The Effects of Plant Compensatory Regrowth and Induced Resistance on Herbivore Population Dynamics

Outbreaks of herbivorous insects are detrimental to natural and agricultural systems, but the mechanisms driving outbreaks are not well understood. Plant responses to herbivory have the potential to produce outbreaks, but long-term effects of plant responses on herbivore dynamics are understudied. To quantify these effects, we analyze mathematical models of univoltine herbivores consuming annual plants with two responses: (1) compensatory regrowth, which affects herbivore survival in food-limited situations by increasing the amount of food available to the herbivore; and (2) induced resistance, which reduces herbivore survival proportional to the strength of the response. Compensatory regrowth includes tolerance, where plants replace some or all of the consumed biomass, and overcompensation, where plants produce more biomass than was consumed. We found that overcompensation can cause bounded fluctuations in the herbivore density (called outbreaks here) by itself, whereas neither tolerance nor induced resistance can cause an outbreak on its own. Food limitation and induced resistance can also drive outbreaks when they act simultaneously. Tolerance damps these outbreaks, but overcompensation, by contrast, qualitatively changes the conditions under which the outbreaks occur. Not properly accounting for these interactions may explain why it has been difficult to document plant-driven insect outbreaks and could undermine efforts to control herbivore populations in agricultural systems.

[1]  J. Fornoni,et al.  The Evolution of Resistance and Tolerance to Herbivores , 2007 .

[2]  Mathematical analysis of a model for a plant-herbivore system , 1993 .

[3]  P. Tiffin Mechanisms of tolerance to herbivore damage:what do we know? , 2000, Evolutionary Ecology.

[4]  Julia Koricheva,et al.  A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies , 2006 .

[5]  A. Joern,et al.  Plasticity and overcompensation in grass responses to herbivory , 1993, Oecologia.

[6]  M. Crawley,et al.  Contrasting dynamics in the same plant–herbivore interaction , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Fornoni,et al.  Geographic association and temporal variation of chemical and physical defense and leaf damage in Datura stramonium , 2013, Ecological Research.

[8]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[9]  A. Kessler,et al.  Plant‐Induced Responses and Herbivore Population Dynamics , 2012 .

[10]  A. J. Belsky Does Herbivory Benefit Plants? A Review of the Evidence , 1986, The American Naturalist.

[11]  W. Morris,et al.  Disentangling Effects of Induced Plant Defenses and Food Quantity on Herbivores by Fitting Nonlinear Models , 1997, The American Naturalist.

[12]  J. Bergelson,et al.  The effects of foliage damage on casebearing moth larvae, Coleophora serratella, feeding on birch , 1986 .

[13]  S. Wratten,et al.  Wound induced defences in plants and their consequences for patterns of insect grazing , 1983, Oecologia.

[14]  Frédéric Grognard,et al.  Direct and apparent compensation in plant-herbivore interactions , 2014 .

[15]  A. Agrawal,et al.  Insect Outbreaks Revisited: Barbosa/Insect Outbreaks Revisited , 2012 .

[16]  E. Simms,et al.  THE EVOLUTIONARY ECOLOGY OF TOLERANCE TO CONSUMER DAMAGE , 2000 .

[17]  I. Baldwin,et al.  Plant responses to insect herbivory: the emerging molecular analysis. , 2002, Annual review of plant biology.

[18]  Karen C. Abbott,et al.  Simultaneous effects of food limitation and inducible resistance on herbivore population dynamics. , 2008, Theoretical population biology.

[19]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[20]  Alan A. Berryman,et al.  The theory and classification of outbreaks. , 1987 .

[21]  B. Kendall,et al.  WHY DO POPULATIONS CYCLE? A SYNTHESIS OF STATISTICAL AND MECHANISTIC MODELING APPROACHES , 1999 .

[22]  J. Myers,et al.  Can a General Hypothesis Explain Population Cycles of Forest Lepidoptera , 1988 .

[23]  Patric Nilsson,et al.  Herbivory, inducible defence and population oscillations : a preliminary theoretical analysis , 1994 .

[24]  Stephen P. Ellner,et al.  POPULATION CYCLES IN THE PINE LOOPER MOTH: DYNAMICAL TESTS OF MECHANISTIC HYPOTHESES , 2005 .

[25]  J. A. Barone,et al.  HERBIVORY AND PLANT DEFENSES IN TROPICAL FORESTS , 1996 .

[26]  A. Kessler,et al.  Overcompensating plants: their expression of resistance traits and effects on herbivore preference and performance , 2012 .

[27]  Y. Buckley,et al.  Stable coexistence of an invasive plant and biocontrol agent: a parameterized coupled plant-herbivore model , 2005 .

[28]  M. Rausher Co-evolution and plant resistance to natural enemies , 2001, Nature.

[29]  A. Agrawal,et al.  Overcompensation of plants in response to herbivory and the by-product benefits of mutualism. , 2000, Trends in plant science.

[30]  B. E. Silkstone The consequences of leaf damage for subsequent insect grazing on birch (Betula spp.) , 1987, Oecologia.

