Abstract
The evolution of tolerance is one potential plant response to selection imposed by herbivores. Plant architecture, and in turn, sectoriality may influence a plant's ability to tolerate tissue loss. However, each may either constrain or facilitate a plant's ability to compensate following herbivore attack depending on the plant part damaged and the identity of the damaging herbivore.
Plants are limited in their ability to respond to localized damage by chewing insects because carbon does not flow freely from damaged to undamaged plant parts, particularly between branches. Thus, defoliation of individual branches invariably results in decreased growth and reproduction of those branches. Within branches, carbon flow via vascular connections between orthostichies may ameliorate the effects of damage restricted within an orthostichy. Local induction of secondary chemicals to spread damage by folivores throughout a plant's canopy, redistribution of resources within and between IPU's, and delaying reproductive activity until resources have been pooled may all alleviate the constraints on response of plants to grazing.
In contrast to the effects of damage by grazers, the metameric construction of plants typically ensures points of regrowth from dormant buds when apical meristems are destroyed either by vertebrate browsers or galling insects. Sectoriality constrains the ability of sap-sucking insects to tap the entire resource base of a plant, thus having a positive effect on plant fitness. However, both the site and timing of attack mitigate the degree of limitation imposed by sectoriality. During peak periods of assimilation, photosynthate flow is mainly over short distances (between sources and sinks within the canopy), and thus sap-sucking insects have a small resource base to draw upon. In contrast, when sucking insects tap into vascular elements in which the flow is from roots to leaves and vice versa, resource availability to the insect (and in turn, potential resource loss from the plant) are only limited by the resources present in those vascular elements.
Studies of specific traits in species which demonstrate differential tolerance would greatly add to our understanding of herbivore impacts on plant growth and reproduction. In particular, intraspecific variation in tolerance has been documented for individuals within and among populations with different grazing histories. A number of traits related to sectoriality and architecture probably contribute to such variation in tolerance, and because they are easily manipulated and easily quantified, represent potentially profitable avenues of research. These traits include distribution of leaves and buds, ability to release secondary meristems from dormancy, and the timing of resource movement both before and subsequent to damage.
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Alpert P., Newell E. A., Chu C., Glyphis J., Gulmon S. L., Hollinger D. Y., Johnson N. D., Mooney H. A. & Puttick G. 1985. Allocation to reproduction in the chaparral shrub, Diplacus aurantiacus. Oecologia 66: 309–316.
Baker, W. L. 1972. Eastern forest insects. U.S. Department of Agriculture, Forest Service Miscellaneous Publication No. 1175, Washington, D.C.
Bazzaz F. A., Carlson R. W. & Harper J. L. 1979. Contribution to reproductive effort by photosynthesis of flowers and fruits. Nature 279: 554–555.
Beck C. B., Schmid R. and Rothwell G. W. 1982. Stelar morphology and the primary vascular system of seed plants. Bot. Rev. 48: 691–815.
Belsky A. J. 1986. Does herbivory benefit plants? A review of the evidence. Amer. Nat. 127: 870–892.
Benner B. L. 1988. Effects of apex removal and nutrient supplementation on branching and seed production in Thlaspi arvense (Brassicaceae). American Journal of Botany 75: 645–651.
Bergelson J. & Crawley M. J. 1992a. Herbivory and Ipomopsis aggregata: the disadvantages of being eaten. Amer. Nat. 139: 870–882.
Bergelson J. & Crawley M. J. 1992b. The effects of grazers on the performance of individuals and populations of scarlet gilia, Ipomopsis aggregata. Oecologia 90: 435–444.
Bertin R. I. 1982. The ecology of sex expression in red buckeye. Ecology 63: 445–456.
Chan C. B. & Cain J. C. 1967. The effect of seed formation on subsequent flowering in apple. Proc. of the Amer. Soc. of Hort. Sci. 91: 63–68.
Coleman J. S. & Leonard A. S. 1995. Why it matters where on a leaf a folivore feeds. Oecologia 101: 324–328.
