Digestion of pollen components by larvae of the flower-specialist bee Chelostoma florisomne (Hymenoptera: Megachilidae)

Journal of Insect Physiology

Volumn 43, Issue 1, 1997, Pages 89-100

  Dobson, Heidi E M ^a,b   Peng, Ying Shin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WHITMAN COLLEGE   (United States)

Author keywords

Histology; Nutrition; Oligolecty; Ranunculus spp.

Indexed keywords

CHELOSTOMA FLORISOMNE;

EID: 0030758120     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-1910(96)00024-8     Document Type: Article

References (130)

1. Baker H.G., Baker I. Starch in angiosperm grains and its evolutionary significance. Amer. J. Bot. 66:1979;591-600.
2. Baker H. G. and Baker I. (1983) Some evolutionary and taxonomic implications of variation in the chemical reserves of pollen. In: Pollen: Biology and Implications for Plant Breeding, (Eds Mulcahy D. L. and Ottaviano E.), pp. 43-52. Elsevier Sci., New York.
3. Bancroft J. D. and Stevens A. (1977) Theory and Practice of Histological Techniques. Churchill Livingstone, Edinburgh.
4. Barker R.J., Lehner Y. A look at honey bee gut functions. Amer. Bee J. 112:1972;336-338.
5. Barker R.J. Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. J. Nutr. 107:1977;1859-1862.
6. Benedict J.H., Wolfenbarger D.A., Bryant V.M. Jr., George D.M. Pollen ingested by boll weevils (Coleoptera: Curculionidae) in Southern Texas and Northeastern Mexico. J. Econ. Entomol. 84:1991;126-131.
7. Bergström G., Dobson H.E.M., Groth I. Spatial fragrance patterns within the flowers of Ranunculus acris (Ranunculaceae). Pl. Syst. Evol. 195:1995;221-242.
8. Bertholf L.M. The utilization of carbohydrates as food by honeybee larvae. J. Agric. Res. 35:1927;429-452.
9. Bohart G.E., Youssef N.N. The biology and behavior of Evylaeus galpinsiae Cockerell (Halictidae). Wasmann J. Biol. 34:1976;185-234.
10. Bonomi A., Marletto F., Lucchelli L., Anghinetti A., Bonomi A., Sabbioni A. Composizione chimico-bromatologica della gelatina reale in rapporto alla flora nettarifera e pollinifera. Rev. Soc. Ital. Sci. Aliment. 15:1986;53-62.
11. Brian A.D. The pollen collected by bumble-bees. J. Anim. Ecol. 20:1951;191-194.
12. Brice A.T., Dahl K.H., Grau C.R. Pollen digestibility by hummingbirds and Psittacines. Condor. 91:1989;681-688.
13. Campana B.J., Moeller F.E. Honey bees: preference for and nutritive value of pollen from five plant sources. J. Econ. Entomol. 70:1977;39-41.
14. Carretero B., Rodríguez-García M.I. The pollen grain wall as a site for passage of lanthanum in tomato, Lycopersicon esculentum (Solanaceae). Amer. J. Bot. 82:1995;31-36.
15. Chauvin R. (1968) Digestion et nutrition des adultes. In: Traité de biologie de l'abeille (Ed. Chauvin R.), Vol. 1, pp. 347-377. Masson et Cie, Paris.
16. Chayen J., Bitensky L., Butcher R. and Poulter L. (1969) A Guide to Practical Histology, Oliver and Boyd, Edinburg.
17. Churchill D.M., Christensen P. Observations on pollen harvesting by brush-tongued lorikeets. Aust. J. Zool. 18:1970;427-437.
18. Corbet S.A. Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Entomol. 10:1985;143-153.
19. Coville R.E., Frankie G.W., Buchmann S.L., Vinson S.B., Williams H.J. Nesting and male behavior of Centris heithausi (Anthophoridae) in Costa Rica with chemical analysis of the hindleg glands of males. J. Kansas Entomol. Soc. 59:1986;325-336.
