FEEDBACK BETWEEN INDIVIDUAL HOST SELECTION BEHAVIOR AND POPULATION DYNAMICS IN AN ERUPTIVE HERBIVORE

We examined the role of population density in host selection behavior of an eruptive insect herbivore, the spruce beetle Dendroctonus rufipennis. We conducted field and laboratory experiments on spruce beetles from 29 endemic and eruptive populations in Alaska and Utah, USA, and Yukon, Canada. Beetles from both population phases colonized trees that had been felled to remove host defenses. However, only beetles from eruptive populations colonized defended, healthy trees. A series of laboratory assays using host-based media amended with varying concentrations of phytochemicals identified several factors affecting population-dependent responses to hosts. First, beetles were repelled by high concentrations of the predominant spruce monoterpene, alpha-pinene, but intermediate concentrations elicited entry and gallery construction. Second, heritability assays suggested high genetic variance of host selection behavior within populations, and between-population differences persisted following rearing in a common environment. Third, beetles from eruptive populations were less likely to enter medium amended with phytochemicals and constructed shorter galleries, which disagreed with our prediction and seemingly contradicted the field observations. However, fourth, beetle avoidance of high concentrations of alpha-pinene decreased with the addition of other beetles, and this effect was more pronounced among beetles from eruptive populations than among those from endemic populations. This interaction broadened the host range of eruptive beetles. We propose that such density-dependent behaviors can maintain heterogeneity among population phases and contribute to positive feedback in herbivore population dynamics. A conceptual model suggests how heritable and environmentally induced variation in host selection behavior can affect bimodal equilibria and numerical thresholds in eruptive species.

[1]  B. Strom,et al.  VISUAL AND SEMIOCHEMICAL DISRUPTION OF HOST FINDING IN THE SOUTHERN PINE BEETLE , 1999 .

[2]  G. M. Filip,et al.  Beetle-pathogen interactions in conifer forests , 1993 .

[3]  R. C. Beckwith SCOLYTID FLIGHT IN WHITE SPRUCE STANDS IN ALASKA , 1972, The Canadian Entomologist.

[4]  David L. Wood,et al.  THE ROLE OF PHEROMONES, KAIROMONES, AND ALLOMONES IN THE HOST SELECTION AND COLONIZATION BEHAVIOR OF BARK BEETLES , 1982 .

[5]  D. Bigger,et al.  High-density populations of diamondback moth have broader host-plant diets , 1997, Oecologia.

[6]  S. Lessard,et al.  Equilibrium structure and stability in a frequency-dependent, two-population diploid model , 2001, Journal of mathematical biology.

[7]  K. Raffa,et al.  EFFECTS OF FOLIVORY ON SUBCORTICAL PLANT DEFENSES: CAN DEFENSE THEORIES PREDICT INTERGUILD PROCESSES? , 2001 .

[8]  G. Varley,et al.  Estimating the relative roles of top-down and bottom-up forces on insect herbivore populations: a classic study revisited. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Jaenike Effects of early adult experience on host selection in insects: Some experimental and theoretical results , 2005, Journal of Insect Behavior.

[10]  J. L. Foltz,et al.  Plasticity in life-history traits of the bark beetle Ips calligraphus as influenced by phloem thickness , 1987, Oecologia.

[11]  K. Hopper,et al.  Risk-spreading and bet-hedging in insect population biology. , 1999, Annual review of entomology.

[12]  A. Berryman,et al.  The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae) , 1983 .

[13]  Robert D. Holt,et al.  Genetic Variation for Habitat Preference: Evidence and Explanations , 1991, The American Naturalist.

[14]  P. Price Darwinian Methodology and the Theory of Insect Herbivore Population Dynamics , 1991 .

[15]  Brian D. Farrell,et al.  IS SPECIALIZATION A DEAD END? THE PHYLOGENY OF HOST USE IN DENDROCTONUS BARK BEETLES (SCOLYTIDAE) , 1998, Evolution; international journal of organic evolution.

[16]  S. Via THE QUANTITATIVE GENETICS OF POLYPHAGY IN AN INSECT HERBIVORE. I. GENOTYPE‐ENVIRONMENT INTERACTION IN LARVAL PERFORMANCE ON DIFFERENT HOST PLANT SPECIES , 1984, Evolution; international journal of organic evolution.

