Local variation in plant quality influences large‐scale population dynamics

Spatial variation in ecological systems can arise both as a consequence of variation in the quality and availability of resources and as an emergent property of spatially structured interactions. We used a spatially explicit model to simulate populations of herbivore hosts and their parasitoids in landscapes with different levels of variance in plant patch quality and different spatial arrangements of high- and low-quality plant patches. We found that even small variation in patch quality at a fine spatial scale decreased overall herbivore populations, as parasitoid populations on low-quality plant patches were subsidized by those from high-quality neighbors. On landscapes with large, homogeneous regions of high- and low-quality plant patches, herbivore populations increased with variation in patch quality. Overall, our results demonstrate that local variation in resource quality profoundly influences global population dynamics. In particular, fine-scale variation in plant patch quality enhanced biological control of herbivores by parasitoids, suggesting that adding back plant genetic variation into perennial production systems may enhance the biological control of herbivores by their natural enemies.

[1]  M. Bickerton.  Intercropping for conservation biological control of European corn borer Ostrinia nubilalis Hübner (lepidoptera: crambidae) in bell peppers , 2011 .

[2]  C. Huffaker.  Experimental studies on predation : dispersion factors and predator-prey oscillations , 1958 .

[3]  W. Murdoch,et al.  Host-parasitoid spatial dynamics in heterogeneous landscapes , 2007 .

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

[5]  D. Levey,et al.  Habitat patch shape, not corridors, determines herbivory and fruit production of an annual plant. , 2012, Ecology.

[6]  J. D. Reeve.  Environmental Variability, Migration, and Persistence in Host-Parasitoid Systems , 1988, American Naturalist.

[7]  Pejman Rohani,et al.  Host―parasitoid metapopulations : the consequences of parasitoid aggregation on spatial dynamics and searching efficiency , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  M. Gyllenberg,et al.  Exploitation ecosystems in heterogeneous habitat complexes II: Impact of small-scale heterogeneity on predator-prey dynamics , 1992, Evolutionary Ecology.

[9]  Catherine E. Batch,et al.  Plant Spatial Pattern and Herbivore Population Dynamics: Plant Factors Affecting the Movement Patterns of a Tropical Cucurbit Specialist (Acalymma Innubum) , 1984 .

[10]  D. Andow.  Vegetational Diversity and Arthropod Population Response , 1991 .

[11]  J. Roland,et al.  Insect parasitoid species respond to forest structure at different spatial scales , 1997, Nature.

[12]  R. Denno,et al.  INTRODUCTION: Variability: A Key to Understanding Plant–Herbivore Interactions , 1983 .

[13]  G. Ruxton,et al.  The consequences of stochasticity for self-organized spatial dynamics, persistence and coexistence in spatially extended host-parasitoid communities , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  M. Hebblewhite,et al.  Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. , 2009, Ecology.

[15]  T. Whitham,et al.  PLANT GENOTYPE AFFECTS LONG-TERM HERBIVORE POPULATION DYNAMICS AND EXTINCTION: CONSERVATION IMPLICATIONS , 2003 .

[16]  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.

[17]  Jon C. Allen,et al.  Mathematical Models of Species Interactions in Time and Space , 1975, The American Naturalist.

[18]  Tarja Oksanen,et al.  Exploitation ecosystems in heterogeneous habitat complexes , 1990, Evolutionary Ecology.

[19]  M. Hunter,et al.  Elevational Trends in Defense Chemistry, Vegetation, and Reproduction in Sanguinaria canadensis , 2001, Journal of Chemical Ecology.

[20]  Karin Johst,et al.  Metapopulation persistence in dynamic landscapes: the role of dispersal distance , 2002 .

[21]  W. Murdoch,et al.  Diversity and Pattern in Plants and Insects , 1972 .

[22]  J. Pajares,et al.  Geometrid outbreak waves travel across Europe. , 2013, The Journal of animal ecology.

[23]  R. May,et al.  Aggregation of Predators and Insect Parasites and its Effect on Stability , 1974 .

[24]  G. Ruxton,et al.  Dispersal-induced instabilities in host-parasitoid metapopulations. , 1999, Theoretical population biology.

[25]  James S. Clark,et al.  The relative influences of host plant genotype and yearly abiotic variability in determining herbivore abundance , 2011, Oecologia.

[26]  M. A. Foster,et al.  Modelling gypsy moth-virus-leaf chemistry interactions: implications of plant quality for pest and pathogen dynamics , 1992 .

