Plant Systematics and Evolution

, Volume 222, Issue 1–4, pp 187–209

Pollen nutritional content and digestibility for animals

  • T. H. Roulston
  • J. H. Cane
Article

Abstract

This paper reviews the literature concerning digestion and nutrient content of pollen. Four topics are addressed in detail: 1) The mechanism of pollen digestion by animals; 2) The efficiency of mechanical and digestive removal of pollen content by various animals; 3) Range and taxonomic distribution of pollen nutrients, and 4) Adaptive hypotheses proposed to associate pollen chemistry with pollinator reward. Studies on the mechanism(s) of pollen digestion remain inconclusive, but suggest that differences in digestibility among pollen types may reflect differences in pollen wall porosity, thickness, and composition. Although hummingbirds reportedly digest pollen very poorly, most animals studied, including those that do not regularly consume pollen, can digest 50–100% of ingested grains. Overlooked and recent research of pollen protein content shows that pollen grains may contain over 60% protein, double the amount cited in some studies of pollen-feeding animals. Adaptive hypotheses that associate pollen starch and pollen caloric content with pollinator reward remain unsubstantiated when critically viewed through the lens of phylogeny.

Key words

Pollen chemistry pollen digestion pollination syndrome palynology bees nutrition 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agarwal A., Nair P. K. K. (1989) Free and proteinbound amino acids of pollen ofAcacia auriculaeformis (Mimosaceae). Grana 28: 155–157.Google Scholar
  2. Auclair J. L., Jamieson C. A. (1948) Qualitative analysis of amino acids in pollen collected by bees. Science 108: 357–358.Google Scholar
  3. Baker H. G., Baker I. (1979) Starch in angiosperm pollen grains and its evolutionary significance. Amer. J. Bot. 66: 591–600.Google Scholar
  4. Baker H. G., Baker I. (1983) Some evolutionary and taxonomic implications of variation in the chemical reserves of pollen. In: Mulcahy D. L., Ottaviano E. (eds.) Pollen: Biology and Implications for Plant Breeding. Elsevier, New York, pp. 43–52.Google Scholar
  5. Barbier M. (1970) Chemistry and biochemistry of pollens. Progress in Phytochemistry 2: 1–34.Google Scholar
  6. Barth F. G. (1985) Insects and flowers: the biology of a partnership. Princeton Univ. Press, Princeton, NJ.Google Scholar
  7. Bell R. R., Thornber E. J., Seet J. L. L., Groves M. T., Ho N. P., Bell D. T. (1983) Composition and protein quality of honeybee-collected pollen ofEucalyptus marginata andEucalyptus calophylla. J. Nutr. 113: 2479–2484.Google Scholar
  8. Blum M. S. (1985) Fundamentals of Insect Physiology. John Wiley, USA.Google Scholar
  9. Brice A. T., Dahl K. H., Grau C. R. (1989) Pollen digestibility by hummingbirds and Psittacines. Condor 91: 681–688.Google Scholar
  10. Buchmann S. L. (1986) Vibratile pollination inSolanum andLycopersicon: a look at pollen chemistry. In: D'Arcy W. G. (ed.) Solanaceae: Biology and Systematics. Columbia Univ. Press, NY, pp. 237–252.Google Scholar
  11. Calvino E. M. (1952) Le sostanze de riserva dei pollini e il loro significato, filogenetico, ecologico, embriologico. Nuovo Giornale Botanico Italiano 59: 1–26.Google Scholar
  12. Carisey N., Bauce E. (1997) Impact of balsam fir flowering on pollen and foliage biochemistry in relation to spruce budworm growth, development and food utilization. Entomol. Exp. Appl. 85: 17–31.Google Scholar
  13. Cate J. R., Skinner J. L. (1978) Fate and identification of pollen in the alimentary canal of the boll weevil,Anthonomus grandis. Southwest. Entomol. 3: 263–265.Google Scholar
