Pollen feeding in the butterfly Heliconius charitonia: Isotopic evidence for essential amino acid transfer from pollen to eggs

Proceedings of the Royal Society B: Biological Sciences

Volumn 270, Issue 1533, 2003, Pages 2631-2636

  O'Brien, Diane M ^a,b,c   Boggs, Carol L ^a   Fogel, Marilyn L ^b  

^a STANFORD UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

^c WELLESLEY COLLEGE   (United States)

Author keywords

Compound specific stable isotope analysis; Essential amino acids; Heliconius; Pollen feeding; Reproductive resource allocation

Indexed keywords

ALANINE; AMINO ACID; ASPARTIC ACID; GLUTAMIC ACID; GLYCINE; PROLINE; SERINE;

AMINO ACID; BUTTERFLY; FECUNDITY; LONGEVITY; POLLEN; RESOURCE ALLOCATION;

AMINO ACID TRANSPORT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BUTTERFLY; CHEMICAL COMPOSITION; CONTROLLED STUDY; EGG LAYING; FEEDING; FEMALE; FERTILITY; GAS CHROMATOGRAPHY; HELICONIUS CHARITONIA; INSECT; LIFESPAN; MASS SPECTROMETRY; NECTAR; NONHUMAN; POLLEN; PRIORITY JOURNAL;

ANIMALIA; HELICONIUS; HELICONIUS CHARITONIA; INSECTA; LEPIDOPTERA; NYMPHALIDAE; PAPILIONOIDEA; ZEA MAYS;

EID: 0347091982     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2003.2552     Document Type: Article

References (36)

