Skip to main content Accessibility help
  • Print publication year: 2014
  • Online publication date: December 2013

5 - Seedling herbivory and the temporal niche


Seedlings and the temporal niche

The facilitation of plant coexistence via temporal variation in plant recruitment is increasingly studied (see this volume plus Pake and Venable 1996, Chesson and Huntly 1997, Kelly and Bowler 2002, Verhulst et al. 2008). For the most part however, corroborating studies have examined fluctuations in abiotic factors and the role of biotic agents has been largely overlooked. This omission is symptomatic of the plant coexistence literature in general; the role of predators, herbivores, pathogens and parasites in maintaining species coexistence is more often assumed than demonstrated (but see Kelly and Bowler 2009a). Nonetheless, while a number of agents, biotic and abiotic, result in the death of entire seedling cohorts, foremost among the factors limiting seedling recruitment is herbivory (Moles and Westoby 2004, Fenner and Thompson 2005). Herbivore attack has obvious effects on seedling demography (Lindquist and Carroll 2004, Maron and Crone 2006, Maron and Kauffman 2006), but even beyond population-level considerations, selective seedling removal also exerts long-lasting effects on plant community composition. We propose that temporal fluctuation in herbivore populations, and consequently variation in the intensity of herbivory experienced by plants during their regeneration phase, exerts a powerful influence over plant species contribution to the established community.

There are four necessary conditions of any temporal dynamic involving herbivory. First, seedling herbivores must be capable of moderating plant community composition in established vegetation. Second, herbivores should select preferred seedlings on the basis of readily apparent ecophysiological characteristics. Third, and related to the previous assumption, any variation in seedling susceptibility to herbivore attack (i.e. defensive traits) will most probably correlate with competitive ability. Finally, herbivore populations must show fluctuations in numbers and therefore variation in their influence on regenerating plants. Consequently, before it is possible to develop any conceptual framework to explain how temporal variation in seedling herbivory influences species coexistence, we must first evaluate the evidence for these conditions.

