- Natural European
Vegetation The effects of air-borne nitrogen pollutants on species diversity in natural and seminatural
European vegetation. Source: Journal of Ecology Journal of Ecology Journal of Ecology,
86(86), 717–738.
Branco, M. R., Kidd, N. A. C., & Pickard, R. S. (2006). A comparative evaluation of sampling methods
for Varroa destructor (Acari: Varroidae) population estimation. Apidologie, 37, 452–461.
Brittain, C. A., Vighi, M., Bommarco, R., Settele, J., & Potts, S. G. (2010). Impacts of a pesticide on
pollinator species richness at different spatial scales. Basic and Applied Ecology, 11(2), 106–115.
Brown, M. J. F. F., & Paxton, R. J. (2009). The conservation of bees : a global perspective. Apidologie,
40, 410–416.
Buchmann, S. L., & Nabhan, G. P. (1996). The Pollination Crisis. The Sciences, 36(4), 22–27.
Burkle, L. A., & Alarcon, R. (2011). The future of plant-pollinator diversity: Understanding interaction
networks acrosss time, space, and global change. American Journal of Botany, 98(3), 528–538.
Burkle, L. A., & Irwin, R. E. (2009). The effects of nutrient addition on floral characters and pollination
in two subalpine plants, Ipomopsis aggregata and Linum lewisii. Plant Ecology, 203(1), 83–98.
Burkle, L. A., & Irwin, R. E. (2010). Beyond biomass: Measuring the effects of community-level
nitrogen enrichment on floral traits, pollinator visitation and plant reproduction. Journal of
Ecology, 98(3), 705–717.
Cabuy, T., Ceulemans, T., Honnay, O. (2015). Verstoorde plant-bestuiver interacties na
nutriëntaanrijking (Unpublished master thesis). KU Leuven, Leuven, Belgium.
Cameron, S. A., Lozier, J. D., Strange, J. P., Koch, J. B., Cordes, N., Solter, L. F., & Griswold, T. L. (2011).
Patterns of widespread decline in North American bumble bees. Proceedings of the National
Academy of Sciences of the United States of America, 108(2), 662–7.
Cane, J. H., Eickwort G. C., Wesley F. R., Spielholz J. 1983 Foraging, grooming and mate-seeking
behaviors of Macropis nuda (Hymenoptera, Melittidae) and use of Lysimachia ciliata
(Primulaceae) oils in larval provisions and cell linings. Am. Midl. Nat. 110, 257–264
Carter, C., Shafir, S., Yehonatan, L., Palmer, R. G., & Thornburg, R. (2006). A novel role for proline in
plant floral nectars. Naturwissenschaften, 93, 72–79.
Carter, C., & Thornburg, R. W. (2004). Is the nectar redox cycle a floral defense against microbial
attack? Trends in Plant Science, 9(7), 320–324.
Carvell, C., Roy, D. B., Smart, S. M., Pywell, R. F., Preston, C. D., & Goulson, D. (2006). Declines in
forage availability for bumblebees at a national scale. Biological Conservation, 132(4), 481–489.
Ceulemans, T., Merckx, R., Hens, M., & Honnay, O. (2013). Plant species loss from European seminatural
grasslands following nutrient enrichment - is it nitrogen or is it phosphorus? Global
Ecology and Biogeography, 22(1), 73–82.
Chapman, R.F. (2012) The insects: structure and function, 5th edn. Cambridge University Press, USA
Chauzat, M., Laurent, M., Antipolis, F.-S., & Kim, B. (2014). A pan-European epidemiological study on
honeybee colony losses. European Union Reference Laboratory for Honeybee Health.
Choi, S., Park, H. Y., Paek, A., Kim, G. S., & Jeong, S. E. (2009). Insect Ornithine Decarboxylase (ODC)
Complements SPE1 Knock-Out of Yeast Saccharomyces cerevisiae. Molecules and Cells, 28, 575–
581.
Clough, Y., Ekroos, J., Baldi, A., Batary, P., Bommarco, R., Gross, N., … Smith, H. G. (2014). Density of
insect-pollinated grassland plants decreases with increasing surrounding land-use intensity.
Ecology Letters, 17(9), 1168–1177.
Cnaani, J., Thomson, J. D., & Papaj, D. R. (2006). Flower Choice and Learning in Foraging Bumblebees:
Effects of Variation in Nectar Volume and Concentration. Ethology, 112, 278–285.
Cook, S. M., Awmack, C. S., Murray, D. A., & Williams, I. H. (2003). Are honey bees’ foraging
preferences affected by pollen amino acid composition? Ecological Entomology, 28, 622–627.
Corbet, S. A., Willimas, I. H., & Osborne, J. L. (1991). Bees and the polllination of crops and wild
flowers: changes in the European community.
Crane, E. (1975). Honey: A Comprehensive Survey, Heinemann in cooperation with International Bee
Research Association, London.
Craine, J.M. (2009) Resource strategies of wild plants. Princeton University Press, New Jersey.
Cresswell, J. E., & Robertson, A. W. (1994). Discrimination by pollen-collecting bumblebees among
differentially rewarding flowers of an alpine wildflower, Campanula rotundifolia
(Campanulaceae). Oikos, 304-308.
