The Ecological Consequences of Shared Natural Enemies

When multiple victim species (e.g. prey, host) are attacked by one or more shared enemy species (e.g. predator, pathogen), the potential exists for apparent competition between victim populations. We review ideas on apparent com­ petition (also called "competition for enemy-free space") and sketch illustrative examples. One puzzling aspect of this indirect interaction is the repeated rediscovery of the essential ideas. Apparent competition arises between focal and alternative prey populations because, in the long term, enemy abundance depends on total prey availability; by increasing enemy numbers, alternative prey intensify predation on focal prey. A frequent empirical finding, consistent with theory, is exclusion of victim species from local communities by resident enemies. Theory suggests victim-species coexistence depends on particular conditions. To understand fully the consequences of shared enemies requires a body of contingent theory, specifying the time-scale of the interactions (short­ and long-term consequences of sharing enemies generally differ), the structure of the food-web encompassing the interactions, its spatial context, etc. The "core criterion" for a focal victim species to invade a community supporting a resident, polyphagous enemy is r> aP (the invader's intrinsic rate of increase

[1]  R D Holt,et al.  Intraguild predation: The dynamics of complex trophic interactions. , 1992, Trends in ecology & evolution.

[2]  D. Simberloff,et al.  Conservation of pristine habitats and unintended effects of biological control. , 1992 .

[3]  M. Hochberg,et al.  Population dynamic consequences of direct and indirect interactions involving a large blue butterfly and its plant and red ant hosts , 1994 .

[4]  Helmut Schlumprecht Dispersal of the thistle gallfly Urophora cardui and its endoparasitoid Eurytoma serraiulae (Hymenoptera: Eurytomidae) , 1989 .

[5]  T. E. Martin,et al.  On the advantage of being different: Nest predation and the coexistence of bird species. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[6]  K. Sieving Nest Predation and Differential Insular Extinction among Selected Forest Birds of Central Panama , 1992 .

[7]  Robert D Holt,et al.  Spatial Heterogeneity, Indirect Interactions, and the Coexistence of Prey Species , 1984, The American Naturalist.

[8]  William A. Mitchell,et al.  Diet selection on depletable resources , 1989 .

[9]  D. Wise Spiders in Ecological Webs , 1993 .

[10]  M. McPeek DETERMINATION OF SPECIES COMPOSITION IN THE ENALLAGMA DAMSELFLY ASSEMBLAGES OF PERMANENT LAKES , 1990 .

[11]  Julie A. Savidge,et al.  Extinction of an Island Forest Avifauna by an Introduced Snake , 1987 .

[12]  H. Wilbur,et al.  Experimental Aquatic Food Webs: Interactions between Two Predators and Two Prey , 1990, The American Naturalist.

[13]  S. Strauss,et al.  Indirect effects in community ecology: Their definition, study and importance. , 1991, Trends in ecology & evolution.

[14]  Robert D. Holt,et al.  Prey communities in patchy environments , 1987 .

[15]  J. Estes,et al.  Aleuts, Sea Otters, and Alternate Stable-State Communities , 1978, Science.

[16]  R. Ricklefs,et al.  ASPECT DIVERSITY IN MOTHS: A TEMPERATE‐TROPICAL COMPARISON , 1975, Evolution; international journal of organic evolution.

[17]  D. Wilson,et al.  Equilibrium diet: optimal foraging and prey coexistence , 1986 .

[18]  D. Miller Introductions and extinction of fish in the African great lakes. , 1989, Trends in ecology & evolution.

[19]  William H. Settle,et al.  Invasion by the variegated leafhopper and biotic interactions: parasitism, competition, and apparent competition. , 1990 .

[20]  S. L. Lima,et al.  Behavioral decisions made under the risk of predation: a review and prospectus , 1990 .

[21]  F. Howarth Environmental Impacts of Classical Biological Control , 1991 .

[22]  J. Connell Apparent versus "real" competition in plants. , 1990 .

[23]  B. Menge,et al.  Indirect Effects in Marine Rocky Intertidal Interaction Webs: Patterns and Importance , 1995 .

[24]  J. Lawton,et al.  Range, population abundance and conservation. , 1993, Trends in ecology & evolution.

[25]  S. Louda,et al.  Herbivore influences on plant performance and competitive interactions. , 1990 .

