Journal of Chemical Ecology

, Volume 28, Issue 7, pp 1393–1410

Seed Chemistry of Sophora chrysophylla (Mamane) in Relation to Diet of Specialist Avian Seed Predator Loxioides bailleui (Palila) in Hawaii

  • P. C. Banko
  • M. L. Cipollini
  • G. W. Breton
  • E. Paulk
  • M. Wink
  • I. Izhaki
Article

Abstract

This study describes the chemical ecology of a tritrophic interaction among species endemic to the island of Hawaii, USA: a tree (Sophora chrysophylla: mamane), an endangered bird (Loxioides bailleui; palila), and moth larvae (Cydia spp.). Palila and Cydia both specialize on the seed embryos of mamane but avoid eating the seed coats. Palila actively seek out and feed mamane embryos and Cydia larvae to their nestlings. Because mamane embryos contain potentially toxic levels of alkaloids, including broadly toxic quinolizidine alkaloids, and because insects often sequester alkaloids from their food plants, we focus on the questions of why palila forage upon mamane embryos and why they supplement their diet with Cydia larvae. Our data show that mamane embryos contain high amounts of potentially toxic alkaloids, but are well balanced nutritionally and contain lipids, carbohydrates, proteins, amino acids, and minerals at levels that are likely to be sufficient for maintenance and breeding. Mamane seed coats contain lower levels of alkaloids and nutrients, somewhat higher levels of phenolics, and much higher levels of nondigestible fiber. Taken together, these results suggest that palila have evolved tolerance to high levels of alkaloids and that they forage upon embryos primarily because of their availability in the habitat and high nutritional reward. Our data also suggest that Cydia are used by palila because they are readily accessible, nontoxic, and nutritious; the larvae apparently do not sequester alkaloids while feeding upon mamane seeds. Our results are interpreted with respect to the likelihood of current and historical coadaptive responses in this ecologically isolated and simplified island setting.

Coadaptation Cydia Hawaii Loxioides bailleui mamane nutrition palila quinolizidine alkaloids seed predation secondary metabolites Sophora chrysophylla toxins 