Cresswell, J. E. (2011). A meta-analysis of experiments testing the effects of a neonicotinoid
insecticide (imidacloprid) on honey bees. Ecotoxicology, 20(1), 149–157.
Culley, T., Weller, S., & Sakai, A. (2002). Evolution of wind pollination in angiosperms. Trends in
Ecology & Evolution, 17(10), 5347–5347.
Dafni, A. (1998). The threat of Bombus terrestris spread. Bee World, 79(3), 113–114.
Danforth, B. (2007). Bees. Current Biology, 17(5), 156–161.
Darwin C. (1862) On the various contrivances by which British and foreign orchids are fertilized by
insects: and on the good effects of intercrossing. John Murray, London
Davis MA (1981) The effect of pollinators, predators, and energy constraints on the floral ecology and
evolution of Trillium erectum. Oecologia 48:400–406
Day, S., Beyer, R., Mercer, A., & Ogden, S. (1990). The Nutrient Composition of Honeybee-Collected
Pollen in Otago, New Zealand. Journal of Apicultural Research, 29(3), 138–146.
De Groot, A.P. (1953) Protein and amino acid requirements of the honeybee (Apis mellifera L.).
Physiol Comp Oecologia 3, 197–285
de Jong, T. J., Waser, N. M., & Klinkhamer, P. G. L. (1993). Geitonogamy: The neglected side of
selfing. Trends in Ecology and Evolution, 8(9), 321–325.
Delaplane, K. S. & Mayer, D. F. (2000). Crop Pollination by Bees. – New York, Oxon (CABI Publishing)
De Luca, P. A., & Vallejo-Marin, M. (2013). What’s the “buzz” about? The ecology and evolutionary
significance of buzz-pollination. Current Opinion in Plant Biology, 16(4), 429–435.
Dias, B. S. F., Raw, A., & Imperatriz-Fonseca, V. L. (1999). International Pollinators initiative: The Sao
Paulo declaration on pollinators. Report on the recommendations of the workshop on the
conservation and sustainable use of pollinators in agriculture with emphasis on bees.
Díaz, S., Tilman, D., Fargione, J., Chapin III, F. S., Dirzo, R., Kitzberger, T., … Eardley, C. (2006).
Biodiversity Regulation of Ecosystem Services. Ecosystems and Human Well-Being: Current State
and Trends, 297–329 ST – Biodiversity Regulation of Ecosystem.
Duchateau, M. J., & Velthuis, H. H. W. (1988). Development and reproductive strategies in Bombus
terrestris colonies. Behaviour, 107(3), 186-207.
Dudash, M. R. (1991). Plant Size Effects on Female and Male Function in Hermaphroditic Sabatia-
Angularis (Gentianaceae). Ecology, 72(3), 1004–1012.
Duffield, G. E., Gibson, R. C., Gilhooly, P. M., Hesse, A. J., Inkley, C. R., Gilbert, F. S., & Barnard, C. J.
(1993). Choice of flowers by foraging honey bees (Apis mellifera): possible morphological cues.
Ecological entomology,18(3), 191-197.
Efstathion, C. A., Bardunias, P. M., Boyd, J. D., & Kern, W. H. (2015). A push-pull integrated pest
management scheme for preventing use of parrot nest boxes by invasive Africanized honey
bees. Journal of Field Ornithology, 86(1), 65–72.
Ellis, A., Ellis, J., Malley, M. O., & Nalen, C. Z. (2013). The Benefits of Pollen to Honey Bees.
Ellstrand, N. C., & Elam, D. R. (1993). Population genetic consequences of small population size:
Implications for plant conservation. Annual Review of Ecology Evolution and Systematics,
24(1993), 217–242.
Elser, J. J., Acharya, K., Kyle, M., Cotner, J., Makino, W., Markow, T., … Sterner, R. W. (2003). Growth
rate-stoichiometry couplings in diverse biota. Ecology Letters, 6(10), 936–943.
Faegri K, van der Pijl L. The principles of pollination ecology. 3rd rev edn. Oxford: Pergamon Press;
1979.
Falkowski, P. G., Scholes, R. J., Boyle, E., Canadell, J., Canfield, D., Elser, J., … Steffen, W. (2000). The
global carbon cycle: a test of our knowledge of earth as a system. Science, 290(5490), 291–296.
Filella, I., Primante, C., Llusià, J., Martín González, A. M., Seco, R., Farré-Armengol, G., … Peñuelas, J.
(2013). Floral advertisement scent in a changing plant-pollinators market. Scientific Reports, 3,
3434.
Fontaine, C., Dajoz, I., Meriguet, J., & Loreau, M. (2006). Functional diversity of plant-pollinator
interaction webs enhances the persistence of plant communities. PLoS Biology, 4(1), 0129–
0135.
Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-Virus Interaction in Collapsing Honey Bee
Colonies. PLoS ONE, 8(3).
Free, J. B. 1993 Insect pollination of crops. London, UK: Academic Press
Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J., & Brown, M. J. F. (2014). Disease
associations between honeybees and bumblebees as a threat to wild pollinators. Nature,
506(7488), 364–6.
