Differential effects of type and quantity of leaf damage on growth, reproduction and defence of lima bean (Phaseolus lunatus L.)

Plant Biology

Volumn 17, Issue 3, 2015, Pages 712-719

  Blue, E ^a   Kay, J ^a   Younginger, B S ^a   Ballhorn, D J ^a  

^a PORTLAND STATE UNIVERSITY   (United States)

Author keywords

Crop plants; Cyanogenesis; Defoliation; Extrafloral nectar; Herbivory; Insect pests; Plant fitness

Indexed keywords

ANTAGONISM; DAMAGE; DEFOLIATION; FITNESS; GROWTH RATE; HERBIVORY; LEAF AREA; LEGUME; NECTAR; PHYTOMASS; PLANT DEFENSE; QUANTITATIVE ANALYSIS; REPRODUCTIVE PRODUCTIVITY;

HEXAPODA; PHASEOLUS LUNATUS;

HYDROGEN CYANIDE; NECTAR;

BIOMASS; COMPARATIVE STUDY; DISEASE RESISTANCE; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; METABOLISM; NECTAR; PHASEOLUS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT SEED; REPRODUCTION;

BIOMASS; DISEASE RESISTANCE; ECOSYSTEM; HERBIVORY; HYDROGEN CYANIDE; PHASEOLUS; PLANT DISEASES; PLANT LEAVES; PLANT NECTAR; REPRODUCTION; SEEDS;

EID: 84927671317     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12285     Document Type: Article

References (85)

