Share This Article:

Only Attract Ants? The Versatility of Petiolar Extrafloral Nectaries in Passiflora

Abstract Full-Text HTML XML Download Download as PDF (Size:2474KB) PP. 460-469
DOI: 10.4236/ajps.2013.42A059    4,812 Downloads   7,422 Views   Citations

ABSTRACT

Passiflora species presents a coevolutive relationship with Heliconiini butterflies, their primary herbivores. The Heliconiini caterpillars are able to detoxify toxic compounds produced by Passiflora, thus morphological defense strategies stand out over chemical innovations. In this framework, we highlight the presence of mimetic structures and extrafloral nectaries (EFN) as morphological strategies. Heliconian butterflies oviposit only on leaves that do not possess previous eggs, so the presence of egg mimics could prevent the oviposition. EFN are glands that offer nectar to territorial and aggressive ants, establishing mutualistic relationships. Here, we present a structural and chemical analysis of petiolar EFN and nectar from Passiflora alata and P. edulis in order to have insights about the implications of these features in deterring heliconian caterpillars. P. alata have one to four stipitate-crateriform EFN while P. edulis possess a pair of convex glands. Butterflies lay their eggs isolatedly or in up to three on leaves of both species. Our morphological results suggest that EFN from P. alata may act as egg mimics. Ontogenetic data suggest that the variation in the number of glands observed in this species is a serial homology, wherein the selection pressure for this variation is possibly the oviposition pattern. P. alata retain alkaloids, flavonoids and terpenoids inside nectariferous cells; sugars and flavonoids are found in the nectar of both species, while alkaloids are also detected in P. edulis. There is a selective retention/release of secondary metabolites from the EFN tissues to nectar. Knowing that these compounds can be dissuasive to some herbivores and inoffensive to others, we plotted this relationship in a consumer growth versus secondary metabolite concentration diagram. Our results suggest a more active role in the modulation of the gland defense from plants besides the establishment of a mutualistic relationship with ants, an important response in a coevolutive scenario.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

P. Cardoso-Gustavson, N. Andreazza, A. Sawaya and M. Castro, "Only Attract Ants? The Versatility of Petiolar Extrafloral Nectaries in Passiflora," American Journal of Plant Sciences, Vol. 4 No. 2A, 2013, pp. 460-469. doi: 10.4236/ajps.2013.42A059.