Coley P. D., Bryant J. P. & ChapinIII F. S. 1985. Resource availability and plant antiherbivore defense. Science 230: 895–899.
Cook C. W. & Stoddart L. A. 1960. Physiological responses of big sagebrush to different types of herbage removal. J. Range Manag. 13: 14–16.
Danell K., Huss-Danell K. & Bergstrom R. 1985. Interactions between browsing moose and two species of birch in Sweden. Ecology 66: 1867–1878.
Davis J. 1967. Some effects of deer browsing on chamise sprouts after fire. Amer. Midl. Nat. 77: 234–238.
Davis J. M., Gordon M. P. & Smit B. A. 1991. Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Proc. Nat. Acad. Sci., USA 88: 2392–2396.
DeClerk-Floate R. & Price P. W. 1994. Impact of a bud-galling midge on bud populations of Salix exigua. Oikos 70: 253–260.
DeStevens D. & Putz F. E. 1984. Mortality rates of some rain forest palms in Panama. Principes 29: 162–165.
DeLong D. M. 1971. The bionomics of leafhoppers. Ann. Rev. Entom. 16: 179–210.
Denno R. F., McClure M. S. & Ott J. R. 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Ann. Rev. of Entom. 40: 297–331.
Doak D. F. 1991. The consequences of herbivory for dwarf fireweed: different time scales, different morphological scales. Ecology 72: 1397–1407.
Dyer M. I., Acra M. A., Wang G. M., Coleman D. C., Freckman D. W., McNaughton S. J. & Strain B. R. 1991. Source-sink carbon relations in two Panicum coloratum ecotypes in response to herbivory. Ecology 72: 1472–1483.
Edwards P. J. & Wratten S. D. 1983. Wound induced defences in plants and their consequences for patterns of insect grazing. Oecologia 59: 88–93.
Fay P. A. & Hartnett D. C. 1991. Constraints on growth and allocation patterns of Silphium integrifolium (Asteraceae) caused by a cynipid gall wasp. Oecologia 88: 243–250.
Feeny P. 1976. Plant apparency and chemical defense. pp. 1–40. In: Wallace J. W. & Mansell R. L. (eds), Biochemical interaction between plants and insects. Plenum Press, New York.
Fox J. F. 1995. Shoot demographic responses to manipulation of reproductive effort by bud removal in a willow. Oikos 72:283–287.
Garrish R. S. & Lee T. D. 1989. Physiological integration in Cassia fasciculata Michx.: inflorescence removal and defoliation experiments. Oecologia 81: 279–284.
Geber M. A. 1990. The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution 44: 799–819.
Gold W. G. & Caldwell M. M. 1989a. The effects of spatial pattern of defoliation on regrowth of a tussock grass. I. Growth responses. Oecologia 80: 289–296.
Gold W. G. & Caldwell M. M. 1989b. The effects of spatial pattern of defoliation on regrowth of a tussock grass. II. Canopy gas exchange. Oecologia 81: 437–442.
Hall F. R. & Ferree D. C. 1976. Effects of insect injury simulation on photosynthesis of apple leaves. J. Econ. Entom. 69: 245–248.
Hartnett D. C. & Abrahamson W. G. 1979. The effects of stem gall insects on life history patterns on Solidago canadensis. Ecology 60: 910–917.
Haukioja E. 1991. The influence of grazing on the evolution, morphology and physiology of plants as modular organisms. Phil. Trans. Roy. Soc. Lond. B 333: 241–247.
Haukioja E., Ruohomäki K., Senn J. Suomela J. & Walls M. 1990. Consequences of herbivory in the mountain birch (Betula pubescens ssp. tortuosa): importance of the functional organization of the tree. Oecologia 82: 238–247.
Honkanen T. & Haukioja E. 1994. Why does a branch suffer more after branch-wide than after tree-wide defoliation? Oikos 71: 441–450.
