Food limitation and insect outbreaks: complex dynamics in plant-herbivore models.

1. The population dynamics of many herbivorous insects are characterized by rapid outbreaks, during which the insects severely defoliate their host plants. These outbreaks are separated by periods of low insect density and little defoliation. In many cases, the underlying cause of these outbreaks is unknown. 2. Mechanistic models are an important tool for understanding population outbreaks, but existing consumer-resource models predict that severe defoliation should happen much more often than is seen in nature. 3. We develop new models to describe the population dynamics of plants and insect herbivores. Our models show that outbreaking insects may be resource-limited without inflicting unrealistic levels of defoliation. 4. We tested our models against two different types of field data. The models successfully predict many major features of natural outbreaks. Our results demonstrate that insect outbreaks can be explained by a combination of food limitation in the herbivore and defoliation and intraspecific competition in the host plant.

[1]  A. Nicholson,et al.  The Balance of Animal Populations.—Part I. , 1935 .

[2]  Judea Pearl,et al.  Direct and Indirect Effects , 2001, UAI.

[3]  B. Kendall,et al.  Single-species models for many-species food webs , 2002, Nature.

[4]  R. B. Root,et al.  Interactive Effects of Different Types of Herbivore Damage: Trirhabda beetle Larvae and Philaenus spittlebugs on Goldenrod (Solidago altissima) , 2002 .

[5]  E. Haukioja,et al.  On the Role of Plant Defences in the Fluctuation of Herbivore Populations , 1980 .

[6]  Sanyi Tang,et al.  Chaos in functional response host–parasitoid ecosystem models , 2002 .

[7]  D. Levin,et al.  The Ecological and Genetic Consequences of Density-Dependent Regulation in Plants , 1980 .

[8]  Ian T. Baldwin,et al.  The Reproductive Consequences Associated with Inducible Alkaloidal Responses in Wild Tobacco , 1990 .

[9]  C. S. Holling,et al.  The structure and behavior of defoliating insect/forest systems , 1981, Researches on Population Ecology.

[10]  F. A. Bazzaz,et al.  THE REGULATION OF LEAF, RAMET AND GENET DENSITIES IN EXPERIMENTAL POPULATIONS OF THE RHIZOMATOUS PERENNIAL SOLIDAGO CANADENSIS , 1985 .

[11]  R. B. Root,et al.  Patterns in Population Change and the Organization of the Insect Community Associated with Goldenrod , 1992 .

[12]  Brian Dennis,et al.  Multiple attractors, saddles, and population dynamics in periodic habitats , 1999, Bulletin of mathematical biology.

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

[14]  Andrew M. Liebhold,et al.  INTRODUCTION: Population dynamics of forest-defoliating insects Are population cycles and spatial synchrony a universal characteristic of forest insect populations? , 2000 .

[15]  J. Beddington,et al.  Mutual Interference Between Parasites or Predators and its Effect on Searching Efficiency , 1975 .

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

[17]  H. Mcbrien,et al.  A Case of Insect Grazing Affecting Plant Succession , 1983 .

[18]  Trirhabda Virgata EFFECTS OF POPULATION DENSITY ON LONG-DISTANCE DISPERSAL IN THE GOLDENROD BEETLE , 1995 .

[19]  Chris Wilcox,et al.  Mobile parasitoids may restrict the spatial spread of an insect outbreak , 1997 .

[20]  D. Lack The natural regulation of animal numbers , 1954 .

[21]  Naoto Kamata,et al.  Are population cycles and spatial synchrony a universal characteristic of forest insect populations? : Population dynamics of forest-defoliating insects , 2000 .

[22]  G. English-loeb,et al.  Testing the resource concentration hypothesis with tarnished plant bug on strawberry: density of hosts and patch size influence the interaction between abundance of nymphs and incidence of damage , 2003 .

[23]  D. A. Raworth,et al.  Insect population ecology in British Columbia , 2001 .

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

[25]  S. Blatt,et al.  PERFORMANCE OF TRIRHABDA VIRGATA (COLEOPTERA: CHRYSOMELIDAE) ON THREE POTENTIAL HOSTS , 1999, The Canadian Entomologist.

[26]  J. Monro,et al.  The Exploitation and Conservation of Resources by Populations of Insects , 1967 .

[27]  David W. Williams,et al.  Influence of weather on the synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks in New England , 1995 .

[28]  C. Krebs,et al.  Population Cycles in Small Mammals , 1974 .

[29]  M. Hunter,et al.  Cycles in insect populations: delayed density dependence or exogenous driving variables? , 1998 .

[30]  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.

[31]  J. Holt,et al.  Modelling pest population resurgence due to recolonization of fields following an insecticide application , 1998 .