  14. Ceausescu S., Mosoiu L. (1981) Identification of free amino acids of some single flower pollens in Romania, collected byApis mellifica carpatica. An. Univ. Bucur. Biol. 30: 101–104.Google Scholar
  15. Clark C. J., Lintas C. (1992) Chemical composition of pollen from kiwifruit vines. New Zealand J. Crop. Hort. Sci. 20: 337–344.Google Scholar
  16. Colin L. J., Jones C. E. (1980) Pollen energetics and pollination modes. Amer. J. Bot. 67: 210–215.Google Scholar
  17. Crailsheim K., Schneider L. H. W., Hrassnigg N., Bühlmann G., Broasch U., Gmeinbauer R., Schöffmann B. (1992) Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. J. Insect. Physiol. 38: 409–419.Google Scholar
  18. Crane E. (1977) Dead bees under lime trees. Sugars poisonous to bees. Bee World 58: 129–130.Google Scholar
  19. Crane E. (1978) Sugars poisonous to bees. Bee World 59: 37–38.Google Scholar
  20. Crowson R. A. (1981) The Biology of the Coleoptera. Academic Press, London.Google Scholar
  21. Cruz-Landim C. (1985) Photographic examination of pollen digestion in the intestine of worker honeybees [Portuguese]. Natural 10: 27–36.Google Scholar
  22. Cruz-Landim C., Serrao J. E. (1994) The evolutive significance of pollen use as protein resource by Trigonini bees (Hymenoptera, Apidae, Meliponinae). J. Adv. Zool. 15: 1–5.Google Scholar
  23. Danforth B. N. (1990) Provisioning behavior and the estimation of investment ratios in a solitary bee,Calliopsis (Hypomacrotera)persimilis (Cockerell) (Hymenoptera: Andrenidae). Behav. Ecol. Sociobiol. 27: 159–168.Google Scholar
  24. Detzel A., Wink M. (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecol. 4: 8–18.Google Scholar
  25. Dobson H. E. M. (1987) Role of flower and pollen aromas in host-plant recognition by solitary bees. Oecologia 72: 618–623.Google Scholar
  26. Dobson H. E. M. (1988) Survey of pollen and pollenkitt lipids — chemical cues to flower visitors? Amer. J. Bot. 75: 170–182.Google Scholar
  27. Dobson H. E. M. (1994) Floral volatiles in insect biology. In: Bernays E. A. (ed.) Insect-Plant Interactions, vol 5. CRC Press, Boca Raton, FL, pp. 47–81.Google Scholar
  28. Dobson H. E. M., Peng Y. S. (1997) Digestion of pollen components by larvae of the flowerspecialist beeChelostoma florisomne (Hymenoptera: Megachilidae). J. Insect. Physiol. 43: 89–100.Google Scholar
  29. Downes J. A. (1955) The food habits and description ofAtrichopogon pollinivorus sp.n. (Diptera: Ceratopogonidae). Transactions of the Royal Entomological Society of London 106: 439–453.Google Scholar
  30. Erhardt A., Baker I. (1990) Pollen amino acids — an additional diet for a nectar feeding butterfly? Plant Syst. Evol. 169: 111–121.Google Scholar
  31. Evans D. E., Taylor P. E., Singh M. B., Knox R. B. (1991) Quantitative analysis of lipids and protein from the pollen ofBrassica napus L. Plant Science 73: 117–126.Google Scholar
  32. Franchi G. G., Bellani L., Nepi M., Pacini E. (1996) Types of carbohydrate reserves in pollen: localization, systematic distribution and ecophysiological significance. Flora 191: 143–159.Google Scholar
  33. Franchi G. G., Franchi G., Corti P., Pompella A. (1997) Microspectrophotometric evaluation of digestibility of pollen grains. Plant Food Hum. Nutr. 50: 115–126.Google Scholar
  34. Gherardini G. L., Healey P. L. (1969) Dissolution of outer wall of pollen grain during pollination. Nature 224: 718–719.Google Scholar
  35. Gilbert L. E. (1972) Pollen feeding and reproductive biology ofHeliconius butterflies. Proc. Natl. Acad. Sci. (USA) 69: 1403–1407.Google Scholar