[17]  A. Berryman Towards a theory of insect epidemiology , 1978, Researches on Population Ecology.

[18]  John Alcock,et al.  Symposium: Insect Behavioral Ecology--'81: Natural Selection and Communication among Bark Beetles , 1982 .

[19]  M. Atkins Behavioural Variation Among Scolytids in Relation to Their Habitat , 1966, The Canadian Entomologist.

[20]  Robert N. Coulson,et al.  Population Dynamics of Bark Beetles , 1979 .

[21]  R. Dukas Ecological relevance of associative learning in fruit fly larvae , 1999, Behavioral Ecology and Sociobiology.

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

[23]  E. Desouhant,et al.  Oviposition pattern of phytophagous insects: on the importance of host population heterogeneity , 1998, Oecologia.

[24]  A. Munson,et al.  The Spruce Beetle , 1999 .

[25]  P. Turchin,et al.  Scramble competition in the southern pine beetle, Dendroctonus frontalis , 1998 .

[26]  D. Ebert,et al.  GENETIC VARIATION IN A HOST‐PARASITE ASSOCIATION: POTENTIAL FOR COEVOLUTION AND FREQUENCY‐DEPENDENT SELECTION , 2001, Evolution; international journal of organic evolution.

[27]  Kenneth F. Raffa,et al.  Mixed messages across multiple trophic levels: the ecology of bark beetle chemical communication systems , 2001, CHEMOECOLOGY.

[28]  P. L. Lorio Environmental stress and whole-tree physiology , 1993 .

[29]  D. Hildebrand,et al.  Volatiles from flowers of Nicotiana sylvestris, N. otophora and Malus × domestica: headspace components and day/night changes in their relative concentrations. , 1990 .

[30]  S. Larsson,et al.  Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant? , 1995 .

[31]  R. Werner,et al.  Response of Lutz, Sitka, and white spruce to attack by Dendroctonus rufipennis (Coleoptera: Scolytidae) and blue stain fungi , 1994 .

[32]  P. Mayhew Adaptive patterns of host-plant selection by phytophagous insects , 1997 .

[33]  K. Raffa,et al.  Density‐mediated responses of bark beetles to host allelochemicals: a link between individual behaviour and population dynamics , 2002 .

[34]  B. Strom,et al.  Energy Reserves of Individual Southern Pine Beetles (Coleoptera: Scolytidae) as Determined by a Modified Phosphovanillin Spectrophotometry Method , 1994 .

[35]  R. Denno,et al.  Role of Enemy‐Free Space and Plant Quality in Host‐Plant Selection by Willow Beetles , 1990 .

[36]  R. Werner,et al.  Dispersal of the spruce beetle, `dendroctonus rufipennis`, and the engraver beetle, `ips perturbatus`, in Alaska. Forest Service research paper , 1997 .

[37]  M. Rossiter,et al.  INCIDENCE AND CONSEQUENCES OF INHERITED ENVIRONMENTAL EFFECTS , 1996 .

[38]  Y. Carrière Constraints on the evolution of host choice by phytophagous insects , 1998 .

[39]  P. Ehrlich,et al.  Plant Chemistry and Host Range in Insect Herbivores , 1988 .

[40]  G. D. Amman Mountain Pine Beetle (Coleoptera: Scolytidae) Mortality in Three Types of Infestations , 1984 .

[41]  J. Rutledge,et al.  Heritability of Host Acceptance and Gallery Construction Behaviors of the Bark Beetle Ips pini (Coleoptera: Scolytidae) , 2002 .

[42]  K. Raffa,et al.  Combined chemical defenses against an insect-fungal complex , 1996, Journal of Chemical Ecology.

[43]  R. Croteau,et al.  Defense mechanisms of conifers : differences in constitutive and wound-induced monoterpene biosynthesis among species. , 1991, Plant physiology.

[44]  P. A. Morrow,et al.  Specialization: species property or local phenomenon? , 1981, Science.

[45]  D. Raubenheimer,et al.  The selection of nutritionally balanced foods by Locusts migratoria: the interaction between food nutrients and added flavours , 1997 .

[46]  Andrea F. Huberty,et al.  Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. , 2000 .

