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Plant allocation of carbon to defense as a function of herbivory, light and nutrient availability

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Abstract

We use modeling to determine the optimal relative plant carbon allocations between foliage, fine roots, anti-herbivore defense, and reproduction to maximize reproductive output. The model treats these plant components and the herbivore compartment as variables. Herbivory is assumed to be purely folivory. Key external factors include nutrient availability, degree of shading, and intensity of herbivory. Three alternative functional responses are used for herbivory, two of which are variations on donor-dependent herbivore (models 1a and 1b) and one of which is a Lotka–Volterra type of interaction (model 2). All three were modified to include the negative effect of chemical defenses on the herbivore. Analysis showed that, for all three models, two stable equilibria could occur, which differs from most common functional responses when no plant defense component is included. Optimal strategies of carbon allocation were defined as the maximum biomass of reproductive propagules produced per unit time, and found to vary with changes in external factors. Increased intensity of herbivory always led to an increase in the fractional allocation of carbon to defense. Decreases in available limiting nutrient generally led to increasing importance of defense. Decreases in available light had little effect on defense but led to increased allocation to foliage. Decreases in limiting nutrient and available light led to decreases in allocation to reproduction in models 1a and 1b but not model 2. Increases in allocation to plant defense were usually accompanied by shifts in carbon allocation away from fine roots, possibly because higher plant defense reduced the loss of nutrients to herbivory.

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References

  • Ågren GI, Bosatta E (1996) Theoretical ecosystem ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392

    Google Scholar 

  • Boyle RR, McLean S, Brandøn S, Wiggins N (2005) Rapid absorption of dietary 1,8-cineole results in critical blood concentration of cineole and immediate cessation of eating in the common brushtail possoum (Trichosurus vulpecula). J Chem Ecol 31:2775–2790

    Article  PubMed  CAS  Google Scholar 

  • Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Buckley TN, Roberts DW (2005a) DESPOT, a process-based tree growth model that allocates carbon to maximize carbon gain. Tree Phys 26:129–144

    Article  Google Scholar 

  • Buckley TN, Roberts DW (2005b) How should leaf area, sapwood area and stomatal conductance vary with tree height to maximize growth? Tree Phys 26:145–157

    Article  Google Scholar 

  • Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. BioScience 37:49–57

    Article  Google Scholar 

  • Chapin FS III, Schulze E, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Coley P, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Comins HN, McMurtrie RE (1993) Long-term response of nutrient-limited forests to CO2 enrichment; equilibrium behavior of plant-soil models. Ecol Appl 3:666–681

    Article  Google Scholar 

  • Craine JM (2009) Resource strategies of wild plants. Princeton University Press, Princeton

    Google Scholar 

  • Dybzinski R, Farrior C, Wolf A, Reich PB, Pacala SW (2011) Evolutionarily stable strategy carbon allocation to foliage, wood, and fine roots in trees competing for light and nitrogen: an analytically tractable, individual-based model and quantitative comparisons to data. Amer Natur 177:153–166

    Article  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter caterpillars. Ecology 51:565–581

    Article  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347

    Article  Google Scholar 

  • Gayler S, Grams TEE, Heller W, Treutter D, Priesack E (2008) A dynamical model of environmental effects on allocation to carbon-based secondary compounds in juvenile trees. Ann Bot Lond 101:1089–1098

    Article  CAS  Google Scholar 

  • Givnish TJ (1995) Plant stems: biomechanical adaptation for energy capture and influence on species distributions. In: Gartner BL (ed) Plant stems: physiology and functional morphology. Chapman & Hall, New York, pp 3–49

    Google Scholar 

  • Grubb PJ (1992) A positive distrust in simplicity—lessons from plant defences and from competition among plants and among animals. J Ecol 80:585–610

    Article  Google Scholar 

  • Herbert DA, Rastetter EB, Shaver GR, Ågren GI (1999) Effects of plant growth characteristics on plant biogeochemistry and community composition in a changing climate. Ecosystems 2:367–382