  36. Gilliam M., McCaughey W. F., Wintermute B. (1980) Amino acids in pollens and nectars of citrus cultivars and in stored pollen and honey from honeybee colonies in citrus groves. J. Apicul. Res. 19: 64–72.Google Scholar
  37. Grant B. R. (1996) Pollen digestion by Darwin's finches and its importance for early breeding. Ecology 77: 489–499.Google Scholar
  38. Grayum M. H. (1985) Evolutionary and ecological significance of starch storage in pollen of the Araceae. Amer. J. Bot. 72: 1565–1577.Google Scholar
  39. Greenberg L. (1982) Year-round culturing and productivity of a sweat bee,Lasioglossum zephyrum (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 55: 13–22.Google Scholar
  40. Grinfel'd E. K. (1959) The feeding of thrips (Thysanoptera) on pollen of flowers and the origin of asymmetry in their mouthparts [Russian]. Entomol. Obozr. 38: 798–804.Google Scholar
  41. Grinfel'd E. K. (1975) Anthophily in beetles (Coleoptera) and a critical evaluation of the cantharophilous hypothesis. Entomol. Rev. 54: 18–22.Google Scholar
  42. De Groot A. P. (1953) Protein and amino acid requirements of the honey bee. Physiol. Comp. Oecol. 3: 1–90.Google Scholar
  43. Haslett J. R. (1983) A photographic account of pollen digestion by adult hoverflies. Physiol. Entomol. 8: 167–171.Google Scholar
  44. Herbert E. W. J. (1992) Honey bee nutrition. In: Graham J. M. (ed.) The Hive and the Honey Bee. Dadant & Sons, Hamilton, IL, pp. 197–233.Google Scholar
  45. Herbert E., Bickley W., Shimanuki H. (1970) The brood-rearing capability of caged honey bees fed dandelion and mixed pollen diets. J. Econ. Entomol. 63: 215–218.Google Scholar
  46. Herrera L. G., Martínez del Rio C. (1998) Pollen digestion by New World bats: effects of processing time and feeding habits. Ecology 79: 2828–2838.Google Scholar
  47. Hesse M. (1979a) Development and ultrastructure of the exine and sticky substance of the pollen in closely related entomophilous and anemophilous angiosperms: Polygonaceae [German]. Flora 168: 558–577.Google Scholar
  48. Hesse M. (1979b) Development and ultrastructure of the exine and the sticky substance of the pollen in closely related entomophilous and anemophilous angiosperms: Salicaceae, Tiliaceae and Ericaceae [German]. Flora 168: 540–557.Google Scholar
  49. Hesse M. (1979c) Ultrastructure and distribution of pollenkitt in insect- and wind-pollinated Acer. [German]. Plant Syst. Evol. 131: 277–289.Google Scholar
  50. Hitchcock J. D. (1959) Poisoning of honey bees by death camas blossoms. Am. Bee J. 99: 418–419.Google Scholar
  51. Howell D. J. (1974) Bats and pollen: physiological aspects of the syndrome of chiropterophily. Comp. Biochem. Physiol. 48A: 263–276.Google Scholar
  52. Hügel M. F. (1962) Étude de quelques constituents du pollen. Ann. Abeille 5: 97–133.Google Scholar
  53. Ibrahim S. H. (1974) Composition of pollen gathered by honeybees from some major sources. Agricultural Research Review, Cairo 52: 121–124.Google Scholar
  54. Johri B. M., Vasil I. K. (1961) Physiology of pollen. Bot. Rev. 27: 325–381.Google Scholar
  55. King L. M., Schaal B. A. (1990) Genotype variation within asexual lineages ofTaraxacum officinale. Proc. Natl. Acad. Sci. (USA) 87: 998–1002.Google Scholar
  56. Kirk W. D. J. (1984) Pollen-feeding in thrips (Insecta: Thysanoptera). J. Zool. 204: 107–117.Google Scholar
  57. Klungness L. M., Peng Y.-S. (1983) A scanning electron microscopic study of pollen loads collected and stored by honeybees. J. Apicul. Res. 22: 264–271.Google Scholar
  58. Klungness L. M., Peng Y.-S. (1984) A histochemical study of pollen digestion in the alimentary canal of honeybees (Apis mellifera L.). J. Insect. Physiol. 30: 511–521.Google Scholar