References

[1] W. W. Benson, K. S. Brown and L. E. Gilbert, “Coevolution of Plants and Herbivorous: Passion Flowers Butterflies,” Evolution, Vol. 29, No. 4, 1975, pp. 659-680. doi:10.2307/2407076
[2] K. S. Brown, “The Biology of Heliconius and Related Genera,” Annual Review of Entomology, Vol. 26, 1981, pp. 427-456. doi:10.1146/annurev.en.26.010181.002235
[3] K. C. Spencer, “Chemical Mediation of Coevolution in the Passiflora-Heliconius Interaction,” In: K. C. Spencer, Ed., Chemical Mediation of Coevolution, Academic Press Inc., San Diego, 1988, pp. 168-175.
[4] L. E. Gilbert and J. T. Smiley, “Determinants of Local Diversity in Phytophagous Insects,” In: L. A. Mound and N. Walloff, Eds., Diversity of Insect Faunas, Blackwell Scientific, London, 1978, pp. 89-104.
[5] W. W. Benson, “Resource Partitioning in Passion Vine Butterflies,” Evolution, Vol. 32, No. 3, 1978, pp. 493-518. doi:10.2307/2407717
[6] K. S. Williams and L. E. Gilbert, “Insects as Selective Agents on Plant Vegetative Morphology: Egg Mimicry Reduces Egg Laying by Butterflies,” Science, Vol. 212, No. 4493, 1981, pp. 467-469. doi:10.1126/science.212.4493.467
[7] J. R. Trigo, “The Chemistry of Antipredator Defense by Secondary Compounds in Neotropical Lepidoptera: Facts, Perspectives and Caveats,” Journal of the Brazilian Chemical Society, Vol. 11, No. 6, 2000, pp. 551-561. doi:10.1590/S0103-50532000000600002
[8] L. E. Gilbert, “Butterfly-Plant Coevolution: Has Passiflora adenopoda Won the Selectional Race with Heliconiine Butterflies?” Science, Vol. 172, No. 3983, 1971, pp. 585-586. doi:10.1126/science.172.3983.585
[9] J. F. Addicott, “Mutualistic Interactions in Population and Community Processes,” In: P. W. Price, C. N. Slobodchikoff and P. S. Gaud, Eds., A New Ecology: Novel Approaches to Interactive Systems, John Wiley, New York, 1984, pp. 437-451.
[10] A. Fahn, “Structure and Function of Secretory Cells,” Advances in Botanical Research, Vol. 31, 2000, pp. 37-75. doi:10.1016/S0065-2296(00)31006-0
[11] S. W. Nicolson, M. Nepi and E. Pacini, “Nectaries and Nectar,” Springer-Verlag, The Netherlands, 2007. doi:10.1007/978-1-4020-5937-7
[12] L. S. Adler and R. E. Irwin, “Ecological Costs and Benefits of Defenses in Nectar,” Ecology, Vol. 86, No. 11, 2005, pp. 2968-2978. doi:10.1890/05-0118
[13] I. G. Varassin, J. R. Trigo and M. Sazima, “The Role of Nectar Production, Flower Pigments and Odour in the Pollination of Four Species of Passiflora (Passifloraceae) in South Eastern Brazil,” Botanical Journal of the Linnean Society, Vol. 136, No. 2, 2001, pp. 139-152. doi:10.1111/j.1095-8339.2001.tb00563.x
[14] A. C. A. Aguiar-Dias, L. Yamamoto and M. M. Castro, “Stipular Extranuptial Nectaries New to Polygala: Morphology and Ontogeny,” Botanical Journal of the Linnean Society, Vol. 166, No. 1, 2011, pp. 40-50. doi:10.1111/j.1095-8339.2011.01123.x
[15] J. E. Kraus and M. Arduin, “Manual básico de métodos em morfologia vegetal,” EDUR, Seropédica, 1997.
[16] D. A. Johansen, “Plant Microtechnique,” McGraw-Hill Books, New York, 1940.
[17] R. D. Lillie, “Histopathologic Technic and Practical Histochemistry,” McGraw Hill, New York, 1965.
[18] G. Gerlach, “Botanische Mikrotechnik,” Georg Thieme Verlag, Stuttgard, 1975.
[19] J. F. A. Mc Manus, “Histological and Histochemical Uses of Periodic Acid,” Stain Technology, Vol. 23, No. 3, 1948, pp. 99-108.
[20] A. G. E. Pearse, “Histochemistry: Theoretical and Applied,” Churchill Livingstone, Edinburgh, 1985.
[21] R. David and J. P. Carde, “Coloration différentielle dês inclusions lipidique et terpeniques dês pseudophylles du pin maritime au moyen du reactif Nadi,” Comptes Rendus de I’Academie des Sciences Paris, Vol. 258, 1964, pp. 1338-1340.
[22] M. Tattini, E. Gravano, P. Pinelli, N. Milinacci and A. Romani, “Flavonoids Accumulate in Leaves and Glandular Trichomes of Phillyrea latifolia Exposed to Excess Solar Radiation,” New Phytologist, Vol. 148, No. 1, 2000, pp. 69-77. doi:10.1046/j.1469-8137.2000.00743.x
[23] L. R. Yoder and P. G. Mahlberg, “Reactions of Alkaloid and Histochemical Indicators in Laticifers and Specialized Parenchyma Cells of Catharanthus roseus (Apocynaceae),” American Journal of Botany, Vol. 63, No. 9, 1976, pp. 1167-1173. doi:10.2307/2441734
[24] K. Dhawan, S. Kumar and A. Sharma, “Passiflora: A Review Update,” Journal of Ethnopharmacology, Vol. 94, No. 1, 2004, pp. 1-23. doi:10.1016/j.jep.2004.02.023
[25] J. Crane, “Imaginal Behaviour of a Trinidad Butterfly, Heliconius erato hydara Hewitson, with Special Reference to the Social Use of Color,” Zoologica, Vol. 40, 1955, pp. 167-196.
[26] J. Crane, “Imaginal Behavior in Butterflies of the Family Heliconiidae: Changing Social Patterns and Irrelevant Actions,” Zoologica, Vol. 42, 1957, pp. 135-145.
[27] C. A. Swihart, “Colour Discrimination by the Butterfly, Heliconius charitonius Linn,” Animal Behavior, Vol. 19, No. 1, 1971, pp. 156-164. doi:10.1016/S0003-3472(71)80151-3