20. Cox P.A. Chiropterophily and ornithophily in Freycinetia (Pandanaceae) in Samoa. Pl. Syst. Evol. 144:1984;277-290.
21. Crailsheim K., Hrassnigg N., Gmeinbauer R., Szolderits M.J., Schneider L.H.W., Brosch U. Pollen utilization in non-breeding honeybees in winter. J. Insect Physiol. 39:1993;369-373.
22. Crailsheim K., Schneider L.H.W., Hrassnigg N., Bühlmann G., Brosch U., Gmeinbauer R., Schöffmann B. Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. J. Insect Physiol. 38:1992;409-419.
23. Cruz-Landim C. Avaliacao fotografica da digestao do polen presente no intestino de operarias de Apis mellifera L. (Hymenoptera, Apidae). Naturalia. 10:1985;27-36.
24. Cruz-Landim C., Serrao J.E. The evolutive significance of pollen use as protein resource by Trigonini bees (Hymenoptera, Apidae, Meliponinae). J. Adv. Zool. 15:1994;1-5.
25. Czeczuga B. Investigation on carotenoids in insects, IV: the occurrence of particular carotenoids in Apis mellifera L. (Apidae). Apidologie. 12:1981;107-112.
26. Dadd R.H. Insect nutrition: current developments and metabolic implications. Ann. Rev. Entomol. 18:1973;381-420.
27. De Groot A.P. Protein and amino acid requirements of the honeybee (Apis mellifera L.). Physiol. Comp. Oecol. 3:1953;197-285.
28. Dietz A. Initiation of pollen consumption and pollen movement through the alimentary canal of newly emerged honey bees. Ann. Entomol. Soc. Amer. 62:1969;43-46.
29. Dobson H. E. M. (1985) Pollen and pollen-coat lipids: chemical survey and role in pollen selection by solitary bees. PhD Dissertation in Botany, Univ. California at Berkeley.
30. Dobson H.E.M. Role of flower and pollen aromas in host-plant recognition by solitary bees. Oecologia. 72:1987;618-623.
31. Dobson H.E.M. Survey of pollen and pollenkitt lipids - chemical cues to flower visitors? Am. J. Bot. 75:1988;170-182.
32. Dobson H. E. M. (1994) Floral volatiles in insect biology. In: Insect-plant Interactions Vol. V, (Ed. Bernays E. A.), pp. 47-81. CRC Press, Boca Raton.
33. Doull K.M. Effects of attractants and phagostimulants in pollen and pollen supplement on the feeding behaviour of honeybees in the hive. J. Apic. Res. 13:1974;47-54.
34. Downes J.A. The food habits and description of Atrichopogon pollinivorus sp. n. Trans R. Ent. Soc. Lond. 106:1955;439-453.
35. Dulberger R. The apertural wall in pollen in Linum grandiflorum. Annals. Bot. 63:1989;421-431.
36. Faegri K. and van der Pijl L. (1979) The Principles of Pollination Ecology, 3rd edn. Pergamon Press, Oxford.
37. Feltwell J. (1978) The distribution of carotenoids in insects. In: Biochemical Aspects of Plant and Animal Coevolution (Ed. Harborne J. B.), pp. 277-306. Acad. Press, New York.
38. Gilbert F.S. Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecol. Entomol. 6:1981;245-262.
39. Gilbert L.E. Pollen feeding and reproductive biology of Heliconius butterflies. Proc. Nat. Acad. Sci. U.S.A. 69:1972;1403-1407.
40. Gilliam M., Prest D.B. Microbiology of feces of the larval honey bee, Apis mellifera. J. Invert. Path. 49:1987;70-75.
41. Gilliam M., Lorenz B.J., Richardson G.V. Digestive enzymes and micro-organisms in honey bees, Apis mellifera: influence of streptomycin, age, season and pollen. Microbios. 55:1988;95-114.