  59. Knight A. H., Crooke W. M., Shepherd H. (1972) Chemical composition of pollen with particular reference to cation exchange capacity and uronic acid content. J. Sci. Food Agri. 23: 263–274.Google Scholar
  60. Knox D. A., Shimanuki H., Herbert J. T. Jr. (1971) Diet and longevity of adult honey bees. J. Econ. Entomol. 64: 1415–1416.Google Scholar
  61. Kress W. J., Stone D. E., Sellers S. C. (1978) Ultrastructure of exine-less pollen:Heliconia (Heliconiaceae). Amer. J. Bot. 65: 1064–1076.Google Scholar
  62. Kroon G. H., van Praagh J. P., Veltuis H. H. W. (1974) Osmotic shock as a prerequisite to pollen digestion in the alimentary tract of the worker honeybee. J. Apicul. Res. 13: 177–181.Google Scholar
  63. Kwiatkowski A., Lubliner-Mianowska K. (1957) Investigation on the chemical composition of pollen. II. The study of the pollen membranes [Polish]. Acta Soc. Bot. Pol. 26: 501–514.Google Scholar
  64. Law B. S. (1992a) The maintenance nitrogen requirements of the Queensland blossom bat (Syconycteris australis) on a sugar pollen diet — is nitrogen a limiting resource? Physiol. Zool. 65: 634–648.Google Scholar
  65. Law B. S. (1992b) Physiological factors affecting pollen use by Queensland blossom bats (Syconycteris australis). Funct. Ecol. 6: 257–64?.Google Scholar
  66. Lee S. (1978) A factor analysis study of the functional significance of angiosperm pollen. Syst. Bot. 3: 1–19.Google Scholar
  67. Levin M. D., Haydak M. H. (1957) Comparative value of different pollens in the nutrition ofOsmia lignaria. Bee World 38: 221–226.Google Scholar
  68. Lidforss B. (1899) Weitere Beiträge zur Biologie des Pollens. Jahrb. f. Wiss. Bot. 33: 232–312.Google Scholar
  69. Linskens H. F., Mulleneers J. M. L. (1967) Formation of “Instant Pollen Tubes”. Acta Bot. Neerland. 16: 132–142.Google Scholar
  70. Linskens H. F., Schrauwen J. (1969) The release of free amino acids from germinating pollen. Acta Bot. Neerland. 18: 605–614.Google Scholar
  71. Loper G. M., Berdel R. L. (1980) The effects of nine pollen diets on broodrearing of honeybees. Apidolog. 11: 351–359.Google Scholar
  72. Loper G. M., Cohen A. C. (1982) The caloric content of bee-gathered pollen. Am. Bee J. 122: 709–710.Google Scholar
  73. Loper G. M., Cohen A. C. (1987) Amino acid content of dandelion pollen, a honey bee (Hymenoptera: Apidae) nutritional evaluation. J. Econ. Entomol. 80: 14–17.Google Scholar
  74. Lundén R. (1956) Literature on pollen chemistry. Grana Palynologica 1: 3–19.Google Scholar
  75. Mann J. S., Crowson R. A. (1981) The systematic position ofOrsodacne Latr. andSyneta Lac. (Coleoptera: Chrysomelidae), in relation to characters of larvae, internal anatomy and tarsal vestiture. J. Nat. Hist. 15: 727–749.Google Scholar
  76. McCaughey W. F., Gilliam M., Standifer L. N. (1980) Amino acids and protein adequacy for honey bees of pollens from desert plants and other floral sources. Apidolog. 11: 75–86.Google Scholar
  77. McLellan A. R. (1977) Minerals, carbohydrates and amino acids of pollens from some woody and herbaceous plants. Ann. Bot. 41: 1225–1232.Google Scholar
  78. Meeuse B. J. D. (1961) The Story of Pollination. Ronald Press, New York.Google Scholar
  79. De Meillon B., Wirth W. W. (1989) A new pollen feedingAtrichopogon midge from Madagascar, with notes on closely related subsaharan species (Diptera: Ceratopogonidae). Revue Francaise D'Entomologie 11: 85–89.Google Scholar
  80. Milton K., Dintzis F. R. (1981) Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica 13: 177–181.Google Scholar