1. Alm, J., Ohnmeiss, T. E., Lanza, J. & Vriesenga, L. 1990 Preference of cabbage white butterflies and honey bees for nectar that contains amino acids. Oecologia 84, 53-57.
2. Baker, H. G. 1975 Sugar concentrations in nectars from hummingbird flowers. Biotropica 7, 37-41.
3. Baker, H. G. & Baker, I. 1973 Amino-acids in nectar and their evolutionary significance. Nature 241, 543-545.
4. Beck, J., Muhlenberg, E. & Fiedler, K. 1999 Mud-puddling behavior in tropical butterflies: in search of proteins or minerals? Oecologia 119, 140-148.
5. Boggs, C. L. 1979 Resource allocation and reproductive strategies in several heliconiine butterfly species. PhD thesis, University of Texas at Austin, USA.
6. Boggs, C. L. 1981a Nutritional and life-history determinants of resource allocation in holometabolous insects. Am. Nat. 117, 692-709.
7. Boggs, C. L. 1981b Selection pressures affecting male nutrient investment at mating in heliconiine butterflies. Evolution 35, 931-940.
8. Boggs, C. L. 1986 Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecological Entomol. 11, 7-15.
9. Boggs, C. L. 1987 Ecology of nectar and pollen feeding in Lepidoptera. In Nutritional ecology of insects, mites and spiders (ed. F. Slansky & J. C. Rodriguez), pp. 369-391. New York: Wiley.
10. Boggs, C. L. 1997 Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology 78, 181-191.
11. Boggs, C. L. & Gilbert, L. E. 1979 Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206, 83-84.
12. Boggs, C. L., Smiley, J. T. & Gilbert, L. E. 1981 Patterns of pollen exploitation by Heliconius butterflies. Oecologia 48, 284-289.
13. Brice, A. T. 1992 The essentiality of nectar and arthropods in the diet of the anna's hummingbird (Calypte anna). Comp. Biochem. Physiol. 101A, 151-155.
14. Cardoso, N. Z. 2001 Patterns of pollen collection and flower visitation by Heliconius butterflies in southeastern Mexico. J. Trop. Ecol. 17, 763-768.
15. Cook, L. M., Thomason, E. W. & Young, A. M. 1976 Population structure, dynamics and dispersal of the tropical butterfly Heliconius charitonia. J. Anim. Ecol. 45, 851-863.
16. Dunlap-Pianka, H., Boggs, C. L. & Gilbert, L. E. 1977 Ovarian dynamics in heliconiine butterflies: programmed senescence versus eternal youth. Science 197, 487-490.
17. Erhardt, A. & Baker, I. 1990 Pollen amino acids - an additional diet for a nectar feeding butterfly? Pl. Syst. Evol. 169, 111-121.
18. Erhardt, A. & Rusterholz, H. P. 1998 Do peacock butterflies (Inachis io L.) detect and prefer nectar amino acids and other nitrogenous compounds? Oecologia 117, 536-542.
19. Estrada, C. & Jiggins, C. D. 2002 Patterns of pollen feeding and habitat preference among Heliconius species. Ecol. Entomol. 27, 448-456.
20. Fantle, M. S., Dittel, A. I., Schwalm, S. M., Epifanio, C. E. & Fogel, M. L. 1999 A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120, 416-426.
21. Farquhar, G. D., Ehleringer, J. R. & Hubick, K. T. 1989 Carbon isotope discrimination and photosynthesis. A. Rev. Pl. Physiol. Pl. Mol. Biol. 40, 503-537.
22. Gilbert, L. E. 1972 Pollen feeding and reproductive biology of Heliconius butterflies. Proc. Natl Acad. Sci. USA 69, 1403-1407.
23. Hagen, K. S., Dadd, R. H. & Reese, J. 1984 The food of insects. In Ecological entomology (ed. C. B. Huffaker & R. L. Rabb), pp. 79-112. New York: Wiley.
24. Hall, J. P. W. & Willmott, K. R. 2000 Patterns of feeding behaviour in adult male riodinid butterflies and their relationship to morphology and ecology. Biol. J. Linnean Soc. 69, 1-23.
25. Karlsson, B. 1994 Feeding-habits and change of body-composition with age in 3 nymphalid butterfly species. Oikos 69, 224-230.
26. Krenn, H. W. & Penz, C. M. 1998 Mouthparts of Heliconius butterflies (Lepidoptera: Nymphalidae): a search for anatomical adaptations to pollen-feeding behavior. Int. J. Insect Morphol. Embryol. 27, 301-309.
27. Linskens, H. F. & Schrauwen, J. 1969 The release of free amino acids from germinating pollen. Acta Bot. Neerl. 18, 605-614.
28. Mevi-Schutz, J. & Erhardt, A. 2002 Can Inachis io detect nectar amino acids at low concentrations? Physiol. Entomol. 27, 256-260.
29. O'Brien, D. M., Schrag, D. P. & del Rio, C. M. 2000 Allocation to reproduction in a hawkmoth: a quantitative analysis using stable carbon isotopes. Ecology 81, 2822-2831.
30. O'Brien, D. M., Fogel, M. L. & Boggs, C. L. 2002 Renewable and nonrenewable resources: amino acid turnover and allocation to reproduction in Lepidoptera. Proc. Natl Acad. Sci. USA 99, 4413-4418.
31. Pan, M. L. & Telfer, W. H. 2001 Storage hexamer utilization in two lepidopterans: difference correlated with the timing of egg formation. J. Insect Sci. 1.2, 1-9.
32. Penz, C. M. & Krenn, H. W. 2000 Behavioral adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae, Heliconiinae): an experiment using Lantana flowers. J. Insect Behav. 13, 865-880.
33. Silfer, J. A., Engel, M. H., Macko, S. A. & Jumeau, E. J. 1991 Stable carbon isotope analysis of amino-acid enantiomers by conventional isotope ratio mass-spectrometry and combined gas-chromatography isotope ratio mass-spectrometry. Analyt. Chem. 63, 370-374.
34. Smith, A. J. 1997 Postcolumn amino acid analysis. Meth. Mol. Biol.: Protein Sequencing Protocols 64, 139-146.
35. Stjernholm, F. & Karlsson, B. 2000 Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly Pieris napi. Proc. R. Soc. Lond. B 267, 807-811. (DOI 10.1098/rspb.2000.1075.)
36. Wheeler, D. E., Tuchinskaya, I., Buck, N. A. & Tabashnik, B. E. 2000 Hexameric storage proteins during metamorphosis and egg production in the diamondback moth, Plutella xylostella (Lepidoptera). J. Insect Physiol. 46, 951-958.