Honkanen T., Haukioja E. & Suomela J. 1994. Effects of simulated defoliation and debudding on needle and shoot growth in Scots pine (Pinus sylvestris): implications of plant source/sink relationships for plant-herbivore studies. Funct. Ecol. 8: 631–639.
Horber E. 1980. Types and classification of resistance. pp. 15–21. In: Maxwell F. G. and Jennings P. R. (eds), Breeding plants resistant to insects, Wiley, New York.
Horton M. & Lacey E. P. 1994. Carbon integration in Plantago aristata (Plantaginaceae): the reproductive effects of defoliation. Amer. J. Bot. 81: 278–286.
Isebrands J. G., Dickson R. E. & Larson P. R. 1976. Translocation and incorporation of 14C into the petiole from different regions within developing cottonwood leaves. Planta 128: 185–194.
Janzen D. H. 1976. Effect of defoliation on fruit-bearing branches of the Kentucky coffee tree, Gymnocladus dioicus (Leguminosae). Amer. Midl. Nat. 95: 474–478.
Jones C. G., Hopper R. F., Coleman J. S. and Krischik V. A. 1993. Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93: 452–456.
Karlsson P. S. 1994. The significance of internal nutrient cycling in branches for growth and reproduction of Rhododendron lapponicum. Oikos 70: 191–200.
Kerley G. I. H., Tiver F. & Whitford W. G. 1993. Herbivory of clonal populations: cattle browsing affects reproduction and population structure of Yucca elata. Oecologia 93: 12–17.
Larson K. C. & Whitham T. G. 1991. Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88: 15–21.
Larson P. R. 1977. Phyllotactic transitions in the vascular system of Populus deltoides Bartr. as determined by 14C labeling. Planta 134:241–249.
Larson P. R. & Dickson R. E. 1973. Distribution of imported 14C in developing leaves of eastern cottonwood according to phyllotaxy. Planta 111: 95–112.
Larson P. R. & Dickson R. E. 1986. 14C translocation pathways in honeylocust and green ash: Woody plants with complex leaf forms. Phys. Plant. 66: 21–30.
Lee S. Y. 1991. Herbivory as an ecological process in a Kandelia candel (Rhizophoraceae) mangal in Hong Kong. Journal of Trop. Ecol. 7: 337–348.
Lehtilä, K. 1996. Optimal distribution of herbivory and localized compensatory responses within a plant. Vegetatio this volume (in press).
Lehtilä K., Tuomi J. & Sulkinoja M. 1994. Bud demography of the mountain birch Betula pubescens ssp. tortuosa near tree line. Ecology 75: 945–955.
Lowman M. D. 1982. Effects of different rates and methods of leaf area removal on rain forest seedlings of coachwood (Ceratopetalum apetalum). Aust. J. Bot. 30: 477–483.
Marquis R. J. 1988. Intra-crown variation in leaf herbivory and seed production in striped maple, Acer pensylvanicum L. (Aceraceae). Oecologia 77: 52–55.
Marquis R. J. 1991. Physiological constraints on response by Ostrya virginiana (Betulaceae) to localized folivory. Can. J. Bot. 69: 1951–1955.
Marquis R. J. 1992. A bite is a bite is a bite? Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73: 143–152.
Marshall D. L. 1989. Integration of response to defoliation within plants of two species of Sesbania. Funct. Ecol. 3: 207–214.
Mauricio R., Bowers M. D. & Bazzaz F. A. 1993. Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74: 2066–2071.
McCarthy B. C. & Quinn J. A. 1992. Fruit maturation patterns of Carya spp. (Juglandaceae): an intra-crown analysis of growth and reproduction. Oecologia 91: 30–38.
McClure M. S. & Price P. W. 1975. Competition and coexistence among sympatric Erythroneura leafhoppers (Homoptera: Cicadellidae) on American sycamore. Ecology 56: 1388–1397.
McCrea K. D., Abrahamson W. G. & Weis A. E. 1985. Goldenrod ball gall effects on Solidago altissima: 14C translocation and growth. Ecology 66: 1902–1907.