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

[33]  John L. Harper,et al.  Population Biology of Plants. , 1978 .

[34]  W. Baltensweiler,et al.  DYNAMICS OF LARCH BUD MOTH POPULATIONS1,2 , 1977 .

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

[36]  R. Holt,et al.  Disentangling Resource and Apparent Competition: Realistic Models for Plant-herbivore Communities , 1998 .

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

[38]  P. McEvoy Insect‐plant interactions on a planet of weeds , 2002 .

[39]  W. Carson,et al.  EXTENDING THE RESOURCE CONCENTRATION HYPOTHESIS TO PLANT COMMUNITIES: EFFECTS OF LITTER AND HERBIVORES , 2003 .

[40]  J. Huisman,et al.  Competition and facilitation in multispecies plant-herbivore systems of productive environments. , 1998 .

[41]  S. D. Cooper,et al.  PRIMARY-PRODUCTIVITY GRADIENTS AND SHORT-TERM POPULATION DYNAMICS IN OPEN SYSTEMS , 1997 .

[42]  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.

[43]  Peter Turchin,et al.  Complex Population Dynamics , 2003 .

[44]  W. Morris,et al.  Population Consequences of Constitutive and Inducible Plant Resistance: Herbivore Spatial Spread , 1997, The American Naturalist.

[45]  J. C. Allen,et al.  Nonlinear Dynamics and Chaos in Insect Populations , 1992 .

[46]  William W. Murdoch,et al.  "Community Structure, Population Control, and Competition"-A Critique , 1966, The American Naturalist.

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

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

[49]  I. Noy-Meir,et al.  Stability of Grazing Systems: An Application of Predator-Prey Graphs , 1975 .

[50]  T. White,et al.  The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants , 1984, Oecologia.

[51]  Jim M Cushing,et al.  ESTIMATING CHAOS AND COMPLEX DYNAMICS IN AN INSECT POPULATION , 2001 .

[52]  Alison F. Hunter,et al.  Traits that distinguish outbreaking and nonoutbreaking Macrolepidoptera feeding on northern hardwood trees , 1991 .

[53]  Michael P. Hassell,et al.  DENSITY-DEPENDENCE IN SINGLE-SPECIES POPULATIONS , 1975 .

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

[55]  C. S. Holling,et al.  Qualitative Analysis of Insect Outbreak Systems: The Spruce Budworm and Forest , 1978 .

[56]  B. Solomon Response of a Host-Specific Herbivore to Resource Density, Relative Abundance, and Phenology , 1981 .

[57]  S. Pacala,et al.  Herbivores and Plant Diversity , 1992, The American Naturalist.

[58]  Kalyan Das,et al.  Stability and oscillations of an autotroph-herbivore model with time delay , 2001 .

[59]  M. Hassell The dynamics of arthropod predator-prey systems. , 1979, Monographs in population biology.

[60]  Naoto Kamata,et al.  Cyclicity and synchrony of historical outbreaks of the beech caterpillar,Quadricalcarifera punctatella (Motschulsky) in Japan , 1996, Researches on Population Ecology.

[61]  L. Milne,et al.  The Balance of Nature , 1953, Oryx.

[62]  M. Cain,et al.  Long-term suppression of insect herbivores increases the production and growth of Solidago altissima rhizomes , 1991, Oecologia.

[63]  R M May,et al.  Biological Populations with Nonoverlapping Generations: Stable Points, Stable Cycles, and Chaos , 1974, Science.

[64]  F. Messina Timing of Dispersal and Ovarian Development in Goldenrod Leaf Beetles, Trirhabda virgata and T. borealis , 1982 .

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

[66]  D. D. Bennett,et al.  EVIDENCE OF SYNCHRONIZED CYCLES IN OUTBREAK PATTERNS OF DOUGLAS-FIR TUSSOCK MOTH, ORGYIA PSEUDOTSUGATA (McDUNNOUGH) (LEPIDOPTERA: LYMANTRIIDAE) , 1988 .

[67]  A. Herzig Effects of Population Density on Long‐Distance Dispersal in the Goldenrod Beetle Trirhabda Virgata , 1995 .

[68]  J. Bryant Phytochemical Deterrence of Snowshoe Hare Browsing by Adventitious Shoots of Four Alaskan Trees , 1981, Science.

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

[70]  M. Duffy,et al.  Selective Predation and Productivity Jointly Drive Complex Behavior in Host‐Parasite Systems , 2004, The American Naturalist.

[71]  I. Bradbury,et al.  Dynamics, structure and performance of shoot populations of the rhizomatous herb Solidago canadensis L. in abandoned pastures , 1981, Oecologia.