[26]  E. Cameron,et al.  Human influence on the terrestrial biota and biotic communities of New Zealand. , 1993, Trends in ecology & evolution.

[27]  Kimberly G. Smith,et al.  Emergence of 13‐Yr Periodical Cicadas (Cicadidae: Magicicada): Phenology, Mortality, and Predators Satiation , 1993 .

[28]  J. Lawton,et al.  Predation by domestic cats in an English village , 1987 .

[29]  R. Woodman,et al.  Differential larval predation by ants can influence willow sawfly community structure , 1992 .

[30]  J. Madsen,et al.  Study of the breeding ecology and behaviour of the Svalbard population of light-bellied brent goose Branta bernicla hrota , 1989 .

[31]  H. Resit Akçakaya,et al.  Population Cycles of Mammals: Evidence for a Ratio‐Dependent Predation Hypothesis , 1992 .

[32]  K. Church,et al.  The Partridge: Pesticides, Predation and Conservation , 1986 .

[33]  James P. Grover,et al.  Simple Rules for Interspecific Dominance in Systems with Exploitative and Apparent Competition , 1994, The American Naturalist.

[34]  G. Belovsky,et al.  The role of vertebrate and invertebrate predators in a grasshopper community , 1993 .

[35]  S. Louda,et al.  Biotic Interference with Insects Imported for Weed Control , 1976 .

[36]  H. Pulliam,et al.  Sources, Sinks, and Population Regulation , 1988, The American Naturalist.

[37]  L. Hansson Predation in heterogeneous landscapes: how to evaluate total impact? , 1989 .

[38]  Contributions to the global analysis of 3-D Lotka-Volterra equations: Dynamic boundedness and indirect interactions in the case of one predator and two prey , 1991 .

[39]  Mark A. McPeek,et al.  Predation, Competition, and Prey Communities: A Review of Field Experiments , 1985 .

[40]  E. Bernays,et al.  On the Evolution of Host Specificity in Phytophagous Arthropods , 1988 .

[41]  T. Ebenhard Introduced birds and mammals and their ecological effects , 1988 .

[42]  Pamela A. Matson,et al.  Ratio-dependent predator−prey theory , 1992 .

[43]  E. Korpimäki,et al.  Does the year-to-year variation in the diet of eagle and Ural owls support the alternative prey hypothesis? , 1990 .

[44]  R. Holt,et al.  Apparent Competition and Enemy-Free Space in Insect Host-Parasitoid Communities , 1993, The American Naturalist.

[45]  Michael J. Crawley,et al.  Natural Enemies: The Population Biology of Predators, Parasites and Diseases , 1992 .

[46]  A. Dobson,et al.  Parasites, disease and the structure of ecological communities. , 1986, Trends in ecology & evolution.

[47]  S. Carpenter,et al.  Regulation of Lake Primary Productivity by Food Web Structure. , 1987, Ecology.

[48]  J. Addicott Predation and Prey Community Structure: An Experimental Study of the Effect of Mosquito Larvae on the Protozoan Communities of Pitcher Plants , 1974 .

[49]  M. Scott,et al.  Parasitism: A cryptic determinant of animal community structure. , 1991, Trends in ecology & evolution.

[50]  T. Schoener,et al.  Effect of Lizards on Spider Populations: Manipulative Reconstruction of a Natural Experiment , 1987, Science.

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

[52]  R. Holt,et al.  Infectious Disease and Species Coexistence: A Model of Lotka-Volterra Form , 1985, The American Naturalist.

[53]  B. Woodward,et al.  Predator-prey interactions and breeding-pond use of temporary-pond species in a desert anuran community , 1983 .

[54]  B. Menge,et al.  Community Regulation: Variation in Disturbance, Competition, and Predation in Relation to Environmental Stress and Recruitment , 1987, The American Naturalist.

[55]  L. Keith,et al.  Demography and ecology of the arctic hare (Lepus arcticus) in southwestern Newfoundland , 1987 .

[56]  Michael E. Gilpin,et al.  Spiral Chaos in a Predator-Prey Model , 1979, The American Naturalist.

[57]  R. J. Schmitt Indirect Interactions Between Prey: Apparent Competition, Predator Aggregation, and Habitat Segregation. , 1987, Ecology.

[58]  S. Lawler Species richness, species composition and population dynamics of protists in experimental microcosms , 1993 .