Miquelle D. G. 1983. Browse regrowth and consumption following sumer defoliation by moose. J. Wildl. Manag. 47: 17–24.
Moran N. A. & Whitham T. G. 1990. Interspecific competition between root-feeding and leaf-galling aphids mediated by hostplant resistance. Ecology 71: 1050–1058.
Obeso J. R. & Grubb P. J. 1993. Fruit maturation in the shrub Ligustrum vulgare (Oleaceae): lack of defoliation effects. Oikos 68: 309–316.
Oesterheld M. & McNaughton S. J. 1988. Intraspecific variation in the response of Themeda triandra to defoliation: the effect of time of recovery and growth rates on compensatory growth. Oecologia 77: 181–186.
Owen-Smith N., Robbins C. T. & Hagerman A. E. 1993. Browse and browsers: interactions between woody plants and mammalian herbivores. Tr. Ecol. Evol. 8: 158–160.
Paige K. N. & Whitham T. G. 1987. Overcompensation in response to mammalian herbivory: The advantages of being eaten. Amer. Nat. 129: 407–416.
Painter R. H. 1958. Resistance of plants to insects. Ann. Rev. Entom. 3: 267–290.
Pilson D. 1992. Aphid distribution and the evolution of goldenrod resistance. Evolution 46: 1358–1372.
Polley H. W. & Detling J. K. 1990. Grazing-mediated differentiation in Agropyron smithii: evidence from populations with different grazing histories. Oikos 57: 326–332.
Price E. A. C. & Hutchings M. J. 1992. The causes and developmental effects of integration and independence between different parts of Glechoma hederacea clones. Oikos 63: 376–386.
Price E. A. C., Marshall C. & Hutchings M. J. 1992. Studies of growth in the clonal herb Glechoma hederacea. I. Patterns of physiological integration. J. Ecol. 80: 25–38.
Quinlan J. D. 1969. Mobilization of 14C in the spring following autumn assimilation of 14CO2 by apple rootstock. J. Hort. Sci. 44: 107–110.
Rosenthal, G. A. & Berenbaum, M. R. 1992. Herbivores, their interactions with secondary plant metabolites. V. II. Ecological and evolutionary processes. Second edition. Academic Press.
Rosenthal J. P. & Kotanen P. M. 1994. Terrestrial plant tolerance to herbivory. Tr. Ecol. Evol. 9: 145–148.
Roundy B. A. & Ruyle G. B. 1989. Effects of herbivory on twig dynamics of a Sonoran desert shrub Simmondsia chinensis (Link) Schn. J. Appl. Ecol. 26: 701–710.
Scott A. W. & Whalley R. D. B. 1984. The influence of intensive sheep grazing on genotypic differentiation in Danthonia linkii, D. richardsonii and D. racemosa on the New England Tablelands. Aust. J. Ecol. 9: 419–429.
Senn J. & Haukioja E. 1994. Reactions of the mountain birch to bud removal: effects of severity and timing, and implications for herbivores. Funct. Ecol. 8: 494–501.
Shea M. M. & Watson M. A. 1989. Patterns of leaf and flower removal: their effect on fruit growth in Chamaenerion angustifolium (fireweed). Amer. J. Bot. 76: 884–890.
Snow A. A. & Stanton M. L. 1988. Aphids limit fecundity of a weedy annual (Raphanus sativus). Am. J. Bot. 75: 589–593.
Spears E. E.Jr. & May P. G. 1988. Effect of defoliation on gender expression and fruit set in Passiflora incarnata. Amer. J. Bot. 75: 1842–1847.
Sprugel D. G., Hinckley T. M. & Schaap W. 1991. The theory and practice of branch autonomy. Ann. Rev. Ecol. and Syst. 22: 309–334.
Stephenson A. G. 1980. Fruit set, herbivory, fruit reduction, and the fruiting strategies of Catalpa speciosa (Bignoniaceae). Ecology 61: 57–64.
