Broad bean cultivars increase extrafloral nectary numbers, but not extrafloral nectar, in response to leaf damage

Abstract

Phenotypic plasticity allows organisms to maximize fitness, by optimizing the expression of costly defensive traits. Broad bean, Vicia faba L. “Broad Windsor”, produces increased numbers of extrafloral nectaries (EFNs) in response to leaf damage to attract mutualistic partners and reduce herbivory. It is currently unknown, however, whether EFN induction is cultivar-specific or is a more general phenomenon. It has also not been determined whether broad beans increase nectar secretion rates in conjunction with EFN induction. We hypothesized that: a) as all broad beans have conspicuous EFNs, all cultivars should produce additional EFNs in response to leaf damage, and b) overall nectar secretion rates should increase with EFN numbers, to attract additional mutualists. We tested our hypothesis by subjecting three broad bean cultivars, Vicia faba L. “Broad Windsor”, “Stereo”, and “Witkiem” to mechanical leaf damage. The degree of change in plant traits associated with growth, in addition to EFN induction, was assessed 1 week after leaf damage. Extrafloral nectar volumes were also assessed, every 24 hours, pre- and post-leaf damage. We confirmed our first, but rejected our second, hypothesis. All cultivars produced additional EFNs, but none increased extrafloral nectar volumes, when experiencing leaf damage. Further experimentation is required to determine if energetic tradeoffs limit multiple forms of defense (i.e., EFN vs. nectar induction), or if this alternative strategy is adaptive for attracting and retaining mutualists. Understanding the costs and benefits of EFN vs. nectar induction will provide insight into the evolution of defensive mutualisms between plants and predatory arthropods.

Share and Cite:

