Apple tree; Nectar; Pear tree; Pollen; Pollinating insects; Fruit production
Résumé :
[en] Pear and apple are among the main fruit crops worldwide. These species can be planted in mixed orchards,and they both depend on insect pollination for fruit set. As pollinating insects are attracted by the floralresources, we investigated nectar and pollen production and chemical composition in four pear (‘Con-corde’, ‘Conférence’, ‘Doyenné du Comice’, ‘Triomphe de Vienne’) and five apple (‘Braeburn’, ‘GoldenReinders’, ‘Jonagored’, ‘Pinova’, ‘Wellant’) cultivars commonly grown in Belgium. We also investigatedwhether insect flower visitation rate and pollination efficiency are linked to floral resource quantityand quality. The pear cultivars flowered one week before the apple cultivars in early spring, and theirflowers were about six times less visited by insects. The visitors foraged more on the pollen of the peartrees and the nectar of the apple trees.
Alexander M.P. Differential staining of aborted and non-aborted pollen. Stain Technol. 1969, 44:117-122.
Allsopp M.H., Lange W.J., de Veldtman R. Valuing insect pollination services with cost of replacement. PLoS One 2008, 3:e3128. 10.1371/journal.pone.0003128.
Behmer S.T., Nes W.D. Insect sterol nutrition and physiology: a global overview. Advances in Insect Physiology 2003, 1-72. Elsevier.
Benedek P., Nyeki J. Considerations on the nectar production and the honeybee visitation of fruit tree flowers. Hortic. Sci. 1997, 29:117-122.
Benedek P., Béres I., Nyéki J. Competition between pear flowers, flowering weeds and other fruit trees for honeybee pollination. Acta Hortic. 1998, 475:417-426. 10.17660/ActaHortic.1998.475.49.
Benedek P., Szabó T., Nyéki J. New results on the bee pollination of quince (Cydonia oblonga Mill.). Acta Hortic. 2001, 561:243-248. 10.17660/ActaHortic.2001.561.35.
Blitzer J.E., Gibbs J., Park M.G., Danforth B.N. Pollination services for apple are dependent on diverse wild bee communities. Agric. Ecosyst. Environ. 2016, 221:1-7. 10.1016/j.agee.2016.01.004.
Broothaerts W., Nerum I.V., Keulemans J. Update on and review of the incompatibility (S-) genotypes of apple cultivars. HortScience 2004, 39:943-947.
Calzoni G.L., Speranza A. Pear and plum pollination: honey bees, bumble bees or both?. Acta Hortic. 1996, 423:83-90. 10.17660/ActaHortic.1996.423.10.
Chapman R.F. The Insects: Structure and Function 2012, Cambridge University Press. 5th ed.
Cnaani J., Thomson J.D., Papaj D.R. Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 2006, 112:278-285. 10.1111/j.1439-0310.2006.01174.x.
Cohen A.C. Insect Diets: Science and Technology 2004, CRC Press, Boca Raton, USA.
Corbet S.A. Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 2003, 34:1-10. 10.1051/apido:2002049.
Díaz P.C., Arenas A., Fernández V.M., Martin C.S., Basilio A.M., Farina W.M. Honeybee cognitive ecology in a fluctuating agricultural setting of apple and pear trees. Behav. Ecol. 2013, 24:1058-1067. 10.1093/beheco/art026.
Faoro I.D., Orth A.I. Nectar production and quality in Japanese pear cultivars in south Brazil. Acta Hortic. 2011, 909:409-414. 10.17660/ActaHortic.2011.909.46.
Faoro I.D., Orth A.I. Flower visiting insects during the bloom period of japanese pear orchards in Brazil. Acta Hortic. 2015, 1094:275-279. 10.17660/ActaHortic.2015.1094.35.
Farkas Á., Orosz-Kovács Z. Nectar secretion dynamics of Hungarian local pear cultivars. Plant Syst. Evol. 2003, 238:57-67. 10.1007/s00606-003-0268-7.
Farkas A., Zajácz E. Nectar production for the Hungarian honey industry. Eur. J. Plant Sci. Biotechnol. 2007, 1:125-151.
Farkas A., Orosz-Kovács Z., Szabó L.G. Insect attraction of flowers in pear cultivars. Acta Hortic. 2002, 596:773-776. 10.17660/ActaHortic.2002.596.133.
Farkas A., Szabo L.G., Orosz-Kovacs Z. Nectar composition in some pear cultivars. Acta Hortic. 2002, 596:761-765. 10.17660/ActaHortic.2002.596.131.