42. Gilliam M., Buchmann S.L., Lorenz B.J., Schmalzel R.J. Bacteria belonging to the genus Bacillus associated with three species of solitary bees. Apidologie. 21:1990;99-105.
43. Goldingay R.L. The foraging behavior of a nectar feeding marsupial, Petaurus australis. Oecologia. 85:1990;191-199.
44. Grinfel'd E. K. (1959) The feeding of thrips (Thysanoptera) on the pollen of flowers and the origin of asymmetry in their mouthparts. Entomol. Rev. 38, 798-804 (in Russian) (pp. 715-720 in English version).
45. Guirguis G.N., Brindley W.A. Insecticide susceptibility and response to selected pollens of larval alfalfa leafcutting bees, Megachile pacifica (Panzer). Environ. Entomol. 3:1974;691-694.
46. Haydak M. H. (1968) Nutrition des larves d'abeilles. In: Traité de Biologie de L'Abeille (Ed. Chauvin R.), Vol. 1, pp. 302-333. Masson et Cie, Paris.
47. Haydak M.H. Honey bee nutrition. Ann. Rev. Entomol. 15:1970;143-156.
48. Herbert E.W., Shimanuki H., Shasha S. Brood rearing and food consumption by honeybee colonies fed pollen substitutes supplemented with starch-encapsulated pollen extracts. J. Apic. Res. 19:1980;115-118.
49. Hesse M. Cytology and morphogenesis of pollen and spores. Prog. Bot. 56:1995;33-55.
50. Hohmann H. Über die Wirkung von Pollenextrakten und Duftstoffen auf das Sammel- und Werbeverhalten höselnder Bienen (Apis mellifica L.). Apidologie. 1:1970;157-178.
51. Holloway B.A. Pollen-feeding in hover-flies (Diptera: Syrphidae). New Zealand J. Zool. 3:1976;339-350.
52. Hopkins C.Y., Jevans A.W., Boch R. Occurrence of octadeca-trans-2, cis-9, cis-12-trienoic acid in pollen attractive to the honeybee. Can. J. Bot. 47:1969;433-436.
53. Howell D.J. Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp. Biochem. Physiol. 48A:1974;263-276.
54. Hunt J.H., Brown P.A., Sago K.M., Kerker J.A. Vespid wasps eat pollen (Hymenoptera: Vespidae). J. Kansas Entomol. Soc. 64:1991;127-130.
55. Hüsing J. O. (1968) Histologie et cytologie de l'intestin. In: Traité de Biologie de L'Abeille (Ed. Chauvin R.), Vol. 1, pp. 334-346. Masson et Cie, Paris.
56. Kevan P.G., Kevan D.K. Collembola as pollen feeders and flower visitors with observations from the high arctic. Quaestiones entomologicae. 6:1970;311-326.
57. Kirk W.D.J. Pollen-feeding in thrips (Insecta: Thysanoptera). J. Zool., Lond. 204:1984;107-117.
58. Klungness L.M., Peng Y.-S. A scanning electron microscopic study of pollen loads collected and stored by honeybees. J. Apic. Res. 22:1983;264-271.
59. Klungness L.M., Peng Y.-S. A histochemical study of pollen digestion in the alimentary canal of honeybees (Apis mellifera L.). J. Insect Physiol. 30:1984;511-521.
60. Klungness L.M., Peng Y.S. Scanning electron microscope observations of pollen food bolus in the alimentary canal of honeybee (Apis mellifera L.). Canad. J. Zool. 62:1984;1316-1319.
61. Knoll F. Über Pollenkitt und Bestaubungsart. Zeit. Bot. 23:1930;609-675.
62. Kress W.J., Stone D.E. Nature of the sporoderm in monocotyledons, with special reference to the pollen grains of Canna and Heliconia. Grana. 21:1982;129-148.
63. Kroon G.H., van Praagh J.P., Velthuis H.H.W. Osmotic shock as a prerequisite to pollen digestion in the alimentary tract of the worker honeybee. J. Apic. Res. 13:1974;177-181.