[72]  M. Hassell,et al.  Insect Population Ecology: An Analytical Approach , 1974 .

[73]  Mark A. Lewis,et al.  Spatial Coupling of Plant and Herbivore Dynamics: The Contribution of Herbivore Dispersal to Transient and Persistent "Waves" of Damage , 1994 .

[74]  T. R. E. Southwood,et al.  A synoptic population model. , 1976 .

[75]  W. Carson,et al.  HERBIVORY AND PLANT SPECIES COEXISTENCE: COMMUNITY REGULATION BY AN OUTBREAKING PHYTOPHAGOUS INSECT , 2000 .

[76]  O. D. Sholes Herbivory By Species Of Trirhabda (Coleoptera, Chrysomelidae) On Solidago altissima (Asteraceae) - Variation Between Years , 1981 .

[77]  Andrew R. Watkinson,et al.  Density-dependence in single-species populations of plants , 1980 .

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

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

[80]  W. Carson,et al.  Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance , 1999, Oecologia.

[81]  William W. Murdoch,et al.  Consumer-resource dynamics , 2003 .

[82]  David F. Rhoades,et al.  Offensive-Defensive Interactions between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory , 1985, The American Naturalist.

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

[84]  Robert M. May,et al.  Patterns of Dynamical Behaviour in Single-Species Populations , 1976 .

[85]  S. Busenberg,et al.  Habitat suitability and herbivore dynamics. , 1994, Bio Systems.

[86]  A. Nicholson,et al.  Supplement: the Balance of Animal Populations , 1933 .

[87]  C. Elton,et al.  Periodic Fluctuations in the Numbers of Animals: Their Causes and Effects , 1924 .

[88]  Paul R. Ehrlich,et al.  The "Balance of Nature" and "Population Control" , 1967, The American Naturalist.

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

[90]  R. May,et al.  Bifurcations and Dynamic Complexity in Simple Ecological Models , 1976, The American Naturalist.

[91]  B. Schmid,et al.  Experimental demography of rhizome populations of establishing clones of Solidago altissima , 1999 .

[92]  R. Tollrian,et al.  The Ecology and Evolution of Inducible Defenses , 1990, The Quarterly Review of Biology.

[93]  M. Hunter,et al.  Time tells: long‐term patterns in the population dynamics of the yew gall midge, Taxomyia taxi (Cecidomyiidae), over 35 years , 2005 .

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

[95]  Greg Dwyer,et al.  The combined effects of pathogens and predators on insect outbreaks , 2004, Nature.

[96]  T. Whitlow,et al.  Effects of leaf and sap feeding insects on photosynthetic rates of goldenrod , 1992, Oecologia.

[97]  Peter Kareiva,et al.  Spatial ecology : the role of space in population dynamics and interspecific interactions , 1998 .

[98]  Pejman Rohani,et al.  Seasonnally forced disease dynamics explored as switching between attractors , 2001 .

[99]  Andrew M. Liebhold,et al.  Spatial Synchrony in Population Dynamics , 2004 .

[100]  J. Daniel Hare,et al.  Ecology and Management of the Colorado Potato Beetle , 1990 .

[101]  R. B. Root,et al.  Effects of Herbivorous Insects and Soil Fertility on Reproduction of Goldenrod , 1993 .

[102]  R. May,et al.  Infectious diseases and population cycles of forest insects. , 1980, Science.

[103]  Lawrence Stark Stability and Oscillations , 1968 .

[104]  H. B. Wilson,et al.  Chaotic stochasticity: a ubiquitous source of unpredictability in epidemics , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[105]  R. B. Root,et al.  Association between Leaf Beetles and Meadow Goldenrods (Solidago spp.) in Central New York , 1980 .

[106]  S. Harrison,et al.  Population outbreaks in a discrete world. , 2000, Theoretical population biology.

[107]  L. Ginzburg,et al.  Population cycles of forest Lepidoptera: a maternal effect hypothesis , 1994 .

[108]  Andrew M. Liebhold,et al.  What causes outbreaks of the gypsy moth in North America? , 2000, Population Ecology.

[109]  A. Hastings,et al.  The impact of resource limitation and the phenology of parasitoid attack on the duration of insect herbivore outbreaks. , 2002, Theoretical population biology.

[110]  M. Crawley Herbivory: the Dynamics of Animal-plant Interactions , 1984 .

[111]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[112]  D. Hartnett Size-dependent allocation to sexual and vegetative reproduction in four clonal composites , 1990, Oecologia.

[113]  H. G. Andrewartha,et al.  The distribution and abundance of animals. , 1954 .

[114]  C. W. Ramm,et al.  Effects of winter temperatures on gypsy moth egg masses in the Great Lakes region of the United States , 2001 .