Garibaldi L.A., Steffan-Dewenter I., Kremen C., Morales J.M., Bommarco R., Cunningham S.A., Carvalheiro L.G., Chacoff N.P., Dudenho J.H., Greenleaf S.S., Holzschuh A., Isaacs R., Krewenka K., Mandelik Y., Mayfield M.M., Morandin L.A., Potts S.G., Ricketts T.H., Szentgyörgyi H., Viana B.F., Westphal C., Winfree R., Klein A.M. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 2011, 14:1062-1072. 10.1111/j.1461-0248.2011.01669.x.
Garibaldi L.A., Steffan-Dewenter I., Winfree R., Aizen M.A., Bommarco M., Cunningham S.A., Kremen C., Carvalheiro L.G., Harder L.D., Afik O., Bartomeus I., Benjamin F., Boreux V., Cariveau D., Chacoff N.P., Dudenhöffer J.H., Freitas B.M., Ghazoul J., Greenleaf S., Hipólito J., Holzschuh A., Howlett B., Isaacs R., Javorek S.K., Kennedy C.M., Krewenka K.M., Krishnan S., Mandelik Y., Mayfield M.M., Motzke I., Munyuli T., Nault B.A., Otieno M., Petersen J., Pisanty G., Potts S.G., Rader R., Ricketts T.H., Rundlöf M., Seymour C.L., Schüepp C., Szentgyörgyi H., Taki H., Tscharntke T., Vergara C.H., Viana B.F., Wanger T.C., Westphal C., Williams N., Klein A.M. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 2013, 339:1608-1611. 10.1126/science.1230200.
Garratt M.P.D., Truslove C.L., Coston D.J., Evans R.L., Moss E.D., Dodson C., Jenner N., Biesmeijer J.C., Potts S.G. Pollination deficits in UK apple orchards. J. Pollinat. Ecol. 2014, 12:9-14.
Goldway M., Takasaki-Yasuda T., Sanzol J., Mota M., Zisovich A., Stern R.A., Sansavini S. Renumbering the S-rNase alleles of European pears (Pyrus communis L.) and cloning the S109 RNase allele. Sci. Hortic. 2009, 119:417-422. 10.1016/j.scienta.2008.08.027.
González-Teuber M., Heil M. Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal. Behav. 2009, 4:809-813. 10.4161/psb.4.9.9393.
Gupta J.K. An overview of insect pollinators of temperate fruit crops. Acta Hortic. 2005, 696:589-591. 10.17660/ActaHortic.2005.696.103.
Human H., Nicolson S.W., Strauss K., Pirk C.W.W., Dietemann V. Influence of pollen quality on ovarian development in honeybee workers (Apis mellifera scutellata). J. Insect Physiol. 2007, 53:649-655. 10.1016/j.jinsphys.2007.04.002.
Jacquemart A.-L., Michotte-van der Aa A. Tests de parthénocarpie chez les poiriers Pyrus communis L. var. Conférence. Durondeau et Doyenné. Fruit Belge 2003, 505:170-173.
Jacquemart A.-L., Michotte-van der Aa A., Raspé O. Compatibility and pollinator efficiency tests on Pyrus communis L. cv. Conférence. J. Hortic. Sci. Biotechnol. 2006, 81:827-830. 10.1080/14620316.2006.11512145.
Jacquemart A.-L. Methods for determining compatibility and pollinator efficiency in temperate fruit species. Fruit Veg. Cereal Sci. Biotechnol. 2007, 1:26-38.
Janson E.M., Grebenok R.J., Behmer S.T., Abbot P. Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. J. Chem. Ecol. 2009, 35:1309-1319. 10.1007/s10886-009-9713-6.
Kearns C.A., Inouye D.W. Techniques for Pollination Biologists 1993, University Press of Colorado, Niwot, Colorado.
Moquet L., Mayer C., Michez D., Wathelet B., Jacquemart A.L. Early spring floral foraging resources for pollinators in wet heathlands in Belgium. J. Insect. Conserv. 2015, 19:837-848. 10.1007/s10841-015-9802-5.
Martins K.T., Gonzalez A., Lechowicz M.J. Pollination services are mediated by bee functional diversity and landscape context. Agric. Ecosyst. Environ. 2015, 200:12-20. 10.1016/j.agee.2014.10.018.
Matsumoto S. Apple pollination biology for stable and novel fruit production: search system for apple cultivar combination showing incompatibility, semi-compatibility, and full-compatibility based on the S-rNase allele database. Int. J. Agron. 2014, 2014:1-9. 10.1155/2014/138271.