Galen, C., & M. E. A. Newport. (1987). Bumble Bee Behavior and Selection on Flower Size in the Sky
Pilot, Polemonium viscosum. Oecologia, 74(1), 20–23
Gallai, N., Salles, J. M., Settele, J., & Vaissière, B. E. (2009). Economic valuation of the vulnerability of
world agriculture confronted with pollinator decline. Ecological Economics, 68(3), 810–821.
Galloway, J. N., Dentener, F. J., Capone, D. G., Boyer, E. W., Howarth, R. W., Seitzinger, S. P., … Vo, C.
J. (2004). Nitrogen cycles : past , present , and future. Biogeochemistry, 70, 153–226.
Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., … Sutton, M. a.
(2008). Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential
Solutions. Science, 320(5878), 889–892.
Gardener, M. C., & Gillman, M. P. (2001). The effects of soil fertilizer on amino acids in the floral
nectar of corncockle, Agrostemma githago (Caryophyllaceae). Oikos, 92(1), 101–106.
Gardener, M. C., & Gillman, M. P. (2002). The taste of nectar - a neglected area of pollination
ecology. Oikos, 98(3), 552–557.
Garibaldi, L. A., Carvalheiro, L. G., Vaissière, B. E., Gemmill-herren, B., Hipólito, J., Freitas, B. M., …
Blochtein, B. (2016). Mutually beneficial pollinator diversity and crop yield outcomes in small
and large Farms. Science, 351(6271), 388–391.
Garibaldi, L. A., Steffan-Dewenter, I., Kremen, C., Morales, J. M., Bommarco, R., Cunningham, S. A., …
Klein, A. M. (2011). Stability of pollination services decreases with isolation from natural areas
despite honey bee visits. Ecology Letters, 14(10), 1062–1072.
Garibaldi, L. A., Steffan-dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., …
Carvalheiro, L. G. (2014). Honey Bee Abundance. Science, 339(May), 1608–1611.
Ghazoul, J. (2005). Buzziness as usual? Questioning the global pollination crisis. Trends in Ecology and
Evolution, 20(7), 367–373.
Gijbels, P., Ceulemans, T., Van den Ende, W., & Honnay, O. (2015). Experimental fertilization
increases amino acid content in floral nectar, fruit set and degree of selfing in the orchid
Gymnadenia conopsea. Oecologia, 179(3), 785–795.
Gijbels, P., Ende, W. Van Den, & Honnay, O. (2015). Phenotypic selection on nectar amino acid
composition in the Lepidoptera pollinated orchid species Gymnadenia conopsea. Oikos, 124,
421–427.
Gijbels, P., Van den Ende, W., & Honnay, O. (2014). Landscape scale variation in nectar amino acid
and sugar composition in a Lepidoptera pollinated orchid species and its relation with fruit set.
Journal of Ecology, 102(1), 136–144.
Gill, R. J., Ramos-Rodriguez, O., & Raine, N. E. (2012). Combined pesticide exposure severely affects
individual- and colony-level traits in bees. Nature, 491(7422), 105–8.
Goka, K. and Japanese Bumblebee Companies Association (2003) The ecological problem caused by
commercialization of bumblebees-the past and the future. Japanese Journal of Plant Protection,
57: 452-456.
González-teuber, M., & Heil, M. (2009). Nectar chemistry is tailored for both attraction of mutualists
and protection from exploiters. Plant Signalling and Behavior, 4(9), 809–813.
González-Teuber, M., & Heil, M. (2009). The role of extrafloral nectar amino acids for the preferences
of facultative and obligate ant mutualists. Journal of Chemical Ecology, 35(4), 459–468.
Goulson, D. (1999). Foraging strategies of insects for gathering nectar and pollen, and implications
for plant ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics, 2(2),
185–209.
Goulson, D. (2003). The conservation of bumble bees. Bee World, 84(3), 105–106.
Goulson, D. (2010). Bumblebees: behaviour, ecology, and conservation (No. Ed. 2). Oxford University
Press. Chicago
Goulson, D., Hanley, M. E., Darvill, B., Ellis, J. S., & Knight, M. E. (2005). Causes of rarity in
bumblebees. Biological Conservation, 122, 1–8.
Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress
from parasites, pesticides, and lack of flowers. SciencExpress, (February), 1–16.
Graham, W. F., & Duce, R. A. (1979). Atmospheric pathways of the phosphorus cycle. Geochimica et
Cosmochimica Acta, 43(8), 1195–1208.
Hanley, M. E., Franco, M., Pichon, S., Darvill, B., & Goulson, D. (2008). Breeding system, pollinator
choice and variation in pollen quality in British herbaceous plants. Functional Ecology, 22(4),
592–598.
Hansen, K., Wacht, S., Seebauer, H., & Schnuch, M. (1998). New Aspects of Chemoreception in Flies.
Annals New York Academy of Sciences, 855(1), 143–147.
Haratym, W., & Weryszko-chmielewska, E. (2012). The ecological features of flowers and
inflorescenses of two species of the genus Petasites Miller (Asteraceae). Acta Agrobotanica,
65(2), 37–45.
Harder, L. D., & Barrett, S. C. H. (1992). The Energy Cost of Bee Pollination for Pontederia cordata
(Pontederiaceae). Functional Ecology, 6(2), 226–233.