[59]  T. Schoener,et al.  An experimental study of the effect of lizards on web-spider communities , 1988 .

[60]  Olof Liberg,et al.  Can Vertebrate Predators Regulate Their Prey? , 1984, The American Naturalist.

[61]  R. Paine Food Web Complexity and Species Diversity , 1966, The American Naturalist.

[62]  W. Murdoch,et al.  Predation and Population Stability , 1975 .

[63]  J. Burdon The Role of Parasites in Plant Populations and Communities , 1994 .

[64]  J. Lawton,et al.  Enemy free space and the structure of ecological communities , 1984 .

[65]  M. Bulmer Phase Relations in the Ten-Year Cycle , 1975 .

[66]  S. Wissinger,et al.  Intraguild Predation and Competition Between Larval Dragonflies: Direct and Indirect Effects on Shared Prey , 1993 .

[67]  F. Ito,et al.  Variance of ant effects on the different life forms of moth caterpillars , 1991 .

[68]  R. Reader Herbivory as a Confounding Factor in an Experiment Measuring Competition Among Plants , 1992 .

[69]  M. Macgarvin,et al.  The Impact of Hairy Wood Ants, Formica lugubris, on the Guild Structure of Herbivorous Insects on Birch, Betula pubescens , 1985 .

[70]  M. Hunter,et al.  Evidence of incidental nest predation and its effects on nests of threatened grassland birds , 1992 .

[71]  Michael P. Hassell,et al.  GENERALIST AND SPECIALIST NATURAL ENEMIES IN INSECT PREDATOR-PREY INTERACTIONS , 1986 .

[72]  The snake that ate Guam , 1987 .

[73]  Robert D. Holt,et al.  Optimal Foraging and the Form of the Predator Isocline , 1983, The American Naturalist.

[74]  R. Copeland,et al.  Interspecific Competition, Parasitism, and Predation Affect Development of Aedes hendersoni and A. triseriatus (Diptera: Culicidae) in Artificial Treeholes , 1992 .

[75]  Norihiko Adachi,et al.  Existence and bifurcation of stable equilibrium in two-prey, one-predator communities , 1983 .

[76]  JoAnn White Resource Partitioning by Ovipositing Cicadas , 1980, The American Naturalist.

[77]  M. Westoby,et al.  Parasite-Mediated Competition: Some Predictions and Tests , 1988, The American Naturalist.

[78]  R. Vance,et al.  Predation and Resource Partitioning in One Predator -- Two Prey Model Communities , 1978, The American Naturalist.

[79]  J. Lawton,et al.  Switching in invertebrate predators , 1974 .

[80]  W. J. Freeland Parasites and the Coexistence of Animal Host Species , 1983, The American Naturalist.

[81]  J. Lawton,et al.  Bracken, ants and extrafloral nectaries. II: The effect of ants on the insect herbivores of bracken , 1984 .

[82]  S. Mori,et al.  Ant-plant interactions. , 1991 .

[83]  J. Lawton,et al.  On feeding on more than one trophic level , 1978, Nature.

[84]  David S. Wilcove,et al.  Nest Predation in Forest Tracts and the Decline of Migratory Songbirds , 1985 .

[85]  L. Keith,et al.  Demography of sympatric arctic and snowshoe hare populations: an experimental assessment of interspecific competition , 1989 .

[86]  Peter A. Abrams,et al.  The Fallacies of "Ratio‐Dependent" Predation , 1994 .

[87]  A. Abrams Indirect effects arising from optimal foraging , 1993 .

[88]  W. Resetarits ECOLOGICAL INTERACTIONS AMONG PREDATORS IN EXPERIMENTAL STREAM COMMUNITIES , 1991 .

[89]  M. Williamson An Elementary Theory of Interspecific Competition , 1957, Nature.

[90]  B. Menge,et al.  Species diversity : prey refuges modify the interactive effects of predation and competition , 1991 .

[91]  The interpretation of tests for ratio-dependence , 1992 .

[92]  G. Polis,et al.  THE ECOLOGY AND EVOLUTION OF INTRAGUILD PREDATION: Potential Competitors That Eat Each Other , 1989 .

[93]  R. Macarthur Mathematical Ecology and Its Place among the Sciences. (Book Reviews: Geographical Ecology. Patterns in the Distribution of Species) , 1974 .

