Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory.

The importance of interspecific competition is a highly controversial and unresolved issue for community ecology in general, and for phytophagous insects in particular. Recent advancements, however, in our understanding of indirect (plant- and enemy-mediated) interactions challenge the historical paradigms of competition. Thus, in the context of this rapidly developing field, we re-evaluate the evidence for interspecific competition in phytophagous insects using a meta-analysis of published studies. Our analysis is specifically designed to test the assumptions underlying traditional competition theory, namely that competitive interactions are symmetrical, necessitate spatial and temporal co-occurrence, and increase in intensity as the density, phylogenetic similarity, and niche overlap of competing species increase. Despite finding frequent evidence for competition, we found very little evidence that plant-feeding insects conform to theoretical predictions for interspecific competition. Interactions were highly asymmetrical, similar in magnitude within vs. between feeding guilds (chewers vs. sap-feeders), and were unaffected by the quantity of resources removed (% defoliation). There was mixed support for the effects of phylogeny, spatial/temporal separation, and the relative strength of intra- vs. interspecific competition. Clearly, a new paradigm that accounts for indirect interactions and facilitation is required to describe how interspecific competition contributes to the organization of phytophagous insect communities, and perhaps to other plant and animal communities as well.

[1]  A. Agrawal Future directions in the study of induced plant responses to herbivory , 2005 .

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

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

[4]  R. Karban,et al.  Effects of an early-season folivorous moth on the success of a later-season species, mediated by a change in the quality of the shared host, Lupinus arboreus Sims , 1986, Oecologia.

[5]  D. Potter,et al.  Early spring defoliation, secondary leaf flush, and leafminer outbreaks on American holly , 1989, Oecologia.

[6]  J. Connell Diversity and the coevolution of competitors, or the ghost of competition past , 1980 .

[7]  R. Marquis,et al.  ECOSYSTEM ENGINEERING BY CATERPILLARS INCREASES INSECT HERBIVORE DIVERSITY ON WHITE OAK , 2003 .

[8]  G. F. Gause The struggle for existence , 1971 .

[9]  K. Raffa,et al.  Interactions Among Insect Herbivore Guilds: Influence of Thrips Bud Injury on Foliar Chemistry and Suitability to Gypsy Moths , 1998, Journal of Chemical Ecology.

[10]  J. Davidson,et al.  The Influence of Rainfall, Evaporation and atmospheric Temperature on Fluctuations in the Size of a natural Population of Thrips imaginis (Thysanoptera). , 1948 .

[11]  M. Hochberg,et al.  Competition between kingdoms. , 1990, Trends in ecology & evolution.

[12]  R. Karban Community organization of Erigeron glaucus folivores: Effects of competition, predation and host plant , 1989 .

[13]  J. Lawton 6. Non-Competitive Populations, Non-Convergent Communities, and Vacant Niches: The Herbivores of Bracken , 1984 .

[14]  S. Wratten,et al.  Wound-induced changes in the acceptability of tree-foliage to Lepidoptera: within-leaf effects , 1988 .

[15]  R. Hamilton,et al.  Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations. , 2007, Ecology.

[16]  C. Darwin The Origin of Species by Means of Natural Selection, Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[17]  Thomas W. Schoener,et al.  Resource Partitioning in Ecological Communities , 1974, Science.

[18]  J. Lawton,et al.  Insects on Plants , 1984 .

[19]  R. Karban,et al.  Jasmonate‐mediated induced plant resistance affects a community of herbivores , 2001 .

[20]  Simon Gates,et al.  Review of methodology of quantitative reviews using meta‐analysis in ecology , 2002 .

[21]  A. Agrawal INDUCED RESPONSES TO HERBIVORY IN WILD RADISH: EFFECTS ON SEVERAL HERBIVORES AND PLANT FITNESS , 1999 .

[22]  V. Volterra Fluctuations in the Abundance of a Species considered Mathematically , 1926, Nature.

[23]  Ian T. Baldwin,et al.  Volatile Signaling in Plant-Plant Interactions: "Talking Trees" in the Genomics Era , 2006, Science.

[24]  S. Faeth CHAPTER 13 – Plant-Mediated Interactions between Seasonal Herbivores: Enough for Evolution or Coevolution? , 1988 .

[25]  Anita Narwani,et al.  SPECIFICITY IN INDUCED PLANT RESPONSES SHAPES PATTERNS OF HERBIVORE OCCURRENCE ON SOLANUM DULCAMARA , 2005 .

[26]  Dean C. Adams,et al.  RESAMPLING TESTS FOR META‐ANALYSIS OF ECOLOGICAL DATA , 1997 .

[27]  D. Strong Harmonious Coexistence of Hispine Beetles on Heliconia In Experimental and Natural Communities , 1982 .

[28]  R. Karban Interspecific Competition Between Folivorous Insects on Erigeron Glaucus , 1986 .

[29]  G. Gauze The struggle for existence, by G. F. Gause. , 1934 .

[30]  J. M. Scriber,et al.  Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids , 2000, Oecologia.

[31]  M. Stout,et al.  Characterization of induced resistance in tomato plants , 1996 .

[32]  H Charles J Godfray,et al.  Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. , 2006, Annual review of entomology.

[33]  J. Grinnell Field Tests of Theories Concerning Distributional Control , 1917, The American Naturalist.

[34]  T. Rand HERBIVORE‐MEDIATED APPARENT COMPETITION BETWEEN TWO SALT MARSH FORBS , 2003 .