Mondor, E. , Keiser, C. , Pendarvis, D. and Vaughn, M. (2013) Broad bean cultivars increase extrafloral nectary numbers, but not extrafloral nectar, in response to leaf damage. Open Journal of Ecology, 3, 59-65. doi: 10.4236/oje.2013.31008.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Karban, R. and Baldwin, I.T. (1997) Induced responses to herbivory. University Press of Chicago, Chicago.
[2] Tollrian, R. and Harvell, C.D. (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, NJ.
[3] Sultan, S.E. (2000) Phenotypic plasticity for plant development, function, and life-history. Trends in Plants Science, 5, 537-542. doi:10.1016/S1360-1385(00)01797-0
[4] Dewitt, T.J. and Scheiner, S.M. (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York.
[5] West-Eberhard, M.J. (1986) Alternative adaptations, speciation, and phylogeny. Proceedings of the National Academy of Sciences of the USA, 83, 1388-1392. doi:10.1073/pnas.83.5.1388
[6] West-Eberhard M.J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20, 249-278. doi:10.1146/annurev.es.20.110189.001341
[7] Moran, N.A. (1992). The evolutionary maintenance of alternative phenotypes. The American Naturalist, 139, 971-989. doi:10.1086/285369
[8] Zangerl, A.R. and Rutledge, C.E. (1996) The probability of attack and patterns of constitutive and induced defense: A test of optimal defense theory. American Naturalist, 147, 599-608. doi:10.1086/285868
[9] Karban, R., Agrawal, A.A. and Mangel, M. (1997). The benefits of induced defenses against herbivores. Ecology, 78, 1351-1355. doi:10.1890/0012-9658(1997)078[1351:TBOIDA]2.0.CO;2
[10] Stearns, S.C. (1992). The evolution of life histories. Oxford University Press, Oxford.
[11] Steiner, U.K. and Pfeiffer, T. (2007) Optimizing time and resource allocation trade-offs for investment into morphological and behavioral defense. The American Naturalist, 169, 118-129. doi:10.1086/509939
[12] Boucher, D.H., James, S. and Keeler, K.H. (1982) The ecology of mutualism. Annual Review of Ecology and Systematics, 13, 315-347. doi:10.1146/annurev.es.13.110182.001531
[13] Pierce, N.E., Kitching, R.L., Buckley, R.C., Taylor, M.F.J. and Benbow, K. (1987) Costs and benefits of cooperation between the Australian lycaenid butterfly Jalmenus evagoras and its attendant ants. Behavioral Ecology and Sociobiology, 21, 237-248. doi:10.1007/BF00292505
[14] Huxley, C.R and Cutler, D.F. (1991) Ant-plant interactions. Oxford University Press, New York.
[15] Morales, M.A. (2000) Mechanisms and density dependence of benefit in an ant-membracid mutualism. Ecology, 81, 482-489.
[16] Koptur, S. (1992) Interactions between insects and plants mediated by extrafloral nectaries. In: Bernays, E., Ed. CRC Series on Insect/Plant Interactions, Volume 4, CRC Press, Boca Raton, 85-132.
[17] Janzen, D.H. (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution, 20, 249-275. doi:10.2307/2406628
[18] Beattie, A.J. (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge. doi:10.1017/CBO9780511721878
[19] Ness, J.H. (2003) Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia, 134, 210-218.
[20] Vesprini, J.L., Galetto, L. and Bernardello, G. (2003) The beneficial effects of ants on the reproductive success of Dyckia floribunda (Bromeliaceae), an extrafloral nectary plant. Canadian Journal of Botany, 81, 24-27. doi:10.1139/b03-003
[21] Bugg, R.L. and Ellis, R.T. (1990) Insects associated with cover crops in Massachusetts. Biology, Agriculture and Horticulture, 7, 47-68.
[22] Kost, C. and Heil, M. (2005) Increased availability of extrafloral nectar reduces herbivory in Lima bean plants (Phaseolus lunatus, Fabaceae). Basic and Applied Ecology, 6, 237-248. doi:10.1016/j.baae.2004.11.002
[23] Wagner, D. and Kay, A. (2002) Do extrafloral nectaries distract ants from visiting flowers? An experimental test of an overlooked hypothesis. Evolutionary Ecology Research, 4, 293-305.
[24] Rosenweig, M.L. (2002). The distraction hypothesis depends on relatively cheap extrafloral nectaries. Evolutionary Ecology Research, 4, 307-311.
[25] Bentley, B.L. (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics, 8, 407-427. doi:10.1146/annurev.es.08.110177.002203
[26] Elias T.S. (1983). Extrafloral nectaries: their structure and distribution. In: Bentley, B.L. and Elias, T.S., Eds. The Biology of Nectaries, Columbia University Press, New York, 174-203.
[27] Heil, M., Fiala, B., Baumann, B. and Linsenmair, K.E. (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology, 14, 749-757. doi:10.1046/j.1365-2435.2000.00480.x
[28] Heil, M., Hilpert, A., Fiala, B. and Linsenmair, K.E. (2001) Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia, 126, 404-408. doi:10.1007/s004420000534
[29] Doak, P., Wagner, D. and Watson, A. (2007) Variable extrafloral nectary expression and its consequences in quaking aspen. Canadian Journal of Botany, 85, 1-9. doi:10.1139/b06-137
[30] Agrawal, A.A. and Rutter, M.T. (1998) Dynamic anti- herbivore defense in ant-plants: The role of induced responses. Oikos, 83, 227-236. doi:10.2307/3546834
[31] Heil, M. and McKey, D. (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution, and Systematics, 34, 425-453. doi:10.1146/annurev.ecolsys.34.011802.132410
[32] Mondor, E.B. and Addicott, J.F. (2003) Conspicuous extra-floral nectaries are inducible in Vicia faba. Ecology Letters, 6, 495-497. doi:10.1046/j.1461-0248.2003.00457.x
[33] Mondor, E.B., Tremblay, M.N. and Messing, R.H. (2006) Extrafloral nectary phenotypic plasticity is damage- and resource-dependent in Vicia faba. Biology Letters, 2, 583-585. doi:10.1098/rsbl.2006.0527