[94]  S. Baillie,et al.  Magpie Pica pica and Songbird Populations. Retrospective Investigation of Trends in Population Density and Breeding Success , 1991 .

[95]  D. Doak,et al.  The Keystone-Species Concept in Ecology and ConservationManagement and policy must explicitly consider the complexity of interactions in natural systems , 1993 .

[96]  Peter Kareiva,et al.  5. Renewing the Dialogue between Theory and Experiments in Population Ecology , 1989 .

[97]  Ilkka Hanski,et al.  Specialist predators, generalist predators, and the microtine rodent cycle. , 1991 .

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

[99]  J. J. Gilbert,et al.  The susceptiblity of Keratella cochlearis to interference from small cladocerans , 1989 .

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

[101]  Andrew Sih,et al.  Predation: direct and indirect impacts on aquatic communities , 1988 .

[102]  S. Diehl Relative consumer sizes and the strengths of direct and indirect interactions in omnivorous feeding relationships , 1993 .

[103]  J. Lawton,et al.  HABITAT AND THE DISTRIBUTION OF WATER VOLES: WHY ARE THERE GAPS IN A SPECIES' RANGE? , 1991 .

[104]  J. Lawton,et al.  Bracken, Ants and Extrafloral Nectaries. I. the Components of the System , 1984 .

[105]  C. Elton The use of cats in farm rat control , 1953 .

[106]  M. J. Way,et al.  Role of Ants in Pest Management , 1992 .

[107]  P. S. Lake,et al.  Red crabs in rain forest, Christmas Island : Biotic resistance to invasion by an exotic snail , 1991 .

[108]  A. Watt A COMPARISON OF GRAZED AND UNGRAZED GRASSLAND A IN EAST ANGLIAN BRECKLAND , 1981 .

[109]  O. Schmitz,et al.  PARASITE-MEDIATED COMPETITION IN DEER AND MOOSE: HOW STRONG IS THE EFFECT OF MENINGEAL WORM ON MOOSE? , 1994 .

[110]  Burt P. Kotler,et al.  Short-Term Apparent Competition , 1987, The American Naturalist.

[111]  S. Wratten,et al.  Creation of island' habitats in farmland to manipulate populations of beneficial arthropods : predator densities and species composition , 1991 .

[112]  J. Fauth,et al.  Interactions Between the Salamander Siren Intermedia and the Keystone Predator Notophthalmus Viridescens , 1991 .

[113]  J. Wootton,et al.  The Nature and Consequences of Indirect Effects in Ecological Communities , 1994 .

[114]  Mark Westoby,et al.  PARASITE MEDIATION IN ECOLOGICAL INTERACTIONS , 1986 .

[115]  N. Knowlton Thresholds and Multiple Stable States in Coral Reef Community Dynamics , 1992 .

[116]  E. Werner Individual Behavior and Higher-Order Species Interactions , 1992, The American Naturalist.

[117]  S. Erlinge Predation and noncyclicity in a microtine population in southern Sweden , 1987 .

[118]  E. Dunn Predation by Weasels (Mustela nivalis) on Breeding Tits (Parus Spp.) in Relation to the Density of Tits and Rodents , 1977 .

[119]  A. Watt FURTHER OBSERVATIONS ON THE EFFECTS OF EXCLUDING RABBITS FROM GRASSLAND A IN EAST ANGLIAN BRECKLAND: THE PATTERN OF CHANGE AND FACTORS AFFECTING IT (1936-73) , 1981 .

[120]  R. Arditi,et al.  Functional responses and heterogeneities: an experimental test with cladocerans , 1991 .

[121]  A. Sinclair,et al.  Predation models for primary and secondary prey species , 1995 .

[122]  M. L. Goff,et al.  THE EPIZOOTIOLOGY AND ECOLOGICAL SIGNIFICANCE OF MALARIA IN HAWAIIAN LAND BIRDS , 1986 .

[123]  A. Sih,et al.  Experimental studies on behaviorally mediated, indirect interactions through a shared predator , 1990 .

[124]  J. Estes Top-Level Carnivores and Ecosystem Effects: Questions and Approaches , 1995 .

[125]  M. Hassell,et al.  Predation in multi-prey communities. , 1976, Journal of theoretical biology.

[126]  L. Oksanen,et al.  Exploitation Ecosystems in Gradients of Primary Productivity , 1981, The American Naturalist.