Mayer D.F., Johansen C.A., Burgett D.M. Bee Pollination of Tree Fruits, Pacific Northwest Cooperative Extension Bulletin 1986, Washington State University.
Mayer D.F., Miliczky E.R., Lunden J.D. Pollination of Pears, In: Pear Production in the Pacific Northwest 1990, Davis, CA.
Michener C.D. The Bees of the World 2007, The Johns Hopkins University Press, Baltimore.
Michotte-van der Aa A., Jacquemart A.-L. Les principales variétés de poirier cultivées en Belgique (Pyrus communis L., var. Conference, var. Doyenné et var. Durondeau) sont-elles compatibles intra-variété?. Fruit Belge 2003, 503:107-112.
Moerman R., Vanderplanck M., Roger N., Declèves S., Wathelet B., Rasmont P., Fournier D., Michez D. Growth rate of bumblebee larvae is related to pollen amino acids. J. Econ. Entomol. 2015, tov279. 10.1093/jee/tov279.
Monzón V.H., Bosch J., Retana J. Foraging behavior and pollinating effectiveness of Osmia cornuta (Hymenoptera: megachilidae) and Apis mellifera (Hymenoptera: apidae) on Comice pear. Apidologie 2004, 35:575-585. 10.1051/apido:2004055.
Oksanen J., Kindt R., Legendre P., O'Hara B., Stevens M.H.H., Oksanen M.J., Suggests M. The vegan package. Community Ecol. Package 2007, 631-637.
Orosz-Kovács Z., Szabó L.G., Szabó T., Botz L., Bubán T., Majer-Bordács M., Tóth E.N. Sugar components and refraction of the floral nectar in apple cultivars. Hortic. Sci. 1997, 29:123-128.
Percival M.S. Types of nectar in angiosperms. New Phytol. 1961, 60:235-281.
Quinet M., Jacquemart A.-L. Difference between pollination and parthenocarpy in the Conférence pear production. Acta Hortic. 2015, 1094:359-366. 10.17660/ActaHortic.2015.1094.45.
Quinet M., Kelecom S., Jacquemart A.-L. S-genotype characterization of 13 north western european pear (Pyrus communis) cultivars. Sci. Hortic. 2014, 165:1-4. 10.1016/j.scienta.2013.10.023.
RDevelopment C., 2012. TEAM 2009: R: A language and environment for statistical computing Vienna Austria Internet Httpwww R-Proj. Org.
Rader R., Bartomeus I., Garibaldi L.A., Garratt M.P.D., Howlett B.G., Winfree R., Cunningham S.A., Mayfield M.M., Arthur A.D., Andersson G.K.S., Bommarco R., Brittain C., Carvalheiro L.G., Chacoff N.P., Entling M.H., Foully B., Freitas B.M., Gemmill-Herren B., Ghazoul J., Griffin S.R., Gross C.L., Herbertsson L., Herzog F., Hipólito J., Jaggar S., Jauker F., Klein A.-M., Kleijn D., Krishnan S., Lemos C.Q., Lindström S.A.M., Mandelik Y., Monteiro V.M., Nelson W., Nilsson L., Pattemore D.E., Pereira N., de O., Pisanty G., Potts S.G., Reemer M., Rundlöf M., Sheffield C.S., Scheper J., Schüepp C., Smith H.G., Stanley D.A., Stout J.C., Szentgyörgyi H., Taki H., Vergara C.H., Viana B.F., Woyciechowski M. Non-bee insects are important contributors to global crop pollination. Proc. Natl. Acad. Sci. 2015, 113:146-151. 10.1073/pnas.1517092112.
Ramírez F., Davenport T.L. Apple pollination: a review. Sci. Hortic. 2013, 162:188-203. 10.1016/j.scienta.2013.08.007.
Reille M., 1992. Pollen et spores d'Europe et d'Afrique du Nord. Laboratoire de Botanique historique et Palynologie, Marseille, France.
Roulston T.H., Cane J.H. Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 2000, 222:187-209. 10.1007/BF00984102.
Sakamoto D., Hayama H., Ito A., Kashimura Y., Moriguchi T., Nakamura Y. Spray pollination as a labor-saving pollination system in Japanese pear (Pyrus pyrifolia (Burm.f.) Nakai): development of the suspension medium. Sci. Hortic. 2009, 119:280-285. 10.1016/j.scienta.2008.08.009.