Harder, L. D., & Barrett, S. C. H. (1995). Mating cost of large floral displays in hermaphrodite plants.
Nature.
Hautier, Y., Niklaus, P.A. & Hector, A. (2009) Competition for light causes plant biodiversity loss after
eutrophication. Science, 324, 636-6387
Heil, M. (2011). Nectar : generation, regulation and ecological functions. Trends in Plant Science,
16(4), 191–200.
Heinrich, B. (1979). Resource heterogeneity and patterns of movement in foraging bumblebees.
Oecologia 40: 235-245.
Hendriksma, H. P., Oxman, K. L., & Shafir, S. (2014). Amino acid and carbohydrate tradeoffs by honey
bee nectar foragers and their implications for plant – pollinator interactions. Journal of Insect
Physiology, 69, 56–64.
Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J., Aupinel, P., … Decourtye, A. (2012). A
common pesticide decreases foraging succes and survival in Honey Bees. Science, 336, 348–350.
Highfield, A. C., El Nagar, A., Mackinder, L. C. M., Noël, L. M. L. J., Hall, M. J., Martin, S. J., &
Schroeder, D. C. (2009). Deformed wing virus implicated in overwintering honeybee colony
losses. Applied and Environmental Microbiology, 75(22), 7212–7220.
Hingston, A. B. and 31 other authors (2002) Extent of invasion of Tasmanian native vegetation by the
exotic bumblebee Bombus terrestris (Apoidea: Apidae). Austral Ecology, 27:162-172
Hobbs G.A., Nummi W.O., Virostek J.F. (1961) Foodgathering behaviour of honey, bumble, and
leafcutting bees (Hymenoptera: Apoidea) in Alberta, Can. Entomol. 93, 409–419.
Hoffmann, F. (2005). Biodiversity and pollination. Flowering plants and flower-visiting insects in
agricultural and semi-natural landscapes. Febodruk BV Enschede, Netherlands.
Holland, J. G., & Bourke, A. F. G. (2015). Colony and individual life-history responses to temperature
in a social insect pollinator, 1209–1217.
Holm S.N. (1966) The utilization and management of bumble bees for red clover and alfalfa seed
production, Annu. Rev. Entomol. 11, 155–182.
Holzschuh, A., Dormann, C. F., Tscharntke, T., & Steffan-Dewenter, I. (2011). Expansion of massflowering
crops leads to transient pollinator dilution and reduced wild plant pollination.
Proceedings. Biological Sciences / The Royal Society, 278(1723), 3444–51.
Holzschuh, A., Steffan-Dewenter, I., & Tscharntke, T. (2008). Agricultural landscapes with organic
crops support higher pollinator diversity. Oikos, 117(3), 354–361.
Hooftman DAP, van Kleunen M, Diemer M (2003) Effects of habitat fragmentation on the fitness of
two common wetland species, Carex davalliana and Succisa pratensis. Oecologia 134:350–359
Hoover, S. E. R., Ladley, J. J., Shchepetkina, A. A., Tisch, M., Gieseg, S. P., & Tylianakis, J. M. (2012).
Warming, CO 2, and nitrogen deposition interactively affect a plant-pollinator mutualism.
Ecology Letters, 15(3), 227–234.
Hopkins I (1914). The history of the introduction of bumble bees to New Zealand. NZ Dept Agric 2-28
Horswill, P., O’Sullivan, O., Phoenix, G.K., Lee, J.A. & Leake, J.R. (2008) Base cation depletion,
eutrophication and acidification of species-rich grasslands in response to long-term simulated
nitrogen deposition. Environmental Pollution, 155, 336-349.
Hrassnigg, N., Leonhard, B., & Crailsheim, K. (2003). Free amino acids in the haemolymph of honey
bee queens (Apis mellifera L .). Amino Acids, 24, 205–212.
Imran, M., Ahmad, M., Nasir, M. F., & Saeed, S. (2015). Effect of different nest box materials on the
mating of European bumblebee, Bombus terrestris (Hymenoptera: Apidae) under controlled
environmental conditions. Pakistan Journal of Zoology, 47(1), 241–247.
Inouye, D. W., & Waller, G. D. (1984). Responses of honey bees (Apis mellifera) to amino acid
solutions mimicking floral nectars. Ecology, 65(2), 618–625.
Irwin, R. E., & Adler, L. S. (2008). Nectar secondary coumpunds affect self-pollen transfer: implication
for female and male reproduction. Ecology, 89(8), 2207–2217.
Isbell, F., Calcagno, V., Hector, A., Connolly, J., Harpole, W. S., Reich, P. B., … Loreau, M. (2011). High
plant diversity is needed to maintain ecosystem services. Nature, 477(7363), 199–202.
Iwata, T., Nagasaki, O., Ishii, H. S., & Ushimaru, A. (2012). Inflorescence architecture affects pollinator
behaviour and mating success in Spiranthes sinensis (Orchidaceae). New Phytologist, 193(1),
196–203.
Jennersten, O., Berg, L., & Lehman, C. (1988). Phenological Differences in Pollinator Visitation, Pollen
Deposition and Seed Set in the Sticky Catchfly, Viscaria Vulgaris. Journal of Ecology, 76(4), 1111–
1132.