[35]  T. Tammaru,et al.  Induced resistance of host tree foliage during and after a natural insect outbreak , 1999 .

[36]  Alfred J. Lotka,et al.  The growth of mixed populations: Two species competing for a common food supply , 1978 .

[37]  T. Ohgushi Indirect Interaction Webs: Herbivore-Induced Effects Through Trait Change in Plants , 2005 .

[38]  J. Lawton Vacant niches and unsaturated communities: a comparison of bracken herbivores at sites on two continents. , 1982 .

[39]  Jessica Gurevitch,et al.  A Meta-Analysis of Competition in Field Experiments , 1992, The American Naturalist.

[40]  J. Lawton,et al.  Community Patterns and Competition in Folivorous Insects , 1981, The American Naturalist.

[41]  A. Agrawal,et al.  COMMUNITY‐WIDE IMPACTS OF HERBIVORE‐INDUCED PLANT RESPONSES IN MILKWEED (ASCLEPIAS SYRIACA) , 2004 .

[42]  D. Janzen Host Plants as Islands. II. Competition in Evolutionary and Contemporary Time , 1973, The American Naturalist.

[43]  H. C. Hanson,et al.  Plant competition : an analysis of community functions , 1929 .

[44]  H. Ross PRINCIPLES OF NATURAL COEXISTENCE INDICATED BY LEAFHOPPER POPULATIONS , 1957 .

[45]  I. Baldwin,et al.  Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. , 2004, The Plant journal : for cell and molecular biology.

[46]  A. Agrawal,et al.  Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca , 2004 .

[47]  C. Darwin On the Origin of Species by Means of Natural Selection: Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[48]  J. R. Ott,et al.  Interspecific interactions in phytophagous insects : competition reexamined and resurrected , 1995 .

[49]  T. Jermy Is there competition between phytophagous insects?1 , 2009 .

[50]  R. Denno,et al.  Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes. , 2006, Ecological applications : a publication of the Ecological Society of America.

[51]  R. Marquis,et al.  Ecological Communities: Effects of arthropods as physical ecosystem engineers on plant-based trophic interaction webs , 2007 .

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

[53]  Jessica Gurevitch,et al.  STATISTICAL ISSUES IN ECOLOGICAL META‐ANALYSES , 1999 .

[54]  B. Rathcke Competition and Coexistence with A Guild of Herbivorous Insects , 1976 .

[55]  I. Kaplan,et al.  APHIDS ALTER THE COMMUNITY‐WIDE IMPACT OF FIRE ANTS , 2005 .

[56]  R. Mayer,et al.  Effects of Sessile Whitefly Nymphs (Homoptera: Aleyrodidae) on Leaf-Chewing Larvae (Lepidoptera: Noctuidae) , 1999 .

[57]  Richard Karban,et al.  Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. , 2006, Ecology.

[58]  A. Eshel,et al.  Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks , 1995 .

[59]  J. Schultz,et al.  Chapter 6 – Community Structure and Folivorous Insect Outbreaks: The Roles of Vertical and Horizontal Interactions , 1987 .

[60]  D. Strong 3. Exorcising the Ghost of Competition Past: Phytophagous Insects , 1984 .

[61]  R. Denno,et al.  Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle , 2007, Oecologia.

[62]  M. Wise,et al.  Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant , 2002 .

[63]  C. Josh Donlan,et al.  Golden eagles, feral pigs, and insular carnivores: How exotic species turn native predators into prey , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Thomas Park,et al.  Interspecies Competition in Populations of Trilobium confusum Duval and Trilobium castaneum Herbst , 1948 .

[65]  Daniel Simberloff,et al.  Ecological Communities: Conceptual Issues and the Evidence , 1984 .

[66]  L. Rockwood Seasonal Changes in the Susceptibility of Crescentia Alata Leaves to the Flea Beetle, Oedionychus SP. , 1974 .

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

[68]  D. Wise,et al.  Terrestrial Trophic Cascades: How Much Do They Trickle? , 2001, The American Naturalist.

[69]  M. Begon,et al.  Ecology: From Individuals to Ecosystems , 2005 .

[70]  Joseph H. Connell,et al.  On the Prevalence and Relative Importance of Interspecific Competition: Evidence from Field Experiments , 1983, The American Naturalist.

[71]  R. Denno,et al.  2 Plant-mediated interactions in herbivorous insects : mechanisms , symmetry , and challenging the paradigms of competition past , 2006 .

[72]  M. Hassell,et al.  Asymmetrical competition in insects , 1981, Nature.

[73]  M. Bonsall,et al.  Enemy-mediated apparent competition: empirical patterns and the evidence , 2000 .

[74]  Thomas W. Schoener,et al.  Field Experiments on Interspecific Competition , 1983, The American Naturalist.

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

[76]  V. Volterra Fluctuations in the Abundance of a Species considered Mathematically , 1926 .

[77]  J. Stachowicz Mutualism, Facilitation, and the Structure of Ecological Communities , 2001 .

[78]  A. Agrawal Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars , 2000 .

[79]  V. Ossipov,et al.  Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak , 1998, Oecologia.

[80]  J. Bruno,et al.  Inclusion of facilitation into ecological theory , 2003 .

[81]  S. Faeth Indirect Interactions Between Temporally Separated Herbivores Mediated by the Host Plant , 1986 .

[82]  G. Arnqvist,et al.  MetaWin: Statistical Software for Meta-Analysis with Resampling Tests. Version 1.Michael S. Rosenberg , Dean C. Adams , Jessica Gurevitch , 1998 .