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REFERENCES

  1. Banko, P. C., Johnson, L., Lindsey, G. D., Fancy, S. G., Pratt, T. K., Jacobi, J. D., and Banko, W. E.2002a. Palila (Loxioides bailleui), inA. Poole and F. Gill (eds.). The Birds of North America. The Birds of North America, Inc. Philadelphia, Pennsylvania. In press.Google Scholar
  2. Banko, P. C., Oboyski, P. T., Slotterback, J. W., Dougill, S. J., Goltz, D. M., Johnson, L., Laut, M. E., and Murray, T. C.2002b. Availability of food resources, distribution, of invasive species, and conservation of a Hawaiian bird along a gradient of elevation. J. Biogeogr. In press.Google Scholar
  3. Barlow, R. B., and McLeod, L. J.1969. Some studies on cytisine and its methylated derivatives. Br. J. Pharmacol. 35:161–174.Google Scholar
  4. Bentley, M. D., Leonard, D. E., Reynolds, E. K., Leach, S., Beck, A. B., and Murakoshi, I.1984. Lupine alkaloids as larval feeding deterrents for spruce budworm, Choristoneura fumiferana(Lepidoptera: Tortricidae). Ann. Entomol. Soc. Am.77:398–400.Google Scholar
  5. Budini, R., Tonelli, D., and Girotti, S.1980. Analysis of total phenols using the Prussian blue method. J. Agric. Food Chem.28:1236–1238.Google Scholar
  6. Cantot, P. and Papineau, J.1983. Discrimination des lupins basse teneur en alcaloides par les adultes de Sitonia lineatusL. (Coleoptera: Curculionidae). Agronomie3:937–940.Google Scholar
  7. Dreyer, D., Jones, K. C., and Molyneux, R. J.1985. Feeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrthosiphon pisum) and evidence for phloem transport of the indolizidine alkaloid swainsonine. J. Chem. Ecol.11:1045–1051.Google Scholar
  8. Graham, H. D.1992. Stabilization of the Prussian Blue color in the determination of polyphenols. J. Agric. Food Chem.40:801–805.Google Scholar
  9. Gray, E. M., Banko, P. C., Dougill, S. J., Goltz, D., Johnson, L., Laut, M. E., Semones, J. D., and Wiley, M. R.1999. Breeding and nonbreeding censuses of the 1998 palila population on Mauna Kea, Hawaii. Elepaio59:33–39.Google Scholar
  10. Hatfield, G. M., Valdes, L. J. J., Keller, W. J., Merrill, W. L., and Jones, V. H.1977. An investigation of Sophora secundifloraseeds (mescalbeans). Lloydia40:374–383.Google Scholar
  11. Hess, S. C., Banko, P. C., Brenner, G. J., and Jacobi, J. D.1999. Factors related to the recovery of subalpine woodland on Mauna Kea, Hawaii. Biotropica31:212–219.Google Scholar
  12. Hess, S. C., Banko, P. C., Reynolds, M.H., Brenner, G. J., Laniawe, L. P., and Jacobi, J. D.2001. Drepanidine movements in relation to food availability in subalpine woodlands on Mauna Kea, Hawaii. Stud. Avian Biol.22:154–163.Google Scholar
  13. Izaddoost, M., Harris, B. G., and Gracy, R.W.1976. Structure and toxicity of alkaloids and amino acids of Sophora secundiflora. J. Pharm. Sci.65:352–354.Google Scholar
  14. Jacobi, J. D., Fancy, S. G., Giffin, J. G., and Scott, J. M.1996. Long-term population variability in the palila, an endangered Hawaiian honeycreeper. Pac. Sci.50:363–370.Google Scholar
  15. Jeffrey, J. J., Fancy, S. G., Lindsey, G. D., Banko, P. C., Pratt, T. K., and Jacobi, J. D.1993. Sex and age identification of palila. J. Field Ornithol.64:490–499.Google Scholar
  16. Johnson, N. D. and Bentley, B. B.1988. Effects of dietary protein and lupine alkaloids on growth and survivorship of Spodoptera eridania. J. Chem. Ecol.14:1391–1403.Google Scholar
  17. Jones, C. G., Hare, J. D., and Compton, S. J.1989. Measuring plant protein with the Bradford assay.I. Evaluation and standard method. J. Chem. Ecol.15:979–992.Google Scholar
  18. Juvik, J. O., Nullet, D., Banko, P., and Hughes, K.1993. Forest climatology near the tree line in Hawaii. Agric. For. Meteorol.66:159–172.Google Scholar
  19. Kadooka, M. M., Chang, M. Y., Fukami, H., Scheuer, P. J., Clardy, J., Solheim, B. A., and Springer, J. P.1976. Mamanine and pohakuline, two unprecedented quinolizidine alkaloids from Sophora chrysophylla. Tetrahedron32:919–924.Google Scholar
  20. Keller, W. J.1975. Alkaloids from Sophora secundiflora. Phytochemistry14:2305–2306.Google Scholar