Jha, S., & Kremen, C. (2013). Resource diversity and landscape-level homogeneity drive native bee
foraging. Proceedings of the National Academy of Sciences of the United States of America,
110(2), 555–8.
Joar Hegland, S., & Totland, Ø. (2008). Is the magnitude of pollen limitation in a plant community
affected by pollinator visitation and plant species specialisation levels? Oikos, 117(6), 883–891.
Jongejans E, de Kroon H (2005) Space versus time variation in the population dynamics of three cooccurring
perennial herbs. J Ecol 93:681–692
Kearns, C. A., & Inouye, D. W. (1997). Pollinators, Flowering Plants, and Conservation Biology.
BioScience, 47(5), 297–307
Kearns, C. A., Inouye, D. W., & Waser, N. M. (1998). Endangered Mutualisms: The Conservation of
Plant-Pollinator Interactions. Annual Review of Ecology and Systematics, 29, 83–112.
Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology and
Evolution, 17(5), 230–241.
Kerr, J. T., Pindar, A., Galpern, P., Packer, L., Potts, S. G., Roberts, S. M., … Gall, L. F. (2015). Climate
change impacts on bumblebees converge across continents. Science, 349(6244), 177–180.
Kessler, M., & Lohaus, G. (2008). Nectar sugar composition and concentration in relation to
pollination syndromes in Bromeliaceae, 10, 502–511.
Kevan, P. G. (1976). Flourescent nectar (technical comment). Science 194: 341-342
Klatt, B. K., Holzschuh, A., Westphal, C., Clough, Y., Smit, I., Pawelzik, E., & Tscharntke, T. (2014). Bee
pollination improves crop quality, shelf life and commercial value. Proceedings. Biological
Sciences / The Royal Society, 281(1775), 20132440.
Kleijn, D., Winfree, R., Bartomeus, I., Carvalheiro, L. G., Henry, M., Isaacs, R., … Potts, S. G. (2015).
Delivery of crop pollination services is an insufficient argument for wild pollinator conservation.
Nature Communications, 6(May), 7414.
Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., &
Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops.
Proceedings. Biological Sciences / The Royal Society, 274(1608), 303–13.
Kosior, A., Celary, W., Olejniczak, P., Fijal, J., Król, W., Solarz, W., & Plonka, P. (2007). The decline of
the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central
Europe. Oryx, 41(01), 79.
Kwak, M. M., Velterop, O., & van Andel, J. (1998). Pollen and gene flow in fragmented habitats.
Applied Vegetation Science, 1(1), 37–54.
Laere, V., Ellis, W. N., Smets, E., & Petanidou, T. (2006). What shapes amino acid and sugar
composition in Mediterranean floral nectars? Oikos, 115, 155–169.
Lanza, J., Smith, G. C., Sack, S., & Cash, A. (1995). Variation in nectar volume and composition of
Impatiens capensis at the individual, plant, and population levels. Oecologia, 102(1), 113-119
Lau, T.-C., & Stephenson, A. G. (1994). Effects of soil phosphorus on pollen production, pollen size,
pollen phosphorus content, and the ability to sire seeds in Cucurbita pepo (Cucurbitaceae).
Sexual Plant Reproduction, 7(4), 215–220.
Lavergne, S., Molina, J., & Debussche, M. (2006). Fingerprints of environmental change on the rare
mediterranean flora: A 115-year study. Global Change Biology, 12(8), 1466–1478.
Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: can Varroa explain
part of the colony losses? Apidologie, 41(3), 353–363.
Le Féon, V., Schermann-Legionnet, A., Delettre, Y., Aviron, S., Billeter, R., Bugter, R., … Burel, F.
(2010). Intensification of agriculture, landscape composition and wild bee communities: A large
scale study in four European countries. Agriculture, Ecosystems and Environment, 137(1-2),
143–150.
Litrico, I., & Maurice, S. (2013). Resources , competition and selfing : their influence on reproductive
system evolution. Evolutionary Ecology, 27, 923–936.
Loper, G. M., & Cohen, A. C. (1987). Amino acid content of dandelion pollen, a honey bee
(Hymenoptera: Apidae) nutritional evaluation. Journal of Economic Entomology, 80(1), 14-17.
Luijten,S.H., Dierick,A., Oostermeijer,J.G.B., Raijman,L.E.L. & Den Nijs,H.C.M. 2000. Population size,
genetic variation, and reproductive success in a rapidly declining, self-incompatible perennial
(Arnica montana) in The Netherlands. Conservation Biology 14: 1776-1787.
Mahowald, N. M., Engelstaedter, S., Luo, C., Sealy, A., Artaxo, P., Benitez-Nelson, C., … Siefert, R. L.
(2009). Atmospheric iron deposition: global distribution, variability, and human perturbations.
Annual Review of Marine Science, 1, 245–278.
Mallinger, R. E., & Gratton, C. (2015). Species richness of wild bees, but not the use of managed
honeybees, increases fruit set of a pollinator-dependent crop. Journal of Applied Ecology, 52(2),
323–330.