64. Law B.S. Physiological factors affecting pollen use by Queensland blossom bats (Syconycteris australis). Func. Ecol. 6:1992;257-264.
65. Leereveld H. Anthecological relations between reputedly anemophilous flowers and syrphid flies, III. Worldwide survey of crop and intestine contents of certain anthophilous syrphid flies. Tijd. Entomol. 125:1982;25-35.
66. Lepage M., Boch R. Pollen lipids attractive to honeybees. Lipids. 3:1968;530-534.
67. Levin M. D. and Bohart G. E. (1955) Selection of pollens by honey bees. Amer. Bee J. 95, 392-393, 402.
68. Levin M.D., Haydak M.H. Comparative value of different pollens in the nutrition of Osmia lignaria. Bee World. 38:1957;221-226.
69. Linsley E.G. The ecology of solitary bees. Hilgardia. 27:1958;543-599.
70. Lockwood J.A., Bomar C.R. Consumption of Prickly Pear Cactus flowers by Melanoplus occidentalis: a coevolutionary association? Environ. Entomol. 21:1992;1301-1307.
71. Loper G.M., Berdel R.L. The effects of nine pollen diets on broodrearing of honeybees. Apidologie. 11:1980;351-359.
72. Loper G.M., Cohen A.C. The caloric content of bee-gathered pollen. Amer. Bee J. 122:1982;709-710.
73. Loper G.M., Cohen A.C. Amino acid content of dandelion pollen, a honey bee (Hymenoptera: Apidae) nutritional evaluation. J. Econ. Entomol. 80:1987;14-17.
74. Louveaux J. Recherches sur la récolte du pollen par les abeilles (Apis mellifica L.). Ann. Abeille. 2:1959;13-111.
75. Louw G.N., Nicolson S.W. Thermal, energetic and nutritional considerations in the foraging and reproduction of the carpenter bee Xylocopa capitata. J. Ent. Soc. Sth. Afr. 46:1983;227-240.
76. Maurizio A. Pollenernahrung und Lebensvorgange bei der Honigbiene (Apis mellifera L.). Landwirtsch. Jahrb. Schweiz. 68:1954;115-182.
77. Maurizio A. (1960) Bienenbotanik. In: Biene und Bienenzucht (Eds Budel A. and Herold E.), pp. 68-104. Ehrenwirth Verlag, München.
78. Michener C. D. (1974) The Social Behavior of the Bees: a Comparative Study. Harvard Univ. Press, Cambridge.
79. Nalepa C.A., Bambara S.B., Burroughs A.M. Pollen and nectar feeding by Chilocorus kuwanae (Silvestri) (Coleoptera: Coccinellidae). Proc. Entomol. Soc. Wash. 94:1992;596-597.
80. Neff J.L. Observations on the biology of Eremapsis parvula Oglobin an anthophorid bee with a metasomal scopa (Anthophoridae). Pan-Pac. Entomol. 60:1984;155-162.
81. Nelson E.V., Roberts R.B., Stephen W.P. Rearing larvae of the leaf-cutter bee Megachile rotundata on artificial diets. J. Apic. Res. 11:1972;153-156.
82. Nicolson S.W. Pollen feeding in the eucalypt nectar fly, Drosophila flavohirta. Physiol. Entomol. 19:1994;58-60.
83. Ouyang Y., Grafton-Cardwell E.E., Bugg R.L. Effects of various pollens on development, survivorship, and reproduction of Euseius tularensis (Acari: Phytoseiidae). Environ. Entomol. 21:1992;1371-1376.
84. Parker R. L. (1926) The collection and utilization of pollen by the honeybee. Agric. Exp. Sta. Cornell Univ. Mem., No. 98.
85. Peng Y.-S., Nasr M.E., Marston J.E., Fang Y. The digestion of dandelion pollen by adult worker honeybees. Physiol. Entomol. 10:1985;75-82.