  21. Keller, W. J., Hatfield, G. M., and Valdes, L. J.1976. Isolation of lupinine and Δ-5-dehydrolupanine from Sophora secundiflora. Lloydia39:472.Google Scholar
  22. Kinghorn, A. D. and Balandrin, M. F.1984. Quinolizidine alkaloids of the Leguminosae: Structural types, analysis, chemotaxonomy, and biological activities, pp. 105–148, inS. W. Pelletier (ed.). Alkaloids: Chemical and Biological Perspectives, Vol. 2. Wiley, New York.Google Scholar
  23. Knauer, K. W., Reagor, J. C., Bailey, E. M. Jr., and Carriker, L.1995. Mescalbean (Sophora secundiflora) toxicity in a dog. Vet. Hum. Toxicol.37:237–238.Google Scholar
  24. Levey, D. J. and Cipollini, M. L.1999. Effects of plant secondary metabolites on diet choice and digestion. Ostrich69:2208–2220.Google Scholar
  25. Matsuda, K., Kimura, M., Komai, K., and Hamada, M.1989. Nematicidal activities of (°)-N-methylcytisine and (°)-anagyrine from Sophora flavescensagainst Pine wood nematodes. J. Agric. Biol. Chem.53:2287–2288.Google Scholar
  26. Montllor, C. B., Bernays, E. A., and Barbehenn, R.V.1990. Importance of quinolizidine alkaloids in the relationship between larvae of Uresphita reversalis(Leptidoptera: Pyralidae) and a host plant, Genista monspessulana. J. Chem. Ecol.16:1853–1865.Google Scholar
  27. Moore, S. and Stein W. H.1951. Chromatography of amino acids on sulfonated polystyrene resins. J. Biol. Chem.192:663–681.Google Scholar
  28. Murakoshi, I., Ito, M., Haginiwa, J., Ohmiya, S., Otomasu, H., and Hirano, R. T.1984. Lupin alkaloids from Sophora chrysophylla. Phytochemistry23:887–891.Google Scholar
  29. Murphy, M. E.1993. The essential amino acid requirements for maintenance in the White-crowned Sparrow, Zonotrichia leucophrys gambelii. Can. J. Zool.71:2121–2130.Google Scholar
  30. Pena, R. C. and Cassels, B. K.1996. Phylogenetic relationships among Chilean Sophoraspecies. Biochem. Syst. Ecol.24:725–733.Google Scholar
  31. Perkins, R. C. L.1903. Vertebrata, pp. 365–466, inD. Sharpe (ed.). Fauna Hawaiiensis, Vol. I, Part IV. The University Press, Cambridge.Google Scholar
  32. Perkins, R. C. L.1913. Introductory essay on the fauna. pp. i–ccxxviii inD. Sharpe (ed.). Fauna Hawaiiensis, Vol. 1, Part VI. The University Press, Cambridge.Google Scholar
  33. Pratt, T.K, Banko, P. C., Fancy, S. G., Lindsey, G. D., and Jacobi, J.D.1997. Status and distribution of the palila, an endangered Hawaiian honeycreeper, 1987–1996.0Pac. Conserv. Biol. 3:330–340.Google Scholar
  34. Robbins, C. T.1993.Wildlife Feeding and Nutrition, 2nd ed. Academic Press, San Diego, California.Google Scholar
  35. Scott, J. M., Mountainspring, S., Ramsey, F. L., and Kepler, C. B.1986. Forest bird communities of the Hawaiian Islands: Their dynamics, ecology, and conservation. Stud. Avian Biol.9:1–431.Google Scholar
  36. Smith, D.1981. Removing and analyzing total nonstructural carbohydrates from plant tissue. Wisconsin Agricultural Experimental Station Bulletin 2107, Madison, Wisconsin.Google Scholar
  37. Sokal, R. R., and Rohlf, F. J.1981. Biometry. Freeman, San Francisco, California.Google Scholar
  38. Spiro, R. G.1966. Analysis of sugars found in glycoproteins, pp. 3–26, inE. F. Newfield and V. Ginsberg (eds.). Methods in Ezymology, Volume VIII, Complex Carbohydrates. Academic Press, New York.Google Scholar
  39. Tyski, S., Markiewicz, M., Gulewicz, K., and Twardowski, T.1988. The effect of lupin alkaloids and ethanol extracts from seeds of Lupinus angustifoliuson selected bacterial strains. J. Plant Physiol.133:240–242.Google Scholar
  40. Van Riper, C., III. 1980a. Observations on the breeding of the palila Psittirostra bailleuiof Hawaii. Ibis122:462–475.Google Scholar
  41. VAN Riper, C., III. 1980b. The phenology of the dryland forest of Mauna Kea, Hawaii, and the impact of recent environmental perturbations. Biotropica12:282–291.Google Scholar
  42. Van Riper, C., III. Scott, J. M., and Woodside, D. M.1978. Distribution and abundance patterns of the palila on Mauna Kea, Hawaii. Auk95:518–527.Google Scholar
  43. Weglarczyk, G.1981. Nitrogen balance and energy efficiencies of protein deposition of the house sparrow, Passer domesticus(L.). Ekol. Pol.29:519–533.Google Scholar