Mamut, J., Xiong, Y. Z., Tan, D. Y., & Huang, S. Q. (2014). Pistillate flowers experience more pollen
limitation and less geitonogamy than perfect flowers in a gynomonoecious herb. New
Phytologist, 201(2), 670–677.
Matheson A, Buchmann S.L, O'Toole C, Westrich P, Williams J.H. Academic Press; London, UK: 1996.
The conservation of bees
Mattila, H. R., & Seeley, T. D. (2007). Genetic Diversity in Honey bee Colonies Enhances Productivity
and Fitness. Science, 317, 362–365.
McDonald AW, Bakker JP, Vegelin K (1996) Seed bank classification and its importance for the
restoration of species-rich flood- meadows. J Veg Sci 7:157–164
Meijer, A., Lamers, H., & Chamuleau, R. (1990). Nitrogen metabolism and Ornithine cycle function.
Physiological Reviews, 70(3), 701–748.
Melo G. A. R., Gaglianone M. C. 2005Females of Tapinotaspoides, a genus in the oil-collecting bee
tribe Tapinotaspidini, collect secretions from non-floral trichomes (Hymenoptera, Apidae). Rev.
Bras. Entomol. 49, 167–168
Memmott, J., Craze, P. G., Waser, N. M., & Price, M. V. (2007). Global warming and the disruption of
plant-pollinator interactions. Ecology Letters, 10(8), 710–717.
Mevi-Schutz, J., & Erhardt, A. (2005). Amino acids in nectar enhance butterfly fecundity: a longawaited
link. The American Naturalist, 165(4), 411–419.
Michener C. D. (2007). The bees of the world, 2nd edn. Baltimore, MD: John Hopkins University Press
Micheu, S., Crailsheim, K., & Leonhard, B. (2000). Importance of proline and other amino acids during
honeybee flight (Apis mellifera carnica POLLMANN). Amino Acids, 18, 157–175.
Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-being: Synthesis. Island
Press, Washington, DC
Mullin, C. A., Frazier, M., Frazier, J. L., Ashcraft, S., Simonds, R., vanEngelsdorp, D., & Pettis, J. S.
(2010). High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for
Honey Bee Health. PLoS ONE, 5(3).
Nabhan, G. (1996). Global List of Threatened Vertebrate Wildlife Species Serving as Pollinators for
Crops and Wild Plants: Pollinator Redbook, Volume One. Forgotten Pollinators Campaign,
Arizona-Sonora Desert Museum
Nepi, M. (2014). Beyond nectar sweetness: the hidden ecological role of non-protein amino acids in
nectar. Journal of Ecology, 102, 108–115.
Newman, E. (1995). Phosphorus inputs to terrestrial ecosystems. Journal of Ecology, 83(4), 713–726.
Nicolson, S. W., Nicolson, S. W., Taylor, P., Nicolson, S. W., Wyk, J. H. Van, & Nicolson, S. W. (2011).
Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. African
Zoology, 46(2), 197–204.
Nicolson, S. & Thornburg, R.W. (2007) Nectar chemistry. Nectaries and Nectar (eds E. Pacini, M. Nepi
& S. Nicolson), pp. 215–263. Springer, Dordrecht.
Oksanen J., Blanchet F., Kindt R., Legendre P., Minchin P., O'Hara R., Simpson G., Solymos P., Stevens
M. & Wagner H. (2016). vegan: Community Ecology Package. R package version 2.3-3.
Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals?
Oikos, 120(3), 321–326.
Oostermeijer,J.G.B., Luijten,S.H., Petanidou,T., Kos,M., Ellis-Adam,A.C. & Den Nijs,H.C.M. 2000.
Pollination in rare plants: is population size important? Det Norske Videnskaps Akademi. I.
Matematisk-Naturvidenskapelige Klasse, Skrifter, Ny Serie 39: 201-213
Osborne, J. L., Williams, I. H., & Corbet, S. A. (1991). Bees, Pollination and Habitat Change in the
European Community. Bee World, 72(3), 99–116.
Otti, O., & Schmid-Hempel, P. (2008). A field experiment on the effect of Nosema bombi in colonies
of the bumblebee Bombus terrestris. Ecological Entomology, 33(5), 577–582.
Palmer, M. J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G. a, & Connolly, C. N. (2013). Cholinergic
pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications,
4, 1634.
Pasquale, G. Di, Salignon, M., Conte, Y. Le, Belzunces, L. P., & Decourtye, A. (2013). Influence of
Pollen Nutrition on Honey Bee Health: do Pollen Quality and Diversity Matter? PLoS ONE, 8(8),
1–14.
Pavlik, B. M., Ferguson, N., & Nelson, M. (1993). Assessing limitations on the growth of endangered
plant populations, II. Seed production and seed bank dynamics of Erysimum capitatum ssp.
Angustatum and Oenothera deltoides ssp. Howellii. Biological Conservation, 65(3), 267–278.
Penuelas, J., Sardans, J., Rivas-ubach, A., & Janssens, I. A. (2012). The human-induced imbalance
between C, N and P in Earth’s life system. Global Change Biology, 18(1), 3–6.
Petanidou, T. (2005). Sugars in Mediterranean floral nectars: an ecological and evolutionary
approach. Journal of Chemical Ecology, 31(5), 1065–1088.