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

[48]  A. Zangerl,et al.  The Probability of Attack and Patterns of Constitutive and Induced Defense: A Test of Optimal Defense Theory , 1996, The American Naturalist.

[49]  Anurag A. Agrawal,et al.  Phenotypic Plasticity in the Interactions and Evolution of Species , 2001, Science.

[50]  N. Stamp,et al.  Direct and indirect effects of predatory wasps (Polistes sp.: Vespidae) on gregarious caterpillars (Hemileuca lucina: Saturniidae) , 1988, Oecologia.

[51]  K. Ross,et al.  HIERARCHICAL GENETIC STRUCTURE AND GENE FLOW IN MACROGEOGRAPHIC POPULATIONS OF THE EASTERN TENT CATERPILLAR (MALACOSOMA AMERICANUM) , 1994, Evolution; international journal of organic evolution.

[52]  D. Simberloff,et al.  LOCAL ADAPTATION AND AGENTS OF SELECTION IN A MOBILE INSECT , 1995, Evolution; international journal of organic evolution.

[53]  W. Wellington,et al.  INDIVIDUAL DIFFERENCES AS A FACTOR IN POPULATION DYNAMICS: THE DEVELOPMENT OF A PROBLEM , 1957 .

[54]  D. Janzen,et al.  Strategies in Herbivory by Mammals: The Role of Plant Secondary Compounds , 1974, The American Naturalist.

[55]  E. Bernays,et al.  INSECT HERBIVORES: DIFFERENT REASONS FOR BEING A GENERALIST , 1997 .

[56]  G. D. Amman Mountain Pine Beetle Brood Production in Relation to Thickness of Lodgepole Pine Phloem , 1972 .

[57]  Y. Carrière,et al.  Trade‐offs in responses to host plants within a population of a generalist herbivore, Choristoneura rosaceana , 1994 .

[58]  Alan A. Berryman,et al.  DENDROCTONUS PONDEROSAE (COLEOPTERA: SCOLYTIDAE): PRE-AGGREGATION LANDING AND GALLERY INITIATION ON LODGEPOLE PINE , 1980, The Canadian Entomologist.

[59]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[60]  R. Werner,et al.  Factors influencing generation times of spruce beetles in Alaska , 1985 .

[61]  M. Rossiter Use of a secondary host by non-outbreak populations of the gypsy moth. [Pinus rigida; Quercus spp; Lymantria dispar] , 1987 .

[62]  Andrew D. Taylor,et al.  Why Do Populations of Southern Pine Beetles (Coleoptera: Scolytidae) Fluctuate? , 1991 .

[63]  R. Gara,et al.  Arthropod associates of the spruce beetle Dendroctonus rufipennis (Kirby) (Col., Scolytidae) in spruce stands of south‐central and interior Alaska , 1995 .

[64]  K. Raffa,et al.  Prior encounters modulate subsequent choices in host acceptance behavior by the bark beetle Ips pini , 2002 .

[65]  K. Raffa,et al.  Effects of biotic and abiotic stress on induced accumulation of terpenes and phenolics in red pines inoculated with bark beetle-vectored fungus , 1995, Journal of Chemical Ecology.

[66]  M. Zalucki,et al.  Learning in host selection in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) , 1998, Animal Behaviour.

[67]  E. Bernays Plasticity and the Problem of Choice in Food Selection , 1999 .

[68]  R. F. Shepherd,et al.  Factors Influencing the Orientation and Rates of Activity of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae) , 1966, The Canadian Entomologist.

[69]  K. Raffa,et al.  Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes , 1995, Oecologia.

[70]  K. Raffa,et al.  Influences of Host Chemicals and Internal Physiology on the Multiple Steps of Postlanding Host Acceptance Behavior of Ips pini (Coleoptera: Scolytidae) , 2000 .

[71]  D. Wood,et al.  Host selection behavior of bark beetles (Coleoptera: Scolytidae) attackingPinus ponderosa, with special emphasis on the western pine beetle,Dendroctonus brevicomis , 2004, Journal of Chemical Ecology.

[72]  S. Larsson,et al.  Influence of plant quality on pine sawfly population dynamics , 2000 .

[73]  T. L. Payne,et al.  Southern Pine Beetle , 2009 .

[74]  D. Bartos Integrated Control of Scolytid Bark Beetles , 2004 .