  44. Williams, S.(ed.) 1984. Official Methods of Analysis of the Association of Analytical Chemists. 14th ed. Association of Official Analytical Chemists, Arlington, Virginia.Google Scholar
  45. Wink, M.1984a. Chemical defence of Leguminosae. Are quinolizidine alkaloids part of the antimicrobial defence system of lupins? Z. Naturforsch.39c:548–552.Google Scholar
  46. Wink, M.1984b. Chemical defense of lupins. Mollusc-repellent properties of quinolizidine alkaloids. Z. Naturforsch.39c:553–558.Google Scholar
  47. Wink, M.1987a. Chemical ecology of quinolizidine alkaloids. ACS Symp. Ser.330:524–533.Google Scholar
  48. Wink, M.1987b. Site of lupanine and sparteine biosynthesis in intact plants and in vitro organ cultures. Z. Naturforsch.42c:868–872.Google Scholar
  49. Wink, M.1992. The role of quinolizidine alkaloids in plant insect interactions, pp. 133–169, inE. A. Bernays (ed.). Insect–Plant Interactions, Vol. IV. CRC Press, Boca Raton, Florida.Google Scholar
  50. Wink, M.1993. Quinolizidine alkaloids, pp. 197–239, inP. Waterman (ed.). Methods in Plant Biochemistry, Vol. 8. Academic Press, London.Google Scholar
  51. Wink, M.1998a. Chemical ecology of alkaloids, pp. 265–300, inM. F. Roberts and M. Wink (eds.). Alkaloids: Biochemistry, Ecology and Medicinal Applications. Plenum Press, New York.Google Scholar
  52. Wink, M.1998b. Modes of action of alkaloids, pp. 301–326, inM. F. Roberts and M. Wink (eds.). Alkaloids: Biochemistry, Ecology and Medicinal Applications. Plenum Press, New York.Google Scholar
  53. Wink, M.1999. Function of Plant Secondary Metabolites and their Exploitation in Biotechnology, Annual Plant Reviews, Vol. 3. Sheffield Academic Press, Sheffield, UK, and CRC Press, Boca Raton, Florida, 362 pp.Google Scholar
  54. Wink, M.2000. Interference of alkaloids with neuroreceptors and ion channels, pp. 3–129, inAtta-Ur-Rahman (ed.). Bioactive Natural Products. Elsevier, Amsterdam.Google Scholar
  55. Wink, M. and Twardowski, T.1992. Allelochemical properties of alkaloids: Effects on plants, bacteria and protein biosynthesis, pp. 129–150, inS. J. H. Rizvi and V. Rizvi (eds.). Allelopathy: Basic and Applied Aspects. Chapman & Hall, London.Google Scholar
  56. Wink, M. and Witte, L.1991. Storage of quinolizidine alkaloids in Macrosiphum albifronsand Aphis genistae(Homoptera: Aphididae). Entomol. Gen.15:237–254.Google Scholar
  57. Wink, M., Hartmann, T., Witte, L., and Rheinheimer, J.1982. Interrelationship between quinolizidine alkaloid producing legumes and infesting insects: Exploitation of the alkaloid-containing phloem sap of Cytisus scopariusby the broom aphid, Aphis cytisorum. Z. Naturforsch.37c:1081–1086.Google Scholar
  58. Wink, M., Heinen, H. J., Vogt, H., and Schiebel, H. M.1984. Cellular localization of quinolizidine alkaloids by laser desorption mass spectrometry (LAMMA 1000). Plant Cell Rep.3:230–233.Google Scholar
  59. Wink, M., Schmeller, T., and Latz-brÜning, B.1998. Modes of action of allelochemical alkaloids: Interaction with neuroreceptors, DNA and other molecular targets. J. Chem. Ecol.24:1881–1937.Google Scholar
  60. Wippich, C. and Wink, M.1985. Biological properties of alkaloids: Influence of quinolizidine alkaloids and gramine on the germination and development of powdery mildew, Erysiphe graminisf.sp. hordei. Experientia41:1477–1478.Google Scholar
  61. Zhao, B., Grant, G. G., Langenin, D., and MacDonald, L.1998. Deterring and inhibiting effects of quinolizidine alkaloids on Spruce Budworm (Lepidoptera: Torticidae) oviposition. Environ. Entomol.27:984–992.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • P. C. Banko
    • 1
  • M. L. Cipollini
    • 2
  • G. W. Breton
    • 3
  • E. Paulk
    • 2
  • M. Wink
    • 4
  • I. Izhaki
    • 5
  1. 1.Pacific Island Ecosystems Research Center, Kilauea Field StationU.S. Geological SurveyHawaii National Park
  2. 2.Department of BiologyBerry CollegeMount Berry
  3. 3.Department of ChemistryBerry CollegeMount Berry
  4. 4.Institut für Pharmazeutische BiologieUniversitat HeidelbergHeidelbergGermany
  5. 5.Department of BiologyUniversity of Haifa at OranimTivonIsrael

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