86. Peng Y.-S., Nasr M.E., Marston J.M. Release of alfalfa, Medicago sativa, pollen cytoplasm in the gut of the honey bee, Apis mellifera (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 79:1986;804-807.
87. Phillips E.F. The utilization of carbohydrates by honeybees. J. Agric. Res. 35:1927;385-428.
88. Rickson F.R., Cresti M., Beach J.H. Plant cells which aid in pollen digestion within a beetle's gut. Oecologia. 82:1990;424-426.
89. Robinson F.A., Nation J.L. Substances that attract caged honeybee colonies to consume pollen supplements and substitutes. J. Apic. Res. 7:1968;83-88.
90. Robinson F.A., Nation J.L. Long-chain fatty acids in honeybees in relation to sex, caste, and food during development. J. Apic. Res. 9:1970;121-127.
91. Rogers C.E. Sunflower moth: feeding behavior of the larva. Environ. Entomol. 7:1978;763-765.
92. Roubik D. W., 1989. Ecology and Natural History of Tropical Bees. Cambrige University Press, Cambridge.
93. Royce L.A., Krantz G.W. Observations on pollen processing by Pneumolaelaps longanalis (Acari: Laelapidae), a mite associate of bumblebees. Exp. Appl. Acarol. 7:1989;161-165.
94. Sala-Llinares A., Suárez-Cervera M., Seoane-Camba J., Márquez J. Ultrastructural modifications in pollen grains stored by honey bees (Apis mellifera L.). J. Apic. Res. 31:1992;53-64.
95. Schmidt J O. Phagostimulants in pollen. J. Apic. Res. 24:1985;107-114.
96. Schmidt J.O., Buchmann S.L. Pollen digestion and nitrogen utilization by Apis mellifera L. (Hymenoptera: Apidae). Comp. Biochem. Physiol. 82A:1985;499-503.
97. Schmidt J.O., Johnson B.E. Pollen feeding preference of Apis mellifera, a polylectic bee. Southwest. Entomol. 9:1984;41-47.
98. Schmidt J.O., Buchmann S.L., Glaiim M. The nutritional value of Typha latifolia pollen for bees. J. Apic. Res. 28:1989;155-165.
99. Schmidt J.O., Thoenes S.C., Levin M.D. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann. Entomol. Soc. Amer. 80:1987;176-183.
100. Scott H.G., Stojanovich C.J. Digestion of juniper pollen by Collembola. Florida Entomol. 46:1963;188-191.
101. Shaw D.E. The incidental collection of fungal spores by bees and the collection of spores in lieu of pollen. Bee World. 71:1990;158-176.
102. Siegfried B.D., Mullin C.A. Effects of alternative host plants on longevity, oviposition, and emergence of Western and Northern Corn Rootworms (Coleoptera: Chrysomelidae). Environ. Entomol. 19:1990;474-480.
103. Simpson B. B. and Neff J. (1983) Evolution and diversity of floral rewards. In: Handbook of Experimental Pollination Biology (Eds Jones C. E. and Little R. J.), pp. 142-159. Sci. Acad. Press, New York.
104. Smith A.P., Green S.W. Nitrogen requirements of the sugar glider (Petaurus breviceps), an ominivorous marsupial, on a honey-pollen diet. Physiol. Zool. 60:1987;82-92.
105. Southwell I.A., Maddox C.D.A., Zalucki M.P. Metabolism of 1,8-cineole in tea tree (Melaleuca alternifolia and M. linariifolia) by pyrgo beetle (Paropsisterna tigrina). J. Chem. Ecol. 21:1995;439-453.
106. Southworth D. Cytochemical reactivity of pollen walls. J. Histochem. Cytochem. 21:1973;73-80.
107. Southworth D. Solubility of pollen exines. Amer. J. Bot. 61:1974;36-44.
108. Southworth D. (1990) Exine biochemistry. In: Microspores: Evolution and Ontogeny, (Eds Blackmore S. and Knox R. B.), pp. 193-212. Academic Press, London.