1. Arimura G., Ozawa R., Shimoda T., Nishioka T., Boland W., Takabayashi J. (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature, 406, 512-515.
2. Bale J.S., Masters G.J., Hodkinson I.D., Awmack C., Bezemer T.M., Brown V.K., Butterfield J., Buse A., Coulson J.C., Farrar J., Good J.E.G., Harrington R., Hartley S., Jones T.H., Lindroth R.L., Press M.C., Symrnioudis I., Watt A.D., Whittaker J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8, 1-16.
3. Ballhorn D.J. (2011) Constraints of simultaneous resistance to a fungal pathogen and an insect herbivore in lima bean (Phaseolus lunatus L.). Journal of Chemical Ecology, 37, 141-144.
4. Ballhorn D.J., Lieberei R., Ganzhorn J.U. (2005) Plant cyanogenesis of Phaseolus lunatus and its relevance for herbivore-plant interaction: the importance of quantitative data. Journal of Chemical Ecology, 31, 1445-1473.
5. Ballhorn D.J., Heil M., Liebereri R. (2006) Phenotypic plasticity of cyanogenesis in lima bean Phaseolus lunatus - activity and activation of beta-glucosidase. Journal of Chemical Ecology, 32, 261-275.
6. Ballhorn D.J., Pietrowski A., Heil M., Lieberei R. (2007) Quantitative effects of cyanogenesis on an adapted herbivore. Journal of Chemical Ecology, 33, 2195-2208.
7. Ballhorn D.J., Kautz S., Lion U., Heil M. (2008a) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). Journal of Ecology, 96, 971-980.
8. Ballhorn D.J., Schiwy S., Jensen M., Heil M. (2008b) Quantitative variability of direct chemical defense in primary and secondary leaves of lima bean (Phaseolus lunatus) and consequences for a natural herbivore. Journal of Chemical Ecology, 34, 1298-1301.
9. Ballhorn D.J., Kautz S., Heil M., Hegeman A.D. (2009) Cyanogenesis of Wild Lima Bean (Phaseolus lunatus L.) Is an Efficient Direct Defence in Nature. PLoS ONE, 4, e5450.
10. Ballhorn D.J., Kautz S., Lieberei R. (2010a) Comparing responses of generalist and specialist herbivores to various cyanogenic plant features. Entomologia Experimentalis et Applicata, 134, 245-259.
11. Ballhorn D.J., Pietrowski A., Lieberei R. (2010b) Direct trade-off between cyanogenesis and resistance to a fungal pathogen in lima bean (Phaseolus lunatus L.). Journal of Ecology, 98, 226-236.
12. 2 mediated changes of plant traits and their effects on herbivores are determined by leaf age. Ecological Entomology, 36, 1-13.
13. Ballhorn D.J., Kautz S., Jensen M., Schmitt I., Heil M., Hegeman A.D. (2011a) Genetic and environmental interactions determine plant defenses against herbivores. Journal of Ecology, 99, 313-326.
14. 2 on jasmonic acid induced plant volatiles of lima bean (Phaseolus lunatus L.). Journal of Applied Botany and Food Quality, 71, 65-71.
15. Ballhorn D.J., Godschalx A.L., Kautz S. (2013a) Co-variation of chemical and mechanical defences in lima bean (Phaseolus lunatus L.). Journal of Chemical Ecology, 39, 413-417.
16. Ballhorn D.J., Kautz S., Heil M. (2013b) Distance and sex determine host plant choice by herbivorous beetles. PLoS ONE, 8, e55602.
17. Ballhorn D.J., Kay J., Kautz S. (2014) Quantitative effects of leaf area removal on indirect defense of lima bean (Phaseolus lunatus) in nature. Journal of Chemical Ecology, 40, 294-296.
18. Bardgett R.D., Wardle D.A., Yeates G.W. (1998) Linking aboveground and belowground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biology and Biochemistry, 30, 1867-1878.
19. Blue J.D., Souza L., Classen A.T., Schweitzer J.A., Sanders N.J. (2011) The variable effects of soil nitrogen availability and insect herbivory on aboveground and belowground plant biomass in an old-field ecosystem. Oecologia, 167, 771-780.
20. Boege K., Dirzo R., Siemens D., Brown P. (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecology Letters, 10, 177-187.
21. Brown D.G. (1994) Beetle folivory increases resource availability and alters plant invasion in monocultures of goldenrod. Ecology, 75, 1673-1683.
22. Coley P.D., Barone J.A. (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecological Systems, 27, 305-335.
23. Coomes D., Grubb P.J. (2003) Colonization, tolerance, competition and seed-size variation within functional groups. Trends in Ecology & Evolution, 18, 283-291.
24. Cyr H., Pace M.L. (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature, 361, 148-150.
25. Eyles A., Smith D., Pinkard E.A., Smith I., Corkrey R., Elms S., Beadle C.L., Mohammed C.L. (2011) Photosynthetic responses of field-grown Pinus radiata trees to artificial and aphid induced defoliation. Tree Physiology, 31, 592-603.
26. Fenner M., Thompson K. (2005) The ecology of seeds. Cambridge University Press, Cambridge, UK, pp 48-57.
27. Gleadow R.M., Møller B.L. (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annual Review of Plant Biology, 65, 155-185.