Stickler F. C. & Pauli A. W. 1961. Leaf removal in grain sorghum. I. Effects of certain defoliation treatments on yield and components of yield. Agr. J. 53: 99–102.
Thomas L. P. & Watson M. A. 1988. Leaf removal and the apparent effects of architectural constraints on development in Capsicum annuum. Amer. J. Bot. 75: 840–843.
Trumble J. T., Kolodny-Hirsch D. M. & Ting I. P. 1993. Plant compensation for arthropod herbivory. Ann. Rev. of Entom. 38: 93–119.
Tscharntke T. 1992. Coexistence, tritrophic interactions and density dependence in a species-rich parasitoid community. J. Anim. Ecol. 61: 59–67.
Tuomi J., Nilsson P. & Éström M. 1994. Plant compensatory reponses: bud dormancy as an adaptation to herbivory. Ecology 75: 1429–1436.
Tuomi J., Niemelä P., Rousi M., Sirén S. & Vuorisalo T. 1988a. Induced accumulation of foliage phenols in mountain birch: branch response to defoliation? Amer. Nat. 132: 602–608.
Tuomi J., Nisula S., Vuorisalo T., Niemelä P. & Jormalainen V. 1988b. Reproductive effort of short shoots in silver birch (Betula pendula Roth). Experientia 44: 540–541.
Tuomi J., Vuorisalo T., Niemelä P., Nisula S. & Jormalainen V. 1988c. Localized effects of branch defoliations on weight gain of female inflorescences in Betula pubescens. Oikos 51: 327–330.
Tuomi J., Vuorisalo T., Niemelä P. & Haukioja E. 1989. Effects of localized defoliations on female inflorescences in mountain birch, Betula pubescens ssp. tortuosa. Can. J. Bot. 67: 334–338.
van derMeijden E., Wijn M. & Verkaar H. J. 1988. Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51: 355–363.
Vranjic J. A. & Gullan P. J. 1990. The effect of a sap-sucking herbivore, Eriococcus coriaceus (Homoptera: Eriococcidae), on seedling growth and architecture in Eucalyptus blakelyi. Oikos 59: 157–162.
Watson M. A. 1986. Integrated physiological units in plants. Tr. Ecol. Evol. 1: 119–123.
Watson M.A. & Casper B.B. 1984. Morphogenetic constraints on patterns of carbon distribution in plants. Ann. Rev. Ecol. Syst. 15: 233–258.
Weis A. E. 1984. Apical dominance asserted over lateral buds by the gall of Rhabdophaga strobiloides (Diptera: Cecidomyiidae). Can. Entom. 116: 1277–1279.
Weis A. E. & Kapelinski A. 1984. Manipulation of host plant development by the gall-midge Rhabdophaga strobiloides. 1984. Ecol. Entom. 9: 457–465.
Whitham T. G. & Mopper S. 1985. Chronic herbivory: impacts on architecture and sex expression of pinyon pine. Science 228: 1089–1091.
Whitham T.G., Maschinski J., Larson K.C. & Paige K.N. 1991. Plant responses to herbivory: the continuum from negative to positive and underlying physiological mechanisms. pp. 227–256. In: Price P. W., Lewinsohn T. M., Fernandes G. W., & W. W.Benson (eds), Plant-animal interactions, evolutionary ecology in tropical and temperate regions. Wiley, New York.
Wisdom C. S., Crawford C. S. & Aldon E. F. 1989. Influence of insect herbivory on photosynthetic area and reproduction in Gutierrezia species. J. Ecol. 77: 685–692.
Zangerl A. R. & Berenbaum M. R. 1990. Furanocoumarin induction in wild parsnip: Genetics and populational variation. Ecology 71: 1933–1940.
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Marquis, R.J. Plant architecture, sectoriality and plant tolerance to herbivores. Vegetatio 127, 85–97 (1996). https://doi.org/10.1007/BF00054850
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DOI: https://doi.org/10.1007/BF00054850