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

[28]  VARIANCE AND SKEW OF THE DISTRIBUTION OF PLANT QUALITY INFLUENCE HERBIVORE POPULATION DYNAMICS , 2004 .

[29]  R. May,et al.  STABILITY IN INSECT HOST-PARASITE MODELS , 1973 .

[30]  M. Eubanks,et al.  Sequential radiation of unrelated organisms: the gall fly Eurosta solidaginis and the tumbling flower beetle Mordellistena convicta , 2003, Journal of evolutionary biology.

[31]  M. Hunter,et al.  Playing Chutes and Ladders: Heterogeneity and the Relative Roles of Bottom‐Up and Top‐Down Forces in Natural Communities , 1992, Ecology.

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

[33]  R. Holt,et al.  Impacts of temporal variation on apparent competition and coexistence in open ecosystems , 2003 .

[34]  J. Cronin,et al.  Host–parasitoid spatial ecology: a plea for a landscape-level synthesis , 2005, Proceedings of the Royal Society B: Biological Sciences.

[35]  S. Pennings,et al.  Latitudinal variation in plant–herbivore interactions in European salt marshes , 2007 .

[36]  D. Pimentel.  Species Diversity and Insect Population Outbreaks , 1961 .

[37]  Robert M. May,et al.  The spatial dynamics of host-parasitoid systems , 1992 .

[38]  Chris D. Thomas,et al.  Effects of habitat patch size and isolation on dispersal by Hesperia comma butterflies : implications for metapopulation structure , 1996 .

[39]  Carsten Thies,et al.  Landscape structure and biological control in agroecosystems , 1999, Science.

[40]  S. Louda,et al.  Spillover of Agriculturally Subsidized Predators as a Potential Threat to Native Insect Herbivores in Fragmented Landscapes , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[41]  J. Cronin.  PATCH STRUCTURE, OVIPOSITION BEHAVIOR, AND THE DISTRIBUTION OF PARASITISM RISK , 2003 .

[42]  Michael P. Hassell,et al.  Aggregation and the Dynamics of Host-Parasitoid Systems: A Discrete-Generation Model with Within-Generation Redistribution , 1994, The American Naturalist.

[43]  Chris Cosner,et al.  The effects of spatial heterogeneity in population dynamics , 1991 .

[44]  Carsten Thies,et al.  Effects of landscape context on herbivory and parasitism at different spatial scales , 2003 .

[45]  J. Régnière,et al.  Spruce budworm impact, abundance and parasitism rate in a patchy landscape , 1998, Oecologia.

[46]  Jonathan Roughgarden,et al.  Population Dynamics in a Spatially Varying Environment: How Population Size "Tracks" Spatial Variation in Carrying Capacity , 1974, The American Naturalist.

[47]  N. Underwood.  Effect of genetic variance in plant quality on the population dynamics of a herbivorous insect. , 2009, The Journal of animal ecology.

[48]  C. Briggs,et al.  The effect of dispersal on the population dynamics of a gall‐forming midge and its parasitoids , 2000 .

[49]  M. Hunter.  Effects of plant quality on the population ecology of parasitoids , 2003 .

[50]  M. D. Loveless,et al.  ECOLOGICAL DETERMINANTS OF GENETIC STRUCTURE IN PLANT POPULATIONS , 1984 .

[51]  Bin Chen,et al.  Effect of intercropping pepper with sugarcane on populations of Liriomyza huidobrensis (Diptera: Agromyzidae) and its parasitoids , 2011 .

[52]  C. Bernstein,et al.  Patch choice from a distance and use of habitat information during foraging by the parasitoid Ibalia leucospoides , 2012 .

[53]  Michael P. Hassell,et al.  Spatial structure and chaos in insect population dynamics , 1991, Nature.

[54]  M. Hunter,et al.  Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids , 2005, Oecologia.

[55]  Andrew D. Taylor.  Studying metapopulation effects in predator-prey systems , 1991 .

[56]  R. B. Root.  Organization of a Plant-Arthropod Association in Simple and Diverse Habitats: The Fauna of Collards (Brassica Oleracea) , 1973 .

[57]  S. Hartley,et al.  Population-level variation in plant secondary chemistry, and the population biology of herbivores , 2005, CHEMOECOLOGY.

[58]  Andrew M. Liebhold,et al.  Waves of Larch Budmoth Outbreaks in the European Alps , 2002, Science.

[59]  Thomas F. Hansen,et al.  Individual variation and population dynamics , 1994 .