28. Gold W.G., Caldwell M.M. (1989) The effects of the spatial pattern of defoliation on regrowth of a tussock grass. Oecologia, 80, 289-296.
29. Gruner D.S., Smith J.E., Seabloom E.W., Sandin S.A., Ngai J.T., Hillebrand H., Harpole W.S., Elser J.J., Cleland E.E., Bracken M.E., Borer E.T., Bolker B.M. (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecology Letters, 11, 740-755.
30. Gulmon S.L. (1992) Patterns of seed germination in Californian serpentine grassland species. Oecologia, 89, 27-31.
31. Harper J.L. (1977) Population biology of plants. Academic Press, London, UK, pp 56-61.
32. Harper J.L., Lovell P.H., Moore K.G. (1970) The shapes and sizes of seeds. Annual Review of Ecology and Systematics, 1, 327-356.
33. Heil M., Kost C. (2006) Priming of indirect defences. Ecology Letters, 9, 813-817.
34. Jurado E., Westoby M. (1992) Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology, 80, 407-416.
35. Kadow D., Voss K., Selmar D., Lieberei R. (2012) The cyanogenic syndrome in rubber tree Hevea brasiliensis: tissue-damage-dependent activation of linamarase and hydroxynitrile lyase accelerates hydrogen cyanide release. Annals of Botany, 109, 1253-1262.
36. Kariyat R.R., Balogh C.M., Moraski R.P., De Moraes C.M., Mescher M.C., Stephenson A.G. (2013) Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae). American Journal of Botany, 100, 1014-1021.
37. Kaschuk G., Kuyper T.W., Leffelaar P.A., Hungria M., Giller K.E. (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry, 41, 1233-1244.
38. Koptur S., Smith C.L., Lawton J.H. (1996) Effects of artificial defoliation on reproductive allocation in the common vetch, Vicia sativa (Fabaceae: Papilionoideae). American Journal of Botany, 83, 886-889.
39. Koricheva J., Nykänen H., Gianoli E. (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks of all trades, masters of all? The American Naturalist, 163, 64-75.
40. Lee W.G., Fenner M. (1989) Mineral nutrient allocation in seeds and shoots of twelve Chionochloa species in relation to soil fertility. Journal of Ecology, 77, 704-716.
41. Leishman M., Westoby M. (1994) The role of large seed size in shaded conditions: experimental evidence. Functional Ecology, 8, 205-214.
42. Leishman M.R., Wright I.J., Moles A.T., Westoby M. (2000) The evolutionary ecology of seed size. In: Fenner M. (Ed.), Seeds: the ecology of regeneration in plant communities, 2nd edition. CAB International, Wallingford, UK, pp 31-58.
43. Li T., Holopainen J.K., Kokko H., Tervahauta A.I., Blande J.D. (2012) Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants. Functional Ecology, 26, 1176-1185.
44. Lieberei R. (1988) Relationship of cyanogenic capacity (HCN-c) of the rubber tree Hevea brasiliensis to susceptibility to Microcydus ulei, the agent causing South American leaf blight. Journal of Phytopathology, 122, 54-67.
45. Lucas-Barbosa D., van Loon J.J., Dicke M. (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry, 72, 1647-1654.
46. Marquis R.J. (1984) Leaf herbivores decrease fitness of a tropical plant. Science, 226, 537-539.
47. Marshall D.L., Abrahamson N.J., Avritt J.J., Hall P.M., Medeiros J.S., Reynolds J., Shaner M.G.M., Simpson H.L., Trafton A.N., Tyler A.P., Walsh S. (2005) Differences in plastic responses to defoliation due to variation in the timing of treatments for two species of Sesbania (Fabaceae). Annals of Botany, 95, 1049-1058.
48. Martínez-Castillo J., Zizumbo-Villarreal D., Perales-Rivera H., Colunga-Garcíamarin P. (2004) Intraspecific diversity and morpho-phenological variation in Phaseolus lunatus L. from the Yucatan Peninsula, Mexico. Economic Botany, 58, 354-380.
49. Mauricio R., Bowers M.D., Bazzaz F.A. (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology, 74, 2066-2207.
50. McArt S.H., Halitschke R., Salminen J., Thaler J.S. (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology, 94, 966-975.
51. McKey D. (1974) Adaptive patterns in alkaloid physiology. The American Naturalist, 108, 305-320.
52. McKey D. (1979) The distribution of plant secondary compounds within plants. In: Rosenthal G. A., Janzen D. H. (Eds), Herbivores: their interactions with secondary plant metabolites. Academic Press, NY, USA, pp 55-133.
53. McNaughton S.J. (1979) Grazing as an optimization process: grass-ungulate relationships in the Serengeti. The American Naturalist, 113, 691-703.
54. van der Meijden E., Wijn M., Verkaar H.J. (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos, 51, 355-363.
55. Moles A.T., Westoby M. (2004) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology, 92, 372-383.
56. Mothershead K., Marquis R.J. (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology, 81, 30-40.
57. Mumm R., Posthumus M.A., Dicke M. (2008) Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant, Cell & Environment, 31, 575-585.