[28] G. Struwe, “Spectral Sensitivity of Single Photoreceptors in the Compound Eye of a Tropical Butterfly (Heliconius numata),” Journal of Comparative Physiology, Vol. 79, No. 2, 1972, pp. 196-201.
[29] A. Kelber, A. Balkenius and E. J. Warrant, “Colour Vision in Diurnal and Nocturnal Hawkmoths,” Integrative and Comparative Biology, Vol. 43, No. 4, 2003, pp. 571579. doi:10.1093/icb/43.4.571
[30] K. C. Spencer, “Chemical Mediation of Coevolution in the Passiflora-Heliconius Interaction,” In: K. C. Spencer, Ed., Chemical Mediation of Coevolution, San Diego, Academic Press Inc., 1988, pp.168-175.
[31] R. Dell’Erba, L. A. Kaminski and G. R. P. Moreira, “O estágio de ovo dos Heliconiini (Lepidoptera: Nymphalidae) do Rio Grande do Sul, Brasil,” Iheringia Série Zoologia, Vol. 95, No. 1, 2005, pp. 29-46. doi:10.1590/S0073-47212005000100006
[32] S. Koptur, “Extrafloral Nectary-Mediated Interactions between Insects and Plants,” In: E. Bernays, Ed., Insect Plant Interactions, CRC Press, Boca Raton, 1992, pp. 81129.
[33] P. Karageorgou, C. Buschmann and Y. Manetas, “Red Leaf Color as a Warning Signal against Insect Herbivory: Hones or Mimetic?” Flora, Vol. 203, No. 8, 2008, pp. 648-652. doi:10.1016/j.flora.2007.10.006
[34] B. L. Bentley, “Plants Bearing Extrafloral Nectaries and the Associated Ant Community Interhabitat Differences in the Reduction of Herbivory Damage,” Ecology, Vol. 57, No. 4, 1976, pp. 815-820. doi:10.2307/1936195
[35] J. Lanza, “Ant Preferences for Passiflora Nectar Mimics That Contain Amino Acids,” Biotropica, Vol. 20, No. 4, 1988, pp. 341-344. doi:10.2307/2388328
[36] M. Heil, J. Pattke and W. Boland, “Postsecretory Hydrolysis of Nectar Sucrose and Specialization in Ant/Plant Mutualism,” Science, Vol. 308, No. 5721, 2005, pp. 560563. doi:10.1126/science.1107536
[37] D. A. Baker, J. L. Hall and J. R. Thorpe, “A study of the Extrafloral Nectaries of Ricinus communis,” New Phytologist, Vol. 81, No. 1, 1978, pp. 129-137. doi:10.1111/j.1469-8137.1978.tb01612.x
[38] D. J. O’Dowd, “Foliar Nectar Production and Ant Activity on a Neotropical Tree, Ochroma pyramidale,” Oecologia, Vol. 43, No. 2, 1979, pp. 233-248. doi:10.1007/BF00344773
[39] T. S. Elias, “Extrafloral Nectaries: Their Structure and Distribution,” In: B. Bentley and T. Elias, Eds., The Biology of Nectaries, Columbia University Press, New York, 1983, pp. 174-182.
[40] R. F. Denno and M. A. Donnelly, “Patterns of Herbivory on Passiflora Leaf Tissues and Species by Generalized and Specialized Feeding Insects,” Ecological Entomology, Vol. 6, No. 1, 1981, pp. 11-16. doi:10.1111/j.1365-2311.1981.tb00967.x
[41] D. I. Rocha, L. C. Silva, V. M. M. Valente, D. M. T. Francino and R. M. S. A. Meira, “Morphoanatomy and Development of Leaf Secretory Structures in Passiflora amethystine Mikan (Passifloraceae),” Australian Journal of Botany, Vol. 57, No. 7, 2009, pp. 619-626. doi:10.1071/BT09158
[42] L. T. Durkee, “The Floral and Extra-Floral Nectaries of Passiflora. II. The Extra-Floral Nectary,” American Journal of Botany, Vol. 69, No. 9, 1982, pp. 1420-1428. doi:10.2307/2443103
[43] APG III, “An Update of the Angiosperm Phylogeny Group Classification for the Orders and Families of flowering plants: APG III,” Botanical Journal of the Linnean Society, Vol. 161, No. 2, 2009, pp. 105-121. doi:10.1111/j.1095-8339.2009.00996.x
[44] M. T. A. Garcia, B. G. Galati and O. S. Hoc, “Ultrastructure of the Corona of Scented and Scentless Flowers of Passiflora spp. (Passifloraceae),” Flora, Vol. 202, No. 4, 2007, pp. 302-315. doi:10.1016/j.flora.2006.08.003
[45] D. Tholl, C. M. Kish, I. Orlova, et al., “Formation of Monoterpenes in Antirrhinum majus and Clarkia breweri Flowers Involves Heterodimeric Geranyl Diphosphate Synthases,” The Plant Cell, Vol. 16, No. 4, 2004, pp. 977992. doi:10.1105/tpc.020156
[46] L. S. Adler, “The Ecological Significance of Toxic Nectar,” Oikos, Vol. 91, No. 3, 2001, pp. 409-420. doi:10.1034/j.1600-0706.2000.910301.x
[47] L. L. Smith, J. Lanza and G. C. Smith, “Amino Acid Concentrations in Extrafloral Nectar of Impatiens sultani Increase after Simulated Herbivory,” Ecology, Vol. 71, No. 1, 1990, pp. 107-115. doi:10.2307/1940251
[48] R. A. Dixon and N. L. Paiva, “Stress Induced Phenylpropanoid Metabolism,” The Plant Cell, Vol. 7, No. 7, 1995, pp. 1085-1097.
[49] T. M. Kutchan, “A Role for Intraand Intercellular Translocation in Natural Product Biosynthesis,” Current Opinion in Plant Biology, Vol. 8, No. 3, 2005, pp. 292-300. doi:10.1016/j.pbi.2005.03.009
[50] M. Otani, N. Shitan, K. Sakai, E. Martinoia, F. Sato and K. Yazaki, “Characterization of Vacuolar Transport of the Endogenous Alkaloid Berberine in Coptis japonica,” Plant Physiology, Vol. 138, 2005, pp. 1939-1946. doi:10.1104/pp.105.064352
[51] D. Treutter, “Significance of Flavonoids in Plant Resistance: A Review,” Environmental Chemistry Letters, Vol. 4, No. 4, 2006, pp. 147-157. doi:10.1007/s10311-006-0068-8

  
comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.