109. Ssymank A., Gilbert F. Anemophilous pollen in the diet of Syrphid flies with special reference to the leaf feeding strategy occurring in Xylotini (Diptera, Syrphidae). Dtsch. Ent. Z., N. F. 40:1993;245-258.
110. Stanley R. G. and Linskens H. F. (1974) Pollen: Biology, Biochemistry, Management. Springer-Verlag, New York. 307 pp.
111. Suárez-Cervera M., Marquez J., Bosch J., Seoane-Camba J. An ultrastructural study of pollen grains consumed by larvae of Osmia bees (Hymenoptera, Megachilidae). Grana. 33:1994;191-204.
112. Suárez-Cervera M., Marquez J., Seoane-Camba J. Pollen grain and Ubisch body development in Platanus acerifolia. Rev. Palaeobot. Palynol. 85:1995;63-84.
113. Svoboda J.A., Herbert E.W., Lusby W.R., Thompson M.J. Comparison of sterols of pollens, honeybee workers, and prepupae from field sites. Arch. Insect Biochem. 1:1983;25-31.
114. Svoboda J.A., Herbert E.W., Thompson M.J. Sterols of organs involved in brood food production and of royal jelly in honey bees. Insect Biochem. 16:1986;479-482.
115. Szolderits M.J., Crailsheim K. A comparison of pollen consumption and digestion in honeybee (Apis mellifera carnica) drones and workers. J. Insect Physiol. 39:1993;877-881.
116. Tasei J.N., Masure M.M. Sur quelques facteurs influençant le dévelopment de Megachile pacifica Panz. (Megachilidae). Apidologie. 9:1978;173-290.
117. Tepedino V.J. Notes on the reproductive biology of Zigadenus paniculatus, a toxic range plant. Great Basin Nat. 41:1981;427-430.
118. Thorp R.W. Systematics and ecology of bees of the subgenus Diandrena (Andrenidae). Univ. Calif. Publ. Entomol. 52:1969;1-146.
119. Tompson R. G. and Hunt R. D. (1966) Selected Histochemical and Histopathological Methods, Charles C. Thomas, Springfield, Ill.
120. Todd F.E., Bretherick O. The composition of pollens. J. Econ. Entomol. 35:1942;312-317.
121. Turner V. Banksia pollen as a source of protein in the diet of two Australian marsupials Cercartetus nanus and Tarsipes rostratus. Oikos. 43:1984;3-61.
122. van der Vorst E., Mattys J., Jacobs F.J., De Rycke P.H. Fatty acid and sterol composition during larval development in the honeybee. J. Apic. Res. 22:1983;3-8.
123. Vivino A.E., Palmer L.S. The chemical composition and nutritional value of pollens collected by bees. Arch. Biochem. 4:1944;129-136.
124. Vogel S. Ölblumen und Ölsammelnde Bienen. Trop. Subtrop. Pflanz. 7:1974;285-547.
125. Weber M. The formation of pollenkitt in Apium nodiflorum (Apiaceae). Ann. Bot. 70:1992;573-577.
126. Westrich P. (1989) Die Wildbienen Baden-Württembergs, Vol. I and II. Ulmer Verlag, Stuttgart.
127. Whitcomb W. and Wilson H. F. (1929) Mechanics of digestion of pollen by the adult honey bee and the relation of undigested parts to dysentery of bees. Wisconsin Agric. Exp. Sta. Res. Bull. No. 92.
128. Wightman J.A., Rogers V.M. Growth, energy and nitrogen budgets and efficiencies of the growing larvae of Megachile pacifica (Panzer)(Hymenoptera: Megachilidae). Oecologia. 36:1978;245-257.
129. Wilson B.H., Lieux M. Pollen grains in the guts of field collected tabanids in Louisiana. Ann. Entomol. Soc. Amer. 65:1972;1264-1266.
130. Wooller R.D., Richardson K.C., Pagendham C.M. The digestion of pollen by some Australian birds. Aust. J. Zool. 36:1988;357-362.