58. Nepi M., Stpiczyńska M. (2008) The complexity of nectar: secretion and resorption dynamically regulate nectar features. Naturwissenschaften, 95, 177-184.
59. Nishida T., Izumi N., Katayama N., Ohgushi T. (2009) Short-term response of abuscular mycorrhizal association to spider mite herbivory. Population Ecology, 51, 329-334.
60. Nolting S.P., Edwards C.R. (1989) Yield responses of soybeans to defoliation by the Mexican bean beetle (Coleoptera: Coccinellidae). Journal of Economic Entomology, 82, 1212-1218.
61. Núñez-Farfán J., Fornoni J., Valverde P.L. (2007) The evolution of resistance and tolerance to herbivores. Annual Review of Ecology, Evolution and Systematics, 38, 541-566.
62. Ostlie K.R., Pedigo L.P. (1984) Water loss from soybeans after simulated and actual insect defoliation. Environmental Entomology, 13, 1675-1680.
63. Parrish J., Bazzaz F.A. (1985) Nutrient content of Abutilon theophrasti and the competitive ability of the resulting plants. Oecologia, 65, 247-251.
64. Peterson C.J., Facelli J.M. (1992) Contrasting germination and seedling growth of Betula alleghaniensis and Rhus typhina subjected to various amounts and types of plant litter. American Journal of Botany, 79, 1209-1216.
65. Pinkard E.A., Eyles A., O'Grady A.P. (2011) Are gas exchange responses to resource limitation and defoliation linked to source:sink relationships? Plant, Cell & Environment, 34, 1652-1665.
66. Pucheta E., Bonamici I., Cabido M., Diaz S. (2004) Belowground biomass and productivity of a grazed site and a neighboring un-grazed exclosure in a grassland in central Argentina. Austral Ecology, 29, 201-208.
67. Quentin A.G., Pinkard E.A., Beadle C.L., Wardlaw T.J., O'Grady A.P., Paterson S., Mohammed C.L. (2010) Do artificial and natural defoliation have similar effects on physiology of Eucalyptus globulus Labill. seedlings? Annals of Forest Science, 67, 203-203.
68. Quentin A.G., O'Grady A.P., Beadle C.L., Mohammed C.L., Pinkard E.A. (2012) Interactive effects of water supply and defoliation on photosynthesis, plant water status and growth of Eucalyptus globulus Labill. Tree Physiology, 32, 958-967.
69. Radhika V., Kost C., Bartram S., Heil M., Boland W. (2008) Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta, 228, 449-457.
70. Radhika V., Kost C., Mithöfer A., 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 United States of America, 107, 17228-17233.
71. Rees M. (1995) Community structure in sand dune annuals: is seed weight a key quantity? Oecologia, 83, 857-863.
72. Rhoades D.F. (1979) Evolution of plant defense against herbivores. In: Rosenthal G. A., Janzen D. H. (Eds), Herbivores: their interactions with secondary plant metabolites. Academic Press, NY, USA, pp 55-133.
73. Schädler M., Alphei J., Scheu S., Brandl R., Auge H. (2004) Resource dynamics in an early successional plant community are influenced by insect exclusion. Soil Biology and Biochemistry, 36, 1817-1826.
74. Solomonson L.P. (1981) Cyanide as a metabolic inhibitor. In: Vennesland B., Conn E. E., Knowles C. J., Westby J. (Eds), Cyanide in biology. Academic Press, London, UK, pp 11-28.
75. Southwick E.E. (1984) Photosynthate allocation to floral nectar: a neglected energy investment. Ecology, 65, 1775-1779.
76. Steppuhn A., Gase K., Krock B., Halitschke R., Baldwin I.T. (2004) Nicotine's defensive function in nature. PLoS Biology, 2, e217.
77. Strauss S.Y., Agrawal A.A. (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution, 14, 179-185.
78. Strauss S.Y., Zangerl A.R. (2002) Plant-insect interactions in terrestrial ecosystems. In: Herrera C. M., Pellmyr O. (Eds), Plant-animal interactions: an evolutionary approach. Blackwell, Vic., Australia, pp 77-106.
79. Thamer S., Schädler M., Bonte D., Ballhorn D.J. (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant and Soil, 341, 209-219.
80. Vázquez-Yanes C., Orozco-Segovia A. (1992) Effects of litter from a tropical rainforest on tree seed germination and establishment under controlled conditions. Tree Physiology, 11, 391-400.
81. Walling L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation, 19, 195-216.
82. Weiher E., van der Werf A., Thompson K., Roderick M., Garnier E. (1999) Challenging Theophrastus: a common core list of plant traits for functional ecology. Journal of Vegetation Science, 10, 609-620.
83. Westoby M. (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil, 199, 213-227.
84. Yi H.S., Heil M., Adame-Alvarez R.M., Ballhorn D.J., Ryu C.M. (2009) Airborne induction and priming of plant defences against a bacterial pathogen. Plant Physiology, 151, 2152-2161.
85. Zangerl A.R., Hamilton J.G., Miller T.J., Crofts A.R., Oxborough K., Berenbaum M.R., de Lucia E.H. (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences of the United States of America, 99, 1088-1091.