Aars, J. and Ims, R.A. (2002). Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83, 3449–3456.
Agrawal, A. A. and Fishbein, M. (2006). Plant defense syndromes. Ecology 87, S132–S149.
Asquith, N. M. and Mejia-Chang, M. (2005). Mammals, edge effects, and the loss of tropical forest diversity. Ecology 86, 379–390.
Barnes, H. F. and Weil, J. W. (1944). Slugs in gardens: their numbers, activities and distribution: Part I. Journal of Animal Ecology 13, 140–175.
Barton, K. E. (2007). Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. American Journal of Botany 94, 56–66.
Barton, K. E. and Koricheva, J. (2010). The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. American Naturalist 175, 481–493.
Bergelson, J. and Purrington, C. B. (1996). Surveying patterns in the cost of resistance in plants. American Naturalist 148, 536–558.
Bierman, S. M., Fairbairn, J. P., Petty, S. J. et al. (2006). Changes over time in the spatiotemporal dynamics of cyclic populations of field voles (Microtus agrestis L.). American Naturalist 167, 583–590.
Boege, K. and Marquis, R. J. (2005). Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution 20, 441–448.
Bryant, J. P., Clausen, T. P., Swihart, R. K. et al. (2009). Fire drives transcontinental variation in tree birch defense against browsing by snowshoe hares. American Naturalist 174, 13–23.
Burt-Smith, G. S., Grime, J. P. and Tilman, D. (2003). Seedling resistance to herbivory as a predictor of relative abundance in a synthesised prairie community. Oikos 101, 345–353.
Buschmann, H., Keller, M., Porret, N., Dietz, H. and Edwards, P.J. (2005). The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Functional Ecology 19, 291–298.
Chesson, P. and Huntly, N. (1997). The roles of harsh and fluctuating conditions in the dynamics of ecological communities. American Naturalist 150, 519–553.
Crawley, M. J. (1997). Plant-herbivore dynamics. In Crawley, M. J. (ed.), Plant Ecology, 2nd edn. Oxford: Blackwell, pp. 401–474.
Darwin, C. R. (1859). The Origin of Species. London: John Murray.
Elger, A., Lemoine, D. G., Fenner, M. and Hanley, M. E. (2009). Plant ontogeny and chemical defence: older seedlings are better defended. Oikos 118, 767–773.
Elton, C. R. (1924). Periodic fluctuations in the numbers of animals: their causes and effects. British Journal of Experimental Biology 2, 119–163.
Elton, C. R. (1927). Animal Ecology. London: Sidgwick and Jackson.
Fenner, M., Hanley, M. E. and Lawrence, R. (1999). Comparison of seedling and adult palatability in annual and perennial plants. Functional Ecology 13, 546–551.
Fenner, M. and Thompson, K. (2005). The Ecology of Seeds, 2nd edn. Cambridge: Cambridge University Press.
Fine, P. V. A., Miller, Z. J., Mesones, I. et al. (2006). The growth defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87, S150–S162.
Gause, G. F. (1932). Experimental studies on the struggle for existence. I. Mixed population of two species of yeast. Journal of Experimental Biology 9, 389–402.
Glynn, C., Herms, D. A., Orians, C. M., Hansen, R. C. and Larsson, S. (2007). Testing the growth differentiation balance hypothesis: dynamic responses of willows to nutrient availability. New Phytologist 176, 623–634.
Green, P.T., Lake, P. S. and O’Dowd, D. J. (1997). Control of seedling recruitment by land crabs in rain forest on a remote island. Ecology 78, 2474–2486.
Green, P. T., O’Dowd, D. J. and Lake, P. S. (2008). Recruitment dynamics in a rainforest seedling community: context-independent impact of a keystone consumer. Oecologia 156, 737–385.
Grime, J. P., Thompson, K., Hunt, R. et al. (1997). Integrated screening validates primary axes of specialisation in plants. Oikos 79, 259–281.
Hanley, M. E. (2004). Seedling herbivory and the influence of plant species richness in seedling neighbourhoods. Plant Ecology 170, 35–42.
Hanley, M. E., Collins, S. A. and Swann, C. (2011). Advertising acceptability: is mollusk olfaction important in seedling selection? Plant Ecology 212, 727–731.
Hanley, M. E., Cordier, P. K., May, O. C. and Kelly, C. K. (2007a). Seed size and seedling growth: differential response of Australian and British Fabaceae to nutrient limitation. New Phytologist 174, 381–388.
Hanley, M. E. and Fegan, E. L. (2007). Timing of cotyledon damage affects growth and flowering in mature plants. Plant, Cell and Environment 30, 812–819.
Hanley, M. E., Fenner, M. and Edwards, P. J. (1995a). An experimental field study of the effects of mollusc grazing on seedling recruitment and survival in grassland. Journal of Ecology 83, 621–627.
Hanley, M. E., Fenner, M. and Edwards, P. J. (1995b). The effect of seedling age on the likelihood of herbivory by the slugDeroceras reticulatum. Functional Ecology 9, 754–759.
Hanley, M. E., Fenner, M. and Edwards, P. J. (1996a). The effect of mollusc grazing on seedling recruitment in artificially created grassland gaps. Oecologia 106, 240–246.
Hanley, M. E., Fenner, M. and Edwards, P. J. (1996b). Mollusc grazing and seedling survivorship of four common grassland species: the role of gap size, species and season. Acta Oecologica 17, 331–341.
Hanley, M. E., Fenner, M., Whibley, H. and Darvil, B. (2004). Early plant growth: identifying the end point of the seedling phase. New Phytologist 163, 61–66.
Hanley, M. E. and Lamont, B. B. (2001). Herbivory, serotiny and seedling defence in Western Australian Proteaceae species. Oecologia 126, 409–417.
Hanley, M. E. and Lamont, B. B. (2002). Relationships between physical and chemical attributes of seedlings: how important is seedling defence? Functional Ecology 16, 216–222.
Hanley, M. E., Lamont, B. B., Fairbanks, M. M. and Rafferty, C. M. (2007b). Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8, 157–178.