  81. Moldenke A. R. (1976) California pollination ecology and vegetation types. Phytol. 34: 305–361.Google Scholar
  82. Neff J. L., Simpson B. B. (1997) Nesting and foraging behavior ofAndrena (Callandrena)Rudbeckiae Robertson (Hymenoptera: Apoidea: Andrenidae) in Texas. J. Kans. Entomol. Soc. 70: 100–113.Google Scholar
  83. Nepi M., Pacini E., Pinzauti M. (1997) Preliminary studies on pollen digestibility byOsmia cornuta Latr. (Hymenoptera: Megachilidae). In: Richards K. W. (ed.) Proceedings of the 7th International Symposium on Pollination, Lethbridge, Alberta, Canada, 23–28 June 1996. International Society for Horticultural Science, Leiden, The Netherlands, 435–439.Google Scholar
  84. Nicolson S. W. (1994) Pollen feeding in the eucalypt nectar fly,Drosophila flavohirta. Physiol. Entomol. 19: 58–60.Google Scholar
  85. Nielsen N., Grömmer J., Lundén R. (1955) Investigations on the chemical composition of pollen from some plants. Acta Chemica Scandinavica 9: 1100–1106.Google Scholar
  86. O'Neal R. J., Waller G. W. (1984) On the pollen harvest by the honey bee (Apis mellifera L.) near Tucson, Arizona (1976–1981). Desert Plants 6: 81–109.Google Scholar
  87. Pacini E. (1997) Tapetum character states: analytical keys for tapetum types and activities. Can. J. Bot. 75: 1448–1459.Google Scholar
  88. Parker R. L. (1926) The collection and utilization of pollen by the honeybee. Agric. Exp. Sta. Cornell Univ. Mem. 98.Google Scholar
  89. Paton D. C. (1981) The significance of pollen in the diet of the New Holland Honeyeater,Phylidonyris novaehollandiae (Aves: Meliphagidae). Aust. J. Zool. 29: 217–224.Google Scholar
  90. Peng Y. S., Nasr M. E., Marston J. M., Yuenzhen F. (1985) The digestion of dandelion pollen by adult worker honeybees. Physiol. Entomol. 10: 75–82.Google Scholar
  91. Peng Y. S., Nasr M. E., Marston J. M. (1986) Release of alfalfa,Medicago sativa, pollen cytoplasm in the gut of the honey bee,Apis mellifera (Hymenoptera: Apidae). Ann. Entomol. Soc. Amer. 79: 804–807.Google Scholar
  92. Petanidou T., Vokou D. (1990) Pollination and pollen energetics in Mediterranean ecosystems. Amer. J. Bot. 77: 986–992.Google Scholar
  93. Quin D., Goldingay R., Churchill S., Engel D. (1996) Feeding behaviour and food availability of the yellow-bellied glider in North Queensland. Wildlife Research 23: 637–646.Google Scholar
  94. Rabie A. L., Wells J. D., Dent L. K. (1983) The nitrogen content of pollen protein. J. Apicul. Res. 22: 119–123.Google Scholar
  95. Rayner C. J., Langridge D. F. (1985) Amino acids in bee-collected pollens from Australian indigenous and exotic plants. Aus. J. Exper. Agric. 25: 722–726.Google Scholar
  96. Regali A., Rasmont P. (1995) New bioassays to evaluate diet in orphan colonies ofBombus terrestris [French]. Apidolog. 26: 273–281.Google Scholar
  97. Rhoades D. F., Bergdahl J. C. (1981) Adaptive significance of toxic nectar. Am. Nat. 117: 798–803.Google Scholar
  98. Richardson K. C., Wooller R. D., Collins B. G. (1986) Adaptations to a diet of nectar and pollen in the marsupialTarsipes rostratus (Marsupialia: Tarsipedidae). J. Zool. Lond. 208: 285–297.Google Scholar
  99. Rickson F. R., Cresti M., Beach J. H. (1990) Plant cells which aid in pollen digestion within a beetle's gut. Oecologia 82: 424–426.Google Scholar
  100. Rink G., Carroll E. R., Kung F. H. (1989) Estimation ofJuglans nigra mating system parameters. Forest Science 35: 623–627.Google Scholar
  101. Roulston T. H., Buchmann S. L. (2000) A phylogenetic reconsideration of the pollen starchpollination correlation. Evolutionary Ecology Research (in press).Google Scholar