    Article  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335

    Article  Google Scholar 

  • Hof J, Rideout D, Binkley D (1990) Carbon fixation in trees as a micro optimization process: an example of combining ecology and economics. Ecol Econ 2:243–256

    Article  Google Scholar 

  • Ju S, DeAngelis DL (2009) The R* rule and energy flux in a plant-nutrient ecosystem. J Theor Biol 256(3):326–332

    Article  PubMed  CAS  Google Scholar 

  • Ju S, DeAngelis DL (2010) Nutrient fluxes at the landscape level and the R* rule. Ecol Model 221:141–146

    Article  CAS  Google Scholar 

  • King DA (1993) A model analysis of the influence of root and foliage allocation on forest production and competition between trees. Tree Phys 12:119–135

    Google Scholar 

  • Kozlowski TT (1971) Growth and development of trees, vol 1. Academic, New York

    Google Scholar 

  • Kramer PJ, Kozlowski TT (1979) Physiology of woody plants phytochemistry and insect performance. J Chem Ecol 27:1289–1313

    Google Scholar 

  • Mäkelä A, Valentine HT, Helmisaari H-S (2008) Optimal co-allocation of carbon and nitrogen in a forest stand at steady state. New Phytol 180:114–123

    Article  PubMed  Google Scholar 

  • Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Ann Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 55–133

    Google Scholar 

  • McLean S, Duncan AJ (2006) Pharmacological perspectives on the detoxification of plant secondary metabolites: implications for ingestive behavior of herbivores. J Chem Ecol 32:1213–1228

    Article  PubMed  CAS  Google Scholar 

  • Moran N, Hamilton WD (1980) Low nutritive quality as defense against herbivores. J Theor Biol 86:247–254

    Article  Google Scholar 

  • Osier T, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27(7):1289–1313

    Article  PubMed  CAS  Google Scholar 

  • Osier TL, Hwang S, Lindroth RL (2000) Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol Entom 25:197–2007

    Article  Google Scholar 

  • Perry DA (1994) Forest ecosystems. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Rastetter EB, Ågren GI, Shaver GR (1997) Responses of N-limited ecosystems to increased CO2: a balanced-nutrition, coupled-element-cycles model. Ecol Applic 7:444–460

    Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, Orlando, pp 3–54

    Google Scholar 

  • Schulz JC (1983) Habitat selection and foraging tactic of caterpillars in heterogeneous trees. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic, New York, pp 61–90

    Google Scholar 

  • White TCR (1993) The inadequate environment. Springer, Berlin

    Book  Google Scholar 

Download references

Acknowledgment

DLD was supported by the Biological Resources Division of the US Geological Survey, Southeast Ecological Science Center, and National Science Foundation grant NSF-DMS-0920828. The research of RL was supported by the EPSCoR start-up funds of the University of Wyoming.

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Authors and Affiliations

  1. U.S. Geological Survey, University of Miami, Coral Gables, FL, USA

    Donald L. DeAngelis

  2. Biology Department, University of Miami, Coral Gables, FL, 33124, USA

    Donald L. DeAngelis & Shu Ju

  3. Department of Mathematics and Department of Zoology and Physiology, University of Wyoming, Laramie, WY, USA

    Rongsong Liu

  4. Institute of Arctic Biology, University of Alaska, Fairbanks, AK, USA

    John P. Bryant

  5. University of Surrey, Guildford, Surrey, UK

    Stephen A. Gourley

Authors
  1. Donald L. DeAngelis
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  2. Shu Ju
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  3. Rongsong Liu
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  4. John P. Bryant
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  5. Stephen A. Gourley
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Correspondence to Donald L. DeAngelis.

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DeAngelis, D.L., Ju, S., Liu, R. et al. Plant allocation of carbon to defense as a function of herbivory, light and nutrient availability. Theor Ecol 5, 445–456 (2012). https://doi.org/10.1007/s12080-011-0135-z

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  • DOI: https://doi.org/10.1007/s12080-011-0135-z

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