[34] Jaber, L.R. and Vidal, S. (2009) Interactions between an endophytic fungus, aphids and extrafloral nectaries: Do endphytes induce extrafloral-mediated defenses in Vicia faba? Functional Ecology, 23, 707-714. doi:10.1111/j.1365-2435.2009.01554.x
[35] Pulice, C.E. and Packer, A.A. (2008) Simulated herbivory induces extrafloral nectary production in Prunus avium. Functional Ecology, 22, 801-807. doi:10.1111/j.1365-2435.2008.01440.x
[36] Wackers, F.L. and Wunderlin, R. (1999) Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomologia Experimentalis et Applicata, 91, 149-154. doi:10.1046/j.1570-7458.1999.00477.x
[37] Paiva, E.A.S., Buono, R.A. and Delgado, M.N. (2007) Distribution and structural aspects of extrafloral nectaries in Cedrela fissilis (Meliaceae). Flora—Morphology, Distribution, Functional Ecology of Plants, 202, 455-461. doi:10.1016/j.flora.2006.11.001
[38] Laird, R.A. and Addicott, J.F. (2007). Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in Vicia faba. Oecologia, 152, 541-551. doi:10.1007/s00442-007-0676-4
[39] Erith, A.G. (1930) The inheritance of colour, size, and form of seeds, and of flower colour in Vicia faba L. Genetica, 12, 477-510. doi:10.1007/BF01486760
[40] Ingels, C.A. (1998) Cover cropping in vineyards: A grower’s handbook. University of California, Oakland.
[41] Koptur, S. (1989) Is extrafloral nectar production an inducible defense? In: Bock, J.H. and Linhart, Y.B., Eds., The Evolutionary Ecology of Plants, Westview, Boulder, 323-339.
[42] Katayama, N. and Suzuki, N. (2004) Role of extrafloral nectaries of Vicia faba in attraction of ants and herbivore exclusion by ants. Entomological Science, 7, 119-124. doi:10.1111/j.1479-8298.2004.00057.x
[43] SAS Institute Inc. (2008) JMP, version 8.0. Cary.
[44] Tiffin, P. and Inouye, B. (2000) Measuring tolerance to herbivory: Accuracy and precision of estimates made using natural versus imposed damage. Evolution, 54, 1024-1029.
[45] Heil, M. (2009) Damaged-self recognition in plant herbivore defence. Trends in Plant Science, 14, 356-363. doi:10.1016/j.tplants.2009.04.002
[46] Quinn, G. and Keough, M. (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge. doi:10.1017/CBO9780511806384
[47] Koptur, S. Rico-Gray, V. and Palacios-Rios, M. (1998) Ant protection of the nectaried fern Polypodium plebeium in central Mexico. American Journal of Botany, 85, 736-739. doi:10.2307/2446544
[48] O’Dowd, D.J. (1979) Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale. Oecologia, 43, 233-248. doi:10.1007/BF00344773
[49] Southwick, E.E. (1984) Photosynthate allocation to floral nectar a neglected energy investment. Ecology, 65, 1775-1779. doi:10.2307/1937773
[50] Pyke, G.H. (1991) What does it cost a plant to produce floral nectar? Nature, 350, 58-59. doi:10.1038/350058a0
[51] Radhika, V., Kost, C., Mithofer, A. and Boland, W. (2010) Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proceedings of the National Academy of Sciences of the USA, 107, 17228-17233. doi:10.1073/pnas.1009007107
[52] Zangerl, A.R. and Bazzaz, F.A. (1992) Theory and pattern in plant defense allocation. In: Fritz, R. and Simms, E.L., Eds., Plant Resistance to Herbivores and Pathogens, Uninversity of Chicago Press, Chicago, 363-392.
[53] Cohen, D. (1994) Modelling the coexistence of annual and perennial plants in temporally varying environments. Plant Species Biology, 9, 1-10. doi:10.1111/j.1442-1984.1994.tb00075.x
[54] Wackers, F.L., Zuber, D., Wunderlin, R. and Keller, F. (2001) The effect of herbivory on temporal and spatial dynamics of foliar nectar production in cotton and castor. Annals of Botany, 87, 365-370. doi:10.1006/anbo.2000.1342
[55] McNaughton, S.J. (1983) Compensatory plant growth as a response to herbivory. Oikos, 40, 329-336. doi:10.2307/3544305
[56] Trumble, J.T., Kolodny-Hirsch, D.M. and Ting, I.P. (1993) Plant compensation for arthropod herbivory. Annual Review of Entomology, 38, 93-119. doi:10.1146/annurev.en.38.010193.000521
[57] Bronstein, J.L., Alarcon, R. and Geber, M. (2006) The evolution of plant-insect mutualisms. New Phytologist, 172, 412-428. doi:10.1111/j.1469-8137.2006.01864.x
[58] Stephenson, A.G. (1982) The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology, 63, 663-669. doi:10.2307/1936786
[59] De la Fuente, M.A.S. and Marquis, R.J. (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia, 118, 192-202. doi:10.1007/s004420050718
[60] Bugg, R.L., Ellis, R.T. and Carlson, R.W. (1989) Ichneumonidae (Hymenoptera) using extrafloral nectar of faba bean (Vicia faba L., Fabaceae) in Massachusetts. Biological Agriculture and Horticulture, 6, 107-114. doi:10.1080/01448765.1989.9754509
[61] Limburg, D.D. and Rosenheim, J.A. (2001) Extrafloral nectar consumption and its influence on survival and development of an omnivorous predator, larval Chrysoperla plorabunda (Neuroptera: Chrysopidae). Environmental Entomology, 30, 595-604. doi:10.1603/0046-225X-30.3.595
[62] Rose, U.S.R., Lewis, J. and Tumlinson, J.H. (2006) Extrafloral nectar from cotton (Gossypium hirsutum) as a food source for parasitic wasps. Functional Ecology, 20, 67-74. doi:10.1111/j.1365-2435.2006.01071.x
[63] Bronstein, J.L. (1994) Conditional outcomes in mutualistic interactions. Trends in Ecology and Evolution, 9, 214- 217. doi:10.1016/0169-5347(94)90246-1
[64] Thompson, J.N. (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago.
[65] Chamberlain, S.A. and Holland, J.N. (2009) Quantitative synthesis of context-dependency in ant-plant protection mutualisms. Ecology, 90, 2384-2392. doi:10.1890/08-1490.1
[66] Rutter, M.T. and Rausher, M.D. (2004) Natural selection on extrafloral nectar production in Chamaecrista fasciulata: The costs and benefits of a mutualism trait. Evolution, 58, 2657-2668.

Copyright © 2024 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.