Petanidou, T., Goethals, V., & Smets, E. (1999). The effect of nutrient and water availability on nectar
secretion and nectary structure of the dominant Labiatae species of phrygana. Systematics and
Geography of Plants, 233-244.
Petanidou, T., & Vokou, D. (1990). Pollination and pollen energetics in Mediterranean ecosystems.
American Journal of Botany, 77(8), 986–992.
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global
pollinator declines: Trends, impacts and drivers. Trends in Ecology and Evolution, 25(6), 345–
353.
Proctor, M.C.F. 1978. Insect pollination syndromes in an evolutionary and ecosystemic context. In
A.J. Richards [ed.], The pollination of flowers by insects, 105–166. Academic Press, New York,
USA.
Pyke, G. (1991). What does it cost a plant to produce floral nectar? Nature, 350, 58–59.
Rands, S. A., & Whitney, H. M. (2010). Effects of pollinator density-dependent preferences on field
margin visitations in the midst of agricultural monocultures: A modelling approach. Ecological
Modelling, 221(9), 1310–1316.
Rathcke, B. J., & Jules, E. S. (1993). Habitat fragmentation and plant-pollinator interactions. Current
Science.
Reis, M. G., De Faria, A. D., Bittrich, V., Amaral, M. D. C. E., & Marsaioli, A. J. (2000). The Chemistry of
Flower Rewards - Oncidium (Orchidaceae). Journal of the Brazilian Chemical Society, 11(6), 600–
608.
Ricketts, T. H., Regetz, J., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Bogdanski, A., … Viana,
B. F. (2008). Landscape effects on crop pollination services: Are there general patterns? Ecology
Letters, 11(5), 499–515.
Roberts, S. P., & Harrison, J. O. N. F. (1998). Mechanisms of Thermoregulation in Flying Bees.
American Zoology, 38, 492–502.
Robertson, A., Mountjoy, C., Faulkner, B., Roberts, M., & Macnair, M. (1999). Bumble bee selection of
Mimulus guttatus flowers: The effect of pollen quantity and reward depletion. Ecology, 80(8),
2594–2606.
Rodriguez-Pena, N., Stoner, K. E., Ayala-berdon, J., Rodrı, N., Flores-ortiz, C. M., Duran, A., &
Schondube, J. E. (2013). Nitrogen and amino acids in nectar modify food selection of
nectarivorous bats. Journal of Animal Ecology, 82, 1106–1115.
Roubik, D. W., Yanega, D., Aluja, M., Buchmann, S., & Inouye, D. (1995). On optimal nectar foraging
by some tropical bees (Hymenoptera: Apidae). Apidologie, 26, 197–211.
Roulston, T. A. I. H., & Cane, J. H. (2002). The effect of pollen protein concentration on body size in
the sweat bee Lasioglossum zephyrum (Hymenoptera: Apiformes). Evolutionary Ecology, 16,
49–65.
Rutrecht, S. T., & Brown, M. J. F. (2009). Differential virulence in a multiple-host parasite of bumble
bees: Resolving the paradox of parasite survival? Oikos, 118(6), 941–949.
Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., … Mooney, H. A. (2000).
Global Biodiversity Scenarios for the Year 2100. Science, 287, 1770–1775.
Sammataro, D., Gerson, U., & Needham, G. (2000). Parasitic mites of the honey bees: Life History,
Implications, and Impact. Annual Review Entomology, 45, 519–548.
Saville, N. M., Dramstad, W. E., Fry, G. L. A., & Corbet, S. A. (1997). Bumblebee movement in a
fragmented agricultural landscape. Agriculture, Ecosystems and Environment, 61(2-3), 145–154.
Schiestl, F. P. (2015). Ecology and evolution of floral volatile- mediated information transfer in plants.
New Phytologist, 206, 571–577.
Schmidt, J. O., & Hurley, R. (1995). Selection of nest cavities by Africanized and European honey bees.
Apidologie, 26, 467-476.
Scofield, H. N., & Mattila, H. R. (2015). Honey Bee Workers That Are Pollen Stressed as Larvae
Become Poor Foragers and Waggle Dancers as Adults. PLoS ONE, 10(4), 1–19.
Scott Schneider, S., DeGrandi-Hoffman, G., & Smith, D. R. (2004). The African Honey Bee: Factors
contributing to a successful biological invasion. Annual Review of Entomology, 49(1), 351–376.
Shykoff, J. (1997). Do all sexual signals trade off the same way? Trends in Ecology and Evolution,
12(2), 67–68.
Sladen F.. The Bumble-bee, its Life History and How to Domesticate it, with Descriptions of all the
British Species of Bombus and Psithyrus. MacMillan, London (1912)
Smith, V. H., Tilman, G. D., & Nekola, J. C. (1998). Eutrophication: Impacts of excess nutrient inputs
on freshwater, marine, and terrestrial ecosystems. Environmental Pollution, 100(1-3), 179–196.
Somme, L. S., Vanderplanck, M. V, Michez, D. M., Lombaerde, I. L., Moerman, R. M., Wathelet, B. W.,
… Jacquemart, A. J. (2015). Pollen and nectar quality drive the major and minor floral choices of
bumble bees. Apidologie, 46, 92–106.