Sanzol J., Herrero M. The effective pollination period in fruit trees. Sci. Hortic. 2001, 90:1-17. 10.1016/S0304-4238(00)00252-1.
Sanzol J., Rallo P., Herrero M. Stigmatic receptivity limits the effective pollination period in 'Agua de Aranjuez' pear. J. Am. Soc. Hortic. Sci. 2003, 128:458-462.
Sedivy C., Müller A., Dorn S. Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen. Funct. Ecol. 2011, 25:718-725. 10.1111/j.1365-2435.2010.01828.x.
Sharifani M., Jackson J.F. Nectar analysis, pollen production and anthocyanin measurements revealed distinct variations in pears. Acta Hortic. 2004, 636:415-422. 10.17660/ActaHortic.2004.636.51.
Sheffield C.S. Pollination, seed set and fruit quality in apple: studies with Osmia lignaria (Hymenoptera Megachilidae) in the Annapolis Valley, Nova Scotia. Canada.J. Pollinat. Ecol. 2014, 12:120-128.
Somme L., Vanderplanck M., Michez D., Lombaerde I., Moerman R., Wathelet B., Wattiez R., Lognay G., Jacquemart A.-L. Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 2014, 46:92-106. 10.1007/s13592-014-0307-0.
Stern R.A., Eisikowitch D., Dag A. Sequential introduction of honeybee colonies and doubling their density increases cross-pollination, fruit-set and yield in 'red delicious'apple. J. Hortic. Sci. Biotechnol. 2001, 76:17-23.
Stern R.A., Goldway M., Zisovich A.H., Shafir S., Dag A. Sequential introduction of honeybee colonies increases cross- pollination, fruit-set and yield of Spadona pear (Pyrus communis L.). J. Hortic. Sci. Biotechnol. 2004, 79:652-658.
Stern R.A., Sapir G., Shafir S., Goldway M. The appropriate management of honey bee colonies for pollination of Rosaceae fruit trees in warm climates. Middle East. Russ. J. Plant Sci. Biotechnol. 2007, 1:13-19.
Suzuki R., Shimodaira H. Pvclust: an R package for assessing the incertainty in hierarchical clustering. Bioinformatics 2006, 22:1540-1542.
Tóth E.N., Szabó L.G., Botz L., Orosz-Kovács Z. Effect of rootstocks on floral nectar composition in apple cultivars. Plant Syst. Evol. 2003, 238:43-55. 10.1007/s00606-002-0274-1.
Tassinari P., Zuccherelli S., Sansavini S. Self pollination and fertility in European pear (Pyrus communis L.) cultivars. Acta Hortic. 2003, 663:677-680. 10.17660/ActaHortic.2004.663.122.
Van den Eijnde J. Pollination of pear by bumblebees (Bombus terrestris L.) and honeybees (Apis mellifera L.). Acta Hortic. 1996, 423:73-81. 10.17660/ActaHortic.1996.423.8.
Vanderplanck M., Michez D., Vancraenenbroeck S., Lognay G. Micro-quantitative method for analysis of sterol levels in honeybees and their pollen loads. Anal. Lett. 2011, 44:1807-1820. 10.1080/00032719.2010.526271.
Vanderplanck M., Leroy B., Wathelet B., Wattiez R., Michez D. Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie 2014, 45:192-204. 10.1007/s13592-013-0239-0.
Vanderplanck M., Moerman R., Rasmont P., Lognay G., Wathelet B., Wattiez R., Michez D. How does pollen chemistry impact development and feeding behaviour of polylectic bees?. PLoS One 2014, 9:e86209. 10.1371/journal.pone.0086209.
Viana B.F., da Encarnação Coutinho J.G., Garibaldi L.A., Bragança Castagnino G.L., Peres Gramacho K., Oliveira Silva F. Stingless bees further improve apple pollination and production. J. Poll. Ecol. 2014, 14:261-269.
Warnier O. Quelle est l'intérêt d'une pollinisation croisée en Conférence. Fruit Belge 2000, 484:47-50.
Webster A.D. Factors influencing the flowering, fruit set and fruit growth of European pears. Acta Hortic. 2002, 596:699-709. 10.17660/ActaHortic.2002.596.121.
Weiner C.N., Hilpert A., Werner M., Linsenmair K.E., Blüthgen N. Pollen amino acids and flower specialisation in solitary bees. Apidologie 2010, 41:476-487. 10.1051/apido/2009083.
de Groot A.P. Protein and amino acid requirements of the honeybee (Apis mellifera L.). Physiol. Comp. Oecol. 1953, 3:1-90.