Hanley, M. E. and May, O. C. (2006). Cotyledon damage at the seedling stage affects growth and flowering potential in mature plants. New Phytologist 169, 243–250.
Hanley, M. E. and Sykes, R. J. (2009). Impacts of seedling herbivory on plant competition and implications for species coexistence. Annals of Botany 103, 1347–1353.
Harborne, J. B. (1993). Introduction to Ecological Biochemistry, 4th edn. London: Academic Press.
Haring, D. A., Huber, M. J., Suter, D., Edwards, P. J. and Luescher, A. (2008). Plant enemy derived elicitors increase the foliar tannin concentration of Onobrychis viciifolia without a trade-off to growth. Annals of Botany 102, 979–987.
Herms, D. A. and Mattson, W. J. (1992). The dilemma of plants: to grow or to defend. Quarterly Review of Biology 67, 283–335.
Ims, R. A., Henden, J.-A. and Killengreen, S. T. (2007). Collapsing population cycles. Trends in Ecology and Evolution 23, 79–86.
Izhaki, I. and Ne’eman, G. (1996). The importance of porcupine and bast scale on Aleppo pine recruitment after fire. Acta Oecologica 17, 97– 107.
Kalamees, R. and Zobel, M. (2002). The role of the seed bank in gap regeneration in a calcareous grassland community. Ecology 83, 1017–1025.
Kelly, C. K. and Bowler, M.G. (2002). Coexistence and relative abundance in forest tree species. Nature 417, 437–440.
Kelly, C. K. and Bowler, M.G. (2005). A new application of storage dynamics: differential sensitivity, diffuse competition and temporal niches. Ecology 86, 1012–1022.
Kelly, C. K. and Bowler, M.G. (2009a). Investigating the role of enemies in temporal niche dynamics: differential sensitivity, competition, and stable coexistence. Theoretical Population Biology 76, 278–284.
Kelly, C. K. and Bowler, M.G. (2009b). Temporal niche dynamics, relative abundance and phylogenetic signal in coexisting species. Theoretical Ecology 2, 161–169.
Kelly, C. K. and Hanley, M. E. (2005). Juvenile growth and palatability in congeneric British herbs. American Journal of Botany 92, 1586–1589.
Kendall, B. E., Prendergast, J. and Bjørnstad, O.N. (1998). The macroecology of population dynamics: taxonomic and biogeographic patterns in population cycles. Ecology Letters 1, 160–164.
Koricheva, J. (2002). Meta-analysis of sources of variation in fitness costs of plant anti-herbivore defences. Ecology 83, 176–190.
Lambin, X., Bretagnolle, V. and Yoccoz, N. G. (2006). Vole population cycles in northern and southern Europe: is there a need for different explanations for single pattern? Journal of Animal Ecology 75, 340–349.
Leimu, R. and Koricheva, J. (2006). A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112, 1–9.
Lindquist, E. S. and Carroll, C.R. (2004). Differential seed and seedling predation by crabs: impacts on tropical coastal forest composition. Oecologia 141, 661–671.
Lindquist, E. S., Krauss, K. W., Green, P. T. et al. (2009). Land crabs as key drivers in tropical coastal forest recruitment. Biological Reviews 84, 203–223.
Maron, J. L. and Crone, E. (2006). Herbivory: effects on plant abundance, distribution and population growth. Proceedings of the Royal Society of London B 273, 2575–2584.
Maron, J. L. and Kauffman, M. J. (2006). Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology 87, 113–124.
Meserve, P. L. (1971). Population ecology of prairie vole, Microtus ochrogaster, in western mixed prairie of Nebraska. American Midland Naturalist 86, 417–433.
Moles, A. T. and Westoby, M. (2004). What do seedlings die from and what are the implications for evolution of seed size? Oikos 106, 193–199.
Pake, C. E. and Venable, D. L. (1996). Seed banks in desert annuals: implications for persistence and coexistence in variable environments. Ecology 77, 1427–1435.
Rafferty, C., Lamont, B.B. and Hanley, M. E. (2005). Selective feeding by western grey kangaroos on seedlings of Hakea species varying in morphology and chemistry. Plant Ecology 177, 201–208.
Schaffner, U., Vrieling, K. and van der Meijden, E. (2003). Pyrrolizidine alkaloid content in Senecio: ontogeny and developmental constraints. Chemoecology 13, 39–46.
Siegal, S. and Castellan, N. J. (1988). Nonparametric Statistics for the Behavioral Sciences, 2nd edn. New York: McGraw-Hill.
Stamp, N. (2003). Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78, 23–55.
Strauss, S. Y., Stanton, M. L., Emery, N. C et al. (2009). Cryptic seedling herbivory by nocturnal introduced generalists impacts survival, performance of native and exotic plants. Ecology 90, 419–429.
Symondson, W. O. C., Glen, D. M., Ives, A. R., Langdon, C. J. and Wiltshire, C. W. (2002). Dynamics of the relationship between a generalist predator and slugs over five years. Ecology 83, 137–147.
Tiffin, P. (2000). Mechanisms of tolerance to herbivore damage: what do we know? Evolutionary Ecology 14, 523–536.
Vasconcelos, H. L. and Cherrett, J. M. (1997). Leaf-cutting ants and early forest regeneration in central Amazonia: Effects of herbivory on tree seedling establishment. Journal of Tropical Ecology 13, 357–370.
Vehviläinen, H. and Koricheva, J. (2006). Moose and vole browsing patterns in experimentally manipulated pure and mixed forest stands. Ecography 29, 497–506.
Vehviläinen, H., Koricheva, J. and Ruohomaki, K. (2007). Tree species diversity influences herbivore abundance and damage: meta-analysis of long-term forest experiments. Oecologia 152, 287–298.
Verhulst, J., Montaña, C., Mandujano, M. C. and Franco, M. (2008). Demographic mechanisms in the coexistence of two closely related perennials in a fluctuating environment. Oecologia 156, 95–105.
Westoby, M., Leishman, M. R. and Lord, J. (1996). Comparative ecology of seed size and dispersal. In Silvertown, J., Franco, M. and Harper, J. L. (eds), Plant Life Histories: Ecology, Phylogeny and Evolution. Cambridge: Cambridge University Press, pp. 143–162.