Spek,T. 2004. Het Drentse esdorpenlandschap. Een historisch-geografische studie. Uitgeverij Matrijs,
Utrecht, the Netherlands
Steffan-Dewenter, I., Potts, S. G., Packer, L., & Ghazoul, J. (2005). Pollinator diversity and crop
pollination services are at risk [3] (multiple letters). Trends in Ecology and Evolution, 20(12),
651–653.
Stork, N., & Samways, M. (1995). Global Biodiversity Assessment.
Taylor, P., Nicolson, S. W., Wyk, J. H. Van, & Nicolson, S. W. (2015). Bee food : the chemistry and
nutritional value of nectar , pollen and mixtures of the two, 7020(May), 37–41.
Thomson, D. M. (2006). Detecting the Effects of Introduced Species : A Case Study of Competition
between Apis and the effects of introduced of species : a case study Detecting between Apis
and Bombus competition. Oikos, 114(3), 407–418.
Thorp, R. N., Briggs, D. L., Estes, J. R., and Erikson, E. H. (1975). Nectar flourescence under ultaviolet
irradiation. Science 189: 476-478.
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger,
W.H., Simberloff, D. & Swackhammer, D. (2001) Forecasting agriculturally driven global
environmental change. Science, 292, 281-284
Tomimatsu, H., & Ohara, M. (2002). Effects of forest fragmentation on seed production of the
understory herb Trillium camschatcense. Conservation Biology, 16(5), 1277–1285.
Traveset, A., & Richardson, D. M. (2006). Biological invasions as disruptors of plant reproductive
mutualisms. Trends in Ecology and Evolution, 21(4), 208–216.
Turner, B., & Haygarth, P. (2001). Phosphorus solubilization in rewetted soils. Nature, 411, 258
Tylianakis, J. M., Didham, R. K., Bascompte, J., & Wardle, D. A. (2008). Global change and species
interactions in terrestrial ecosystems. Ecology Letters, 11(12), 1351–1363.
UNEP (2005). Annual Report
Usda. (2012). Report on the National Stakeholders Conference on Honey Bee Health, 62.
van der Meer, S., Dahlgren, J. P., Mildén, M., & Ehrlén, J. (2014). Differential effects of abandonment
on the demography of the grassland perennial Succisa pratensis. Population Ecology, 56(1),
151–160.
Van Der Meijden, R., Odé, B., Groen, C.L.G., Witte, J.-P.M. & Bal, D. (2000) Bedreigde en kwetsbare
vaatplanten in Nederland. Basisrapport met voorstel voor de Rode Lijst. Gorteria, 26, 85–208.
Velthuis, H. H. W., & Doorn, A. Van. (2006). A century of advances in bumblebee domestication and
the economic and environmental aspects of its commercialization for pollination. Apidologie,
37, 421–451.
Vergeer, P., Rengelink, R., Copal, A., & Ouborg, N. J. (2003). The interacting effects of genetic
variation, habitat quality and population size on preformance of Succisa pratensis. Journal of
Ecology, 91(1), 18–26.
Wacht, S., Lunau, K., & Hanse, K. (2000). Chemosensory control of pollen ingestion in the hoverfly
Eristalis tenax by labellar taste hairs. Journal of Comparitive Physiology, 186, 193–203.
Wallin L, Svensson BM, Lonn M (2009) Artificial dispersal as a restoration tool in meadows: sowing or
planting? Restor Ecol 17:270–279
Westrich P., Schwenninger H.-R., Dathe H., Riemann H., Saure C., Voith J. and Weber K. 1998. Rote
Liste der Bienen (Hymenoptera: Apidae). In: Bundesamt fur Naturschutz (ed.), Rote Liste
Gefahrdeter Tiere Deut
Whitehorn, P. R., O’Connor, S., Wackers, F. L., & Goulson, D. (2012). Neonicotinoid Pesticide Reduces
Bumble Bee Colony Growth and Queen Production. Science, 336(6079), 351–352.
Williams, P. H. (1991). The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini).
British Museum (Natural History). Chicago
Williams, C. S. (1998). The identity of the previous visitor influences flower rejection by nectar
collecting bees. Anim. Behav. 56: 673-681.
Winfree, R., Aguilar, R., Vázquez, D. P., Lebuhn, G., Aizen, A., & Hall, M. (2009). A meta-analysis of
bees’ response to anthropogenic disturbance. Ecology, 90(8), 2068–2076.
Winston, M. (1992). The Biology And Management Of Africanized Honey Bees. Annual Review of
Entomology, 37(1), 173–193. http://doi.org/10.1146/annurev.ento.37.1.173
Woodcock, T. S., Larson, B. M. H., Kevan, P. G., Inouye, D. W., & Lunau, K. (2014). Flies and flowers II:
floral attractants and rewards. Journal of Pollination Ecology, 12(8), 63–94.
Zimmerman, M. (1982). Optimal foraging: random movement by pollen collecting bumblebees.
Oecologia, 53(3), 394-398.

Universiteit of Hogeschool
MSc in Biologie
Publicatiejaar
2016
Promotor(en)
Olivier Honnay
Kernwoorden
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