  102. Roulston T. H., Cane J. H., Buchmann S. L. (2000) What governs the protein content of pollen grains: pollinator preferences, pollenpistil interactions, or phylogeny. Ecol. Monog. (in press).Google Scholar
  103. Samuelson G. A. (1994) Pollen consumption and digestion by leaf beetles. In: Jolivet P. H., Cox M. L. (eds.) Novel aspects of the biology of Chrysomelidae. Kluwer Academic Publishers, The Netherlands, pp. 179–183.Google Scholar
  104. Schmidt J. O., Buchmann S. L. (1985) Pollen digestion and nitrogen utilization byApis mellifera L. (Hymenoptera: Apidae). Comp. Biochem. Physiol. 82A: 499–503.Google Scholar
  105. Schmidt J. O., Johnson B. E. (1984) Pollen feeding preference ofApis mellifera, a polylectic bee. Southwest. Natural. 9: 41–47.Google Scholar
  106. Schmidt J. O., Thoenes S. C., Levin M. D. (1987) Survival of honey bees,Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann. Entomol. Soc. Amer. 80: 176–183.Google Scholar
  107. Schmidt P. J., Schmidt J. O., Weber C. W. (1984) Mesquite pollen as a dietary protein source for mice. Nutrition Reports International 30: 513–522.Google Scholar
  108. Scott H. J., Stojanovich C. T. (1963) Digestion of juniper pollen by Collembola. Fla. Entomol. 46: 189–191.Google Scholar
  109. Scott R. W., Strohl M. J. (1962) Extraction and identification of lipids from loblolly pine pollen. Phytochem. 1: 189–193.Google Scholar
  110. Serrao J. E., Cruz-Landim C. (1996) Microscopic observations of the digestion condition of pollen grains in the midgut of stingless bee larvae. J. Hym. Res. 5: 259–263.Google Scholar
  111. Shah C. V. (1997) Are pollen rewards independent of pollination modes? M.A. Dissertation, California State University, Fullerton.Google Scholar
  112. Simpson B. B., Neff J. L. (1983) Evolution and diversity of floral rewards. In: Jones C. E., Little R. J. (eds.) Handbook of Experimental Pollination Biology. Scientific and Academic Editions, Van Nostrand Reinhold Company, New York, NY, pp. 142–159.Google Scholar
  113. Smith A. P., Green S. W. (1987) Nitrogen requirements of the sugar glider (Petaurus breviceps), an omnivorous marsupial, on a honey-pollen diet. Physiol. Zool. 60: 82–92.Google Scholar
  114. Snodgrass R. E. (1925) Anatomy and physiology of the honey bee. McGraw-Hill, New York.Google Scholar
  115. Solberg Y., Remedios G. (1980) Chemical composition of pure and bee-collected pollen. Meldinger fra Norges Landbrukshoegskole. 59(18): 2–12.Google Scholar
  116. Standifer L. N. (1966) Some lipid constituents of pollens collected by honeybees. J. Apicul. Res. 5: 93–98.Google Scholar
  117. Standifer L. N. (1967) A comparison of the protein quality of pollens for growth-stimulation of the hypopharyngeal glands and longevity of honey bees,Apis mellifera L. (Hymenoptera: Apidae). Insectes Soc. 14: 415–426.Google Scholar
  118. Standifer L. N., McCaughey W. F., Dixon S. E., Gilliam M., Loper M. (1980) Biochemistry and microbiology of pollen collected by honey bees (Apis mellifera L.) from almond,Prunus dulcis. II Protein, amino acids and enzymes. Apidolog. 11: 163–171.Google Scholar
  119. Stanley R. G., Linskens H. F. (1965) Protein diffusion from germinating pollen. Physiol. Plant. 18: 47–53.Google Scholar
  120. Stanley R. G., Linskens H. F. (1974) Pollen: Biology, biochemistry, management. 1st edn. Springer, Heidelberg, Germany.Google Scholar
  121. Suárez-Cervera M., Marquez J., Bosch J., Seoane-Camba J. (1994) An ultrastructural study of pollen grains consumed by larvae ofOsmia bees (Hymenoptera, Megachilidae). Grana 33: 191–204.Google Scholar
  122. Svoboda J. A., Thompson M. J., Herbert E. W. Jr., Shimanuki H. (1980) Sterol utilization in honey bees fed a synthetic diet: analysis of prepupal sterols. J. Insect. Physiol. 26: 291–294.Google Scholar