[31]  D. G. Brown,et al.  Direct and indirect effects of prior grazing of goldenrod upon the performance of a leaf beetle , 1995 .

[32]  N. Underwood The Influence of Induced Plant Resistance on Herbivore Population Dynamics , 1999 .

[33]  M. Rausher,et al.  THE EFFECTS OF HOST-PLANT GENOTYPE ON HERBIVORE POPULATION DYNAMICS , 2000 .

[34]  Leah Edelstein-Keshet,et al.  Mathematical theory for plant—herbivore systems , 1986 .

[35]  Brian D. Inouye,et al.  INDUCED VS. CONSTITUTIVE RESISTANCE AND THE SPATIAL DISTRIBUTION OF INSECT HERBIVORES AMONG PLANTS , 2005 .

[36]  M. Oesterheld,et al.  Effect of defoliation on grass growth. A quantitative review , 2002 .

[37]  A. Agrawal,et al.  The ecology and evolution of plant tolerance to herbivory. , 1999, Trends in ecology & evolution.

[38]  Andrei Alyokhin,et al.  Colorado potato beetle management on potatoes: current challenges and future prospects. , 2009 .

[39]  N. Underwood,et al.  The Influence of Plant and Herbivore Characteristics on the Interaction between Induced Resistance and Herbivore Population Dynamics , 1999, The American Naturalist.

[40]  M. Rosenzweig Paradox of Enrichment: Destabilization of Exploitation Ecosystems in Ecological Time , 1971, Science.

[41]  P. Nilsson,et al.  INDUCTION OF OVERCOMPENSATION IN THE FIELD GENTIAN, GENTIANELLA CAMPESTRIS , 1998 .

[42]  A. Kessler,et al.  The enemy as ally: herbivore-induced increase in crop yield. , 2010, Ecological applications : a publication of the Ecological Society of America.

[43]  Donald L. DeAngelis,et al.  Inducible defences and the paradox of enrichment , 2004 .

[44]  A. Agrawal Plant Defense and Density Dependence in the Population Growth of Herbivores , 2004, The American Naturalist.

[45]  A. Honěk,et al.  Intraspecific variation in body size and fecundity in insects: a general relationship , 1993 .

[46]  K. Anderson,et al.  Modeling herbivore competition mediated by inducible changes in plant quality. , 2009 .

[47]  Troy Day,et al.  A Biologist's Guide to Mathematical Modeling in Ecology and Evolution , 2007 .

[48]  Michael S. Gaines,et al.  Biological Populations with Nonoverlapping Generations : Stable Points , Stable Cycles , and Chaos , 2007 .

[49]  J. Schultz,et al.  Chapter 16 – Insect Population Dynamics and Induction of Plant Resistance: The Testing of Hypotheses , 1987 .

[50]  T. Juenger,et al.  The evolution of tolerance to damage in Gentianella campestris: natural selection and the quantitative genetics of tolerance , 2000, Evolutionary Ecology.

[51]  N. Underwood Density dependence in induced plant resistance to herbivore damage: threshold, strength and genetic variation , 2000 .

[52]  Karline Soetaert,et al.  A Practical Guide to Ecological Modelling: Using R as a Simulation Platform , 2008 .

[53]  Leah Edelstein-Keshet,et al.  The Effects of Inducible Plant Defenses on Herbivore Populations. 1. Mobile Herbivores in Continuous Time , 1989, The American Naturalist.

[54]  I. Baldwin,et al.  Constraints on an induced defense: the role of leaf area , 1994, Oecologia.

[55]  A. Berryman What causes population cycles of forest Lepidoptera? , 1996, Trends in ecology & evolution.

[56]  Anurag A. Agrawal,et al.  Induced Plant Defenses Against Pathogens and Herbivores : Biochemistry, Ecology, and Agriculture , 1999 .

[57]  F. Grognard,et al.  Modelling plant compensatory effects in plant-insects dynamics , 2012, 2012 IEEE 4th International Symposium on Plant Growth Modeling, Simulation, Visualization and Applications.

[58]  EVOLUTION OF MIXED STRATEGIES OF PLANT DEFENSE ALLOCATION AGAINST NATURAL ENEMIES , 2004, Evolution; international journal of organic evolution.

[59]  Tolerance in plant ecology and evolution: toward a more unified theory of plant–herbivore interaction , 2004, Evolutionary Ecology.

[60]  M. Rausher,et al.  Comparing the Consequences of Induced and Constitutive Plant Resistance for Herbivore Population Dynamics , 2002, The American Naturalist.

[61]  S. McNaughton Compensatory plant growth as a response to herbivory , 1983 .

[62]  Bruce A. McPheron,et al.  Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies , 1980 .

[63]  Greg Dwyer,et al.  Food limitation and insect outbreaks: complex dynamics in plant-herbivore models. , 2007, The Journal of animal ecology.

[64]  L. Slobodkin,et al.  Community Structure, Population Control, and Competition , 1960, The American Naturalist.

[65]  B. Kendall,et al.  DYNAMICAL EFFECTS OF PLANT QUALITY AND PARASITISM ON POPULATION CYCLES OF LARCH BUDMOTH , 2003 .