  123. Svoboda J. A., Thompson M. J., Herbert E. W. Jr., Shortino T. J., Szczepanik-Vanleeuwen P. A. (1982) Utilisation and metabolism of dietary sterols in the honey bee and yellow fever mosquito. Lipids 17: 220–225.Google Scholar
  124. Svoboda J. A., Herbert E. W. Jr., Thompson M. J. (1987) Effects of steroid metabolism inhibitors and ecdysteroid analogs on honey bee sterol metabolism and development. Arch. Insect Biochem. Physiol. 6: 1–8.Google Scholar
  125. Tepedino V. J. (1981) Notes on the reproductive biology ofZigadenus paniculatus, a toxic range plant. Great Basin Natur. 41: 427–430.Google Scholar
  126. Tepedino V. J., Knapp A. K., Eickwort G. C., Ferguson D. C. (1989) Death camasZigadenus nuttallii in Kansas: pollen collectors and a florivore. J. Kans. Entomol. Soc. 62: 411–412.Google Scholar
  127. Thien L. B., Bernhardt P., Gibbs G. W., Pellmyr O., Bergström G., Groth I., McPherson G. (1985) The pollination ofZygogynum (Winteraceae) by a moth,Sabatinca (Micropterigidae): an ancient association? Science 227: 540–543.Google Scholar
  128. Todd F. E., Bretherick O. (1942) The composition of pollens. J. Econ. Entomol. 35: 312–317.Google Scholar
  129. Turner V. (1984)Banksia pollen as a source of protein in the diet of two Australian marsupialsCercartetus nanus andTarsipes rostratus. Oikos 43: 53–61.Google Scholar
  130. Van Der Moezel P. G., Delfs J. C., Pate J. S., Loneragan W. A., Bell D. T. (1987) Pollen selection by honeybees in shrublands of the Northern Sandplains of Western Australia. J. Apicul. Res. 26: 224–232.Google Scholar
  131. Vansell G. H. (1933) A plant poisonous to adult bees. J. Econ. Entomol. 26: 168–170.Google Scholar
  132. Vansell G. H. (1934) Adult bees found dying on spotted loco. J. Econ. Entomol. 27: 635–637.Google Scholar
  133. Van Tets I. G. (1997) Extraction of nutrients fromprotea pollen by African rodents. Belgian Journal of Zoology 127: 59–65.Google Scholar
  134. Vivino E. A., Palmer L. S. (1944) The chemical composition and nutritional value of pollens collected by bees. Arch. Biochem. Biophys. 4: 129–136.Google Scholar
  135. Waldorf E. (1981) The utilization of pollen by a natural population ofEntomobrya socia. Rev. Ecol. Biol. Sol. 18: 397–402.Google Scholar
  136. Wcislo W. T., Cane J. H. (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Ann. Rev. Entomol. 41: 195–224.Google Scholar
  137. Whitcomb W., Wilson H. F. (1929) Mechanics of digestion of pollen by the adult honey bee and the relation of undigested parts to dysentary of bees. Agric. Exp. Sta. Univ. Wisconsin, Madison, Res. Bull. 92.Google Scholar
  138. Wightman J. A., Rogers V. M. (1978) Growth, energy and nitrogen budgets and efficiencies of the growing larvae ofMegachile pacifica (Hymenoptera: Megachilidae). Oecologia 36: 245–257.Google Scholar
  139. Winston M. L. (1987) The biology of the honey bee. Harvard Univ. Press, Cambridge, MA.Google Scholar
  140. Wooller R. D., Richardson K. C., Pagendham C. M. (1988) The digestion of pollen by some Australian birds. Aust. J. Zool. 36: 357–362.Google Scholar
  141. Wu F. S., Murry L. E. (1985) Changes in protein and amino acid content during anther development in fertile and cytoplasmic sterilePetunia. Theor. Appl. Genet. 71: 68–73.Google Scholar

Copyright information

© Springer-Verlag 2000

Authors and Affiliations

  • T. H. Roulston
    • 1
  • J. H. Cane
    • 2
  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA
  2. 2.USDA-ARS Bee Biology and Systematics LabUtah State UniversityLoganUSA

Personalised recommendations