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Abstract Effects of Landscape Structure On ABSTRACT EFFECTS OF LANDSCAPE STRUCTURE ON GENERALIST AND SPECIALIST INSECT HERBIVORES by Bradley John Schroeder The density responses of insect herbivores to shifts in habitat area may depend on the degree of host-plant specialization and the composition of the matrix. I conducted a study in an experimental field comprised of plots of red clover (Trifolium pratense) that differed in size, fragmentation, and surrounding matrix. Densities of three insect herbivores were measured within the plots during two field seasons. All three species showed positive density-area relationships. The two generalist species, the meadow spittlebug (Philaenus spumarius) and the Agallian leafhopper (Agallia constricta), attained higher densities in red clover surrounded by orchard grass (Dactylis glomerata). The specialist species, the clover leafhopper (Ceratagallia agricola), attained higher densities in red clover surrounded by bare ground. The results of this study suggest that both patch area and matrix habitat strongly affect the densities of insect herbivores, and species responses largely depend upon host-plant specialization and the availability of secondary host plants. EFFECTS OF LANDSCAPE STRUCTURE ON GENERALIST AND SPECIALIST INSECT HERBIVORES A Thesis Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Master of Zoology by Bradley John Schroeder Miami University Oxford, Ohio 2007 Advisor_____________________ Dr. Thomas O. Crist Reader______________________ Dr. Martin Henry H. Stevens TABLE OF CONTENTS Acknowledgements iii Effects of Landscape Structure on Generalist and Specialist Insect Herbivores 1 Introduction 1 Methods 4 Results 7 Discussion 8 Tables and Figures 18 ii ACKNOWLEDGEMENTS I would like to thank my advisor, Dr. Tom Crist, for all of his valuable help and advice throughout the course of this project. I would also like to thank my committee members, Dr. Hank Stevens and Dr. Ann Rypstra for their additional advice and suggestions. I would like to thank Rodney Kolb and the staff at the Ecology Research Center for their valuable time and assistance in the field. I would also like to thank Kyle Haynes, Dave Stasek, Laura Douglas and Sam Evans for their hold both out in the field as well as in the lab. This research was funded by the Miami University Zoology Summer Field Workshop. iii Introduction Understanding species responses to spatial attributes of habitat within the landscape is fundamental to both ecological theory (With and Crist 1995, Ritchie and Olff 1999) and agroecosystem ecology (Tscharntke et al. 2005). Intensive agricultural practices simplify the landscape into large crop monocultures surrounded by semi-natural and natural habitats, causing increases in the abundance of crop pests and a reduction in native species abundances (Robinson and Sutherland 2002). Changes in landscape structure – the size, composition, and spatial arrangement of habitats – due to agricultural development may result in elevated densities of insect herbivores and the loss of natural enemies. Together, these shifts in herbivore or natural-enemy abundance cause reductions in plant biomass and agricultural production (Tscharntke et al. 2005). Generalist predators and non-crop feeding insects often prefer or require natural and semi-natural areas to undergo life processes, such as overwintering and oviposition (Landis 2000). Many pest insects, however, may complete their entire life cycle within crop fields, and intensive agriculture creates greater areas of habitat for these pest species. Landscape studies of arthropods in agricultural systems have focused on the spillover of generalists, particularly generalist predators, from non-crop into crop areas to understand their roles in the control of pest outbreaks (see Kreuss and Tscharntke 1994, Bianchi et al. 2006, Rand et al. 2006). Few studies have compared the responses of insect herbivores differing in habitat or host-plant specialization to habitat area and spatial arrangement (but see Jonsen and Fahrig 1997). Studies of density-area relationships show an increase in population density in larger habitats, a trend that is particularly strong in insect populations (Connor et al. 2000). The resource-concentration hypothesis, proposed by Root (1973) predicts that specialist herbivores in large, monospecific patches of host plants will attain greater relative densities in these simple environments compared to smaller areas with fewer host plants. One primary mechanism for this pattern is based on insect movement, whereby individuals are more likely to find and remain in large stands of host plants, leading to increased densities in larger areas of habitat (Root 1973). Specialist herbivores with life requirements that can be met within the host plants will remain the longest, while those with broader ranges and life requirements will drift out of the patches more quickly. 1 A number of studies have supported positive density-area relationships (e.g. Bach 1984, Kareiva 1985, Kindvall and Ahlén 1992, Matter 1997), while other studies found no relationship and or even negative relationships between insect herbivore densities and habitat area (Bach 1988, Grez & Gonzalez 1995). Hambäck and Englund (2005) have suggested that the inclusion of additional elements of patch geometry (e.g., edge:area ratio) may enhance the predictive value of the resource concentration hypothesis. For species that are visual foragers, for example, immigrants are expected to use patch diameter to locate patches while emigrants use the patch edge, so that population density increases as perimeter-to-area ratio increases, resulting in negative density-area relationships. Alternatively, for species arriving from the air, area-dependent immigration and perimeter-dependent emigration will result in positive density-area relationships. These predictions were supported by Hambäck et al. (in press), who found that moth species, which search for host plants via olfactory information, generally showed positive density-area relationships, while butterflies, which are visual foragers, often showed negative density-area relationships. A reduction in suitable habitat area usually occurs simultaneously with habitat isolation or fragmentation (Carlson & Hartman 2001, Fuller 2001, Summerville and Crist 2001, Fahrig 2003). Therefore, it is difficult to distinguish the effects of habitat loss and fragmentation from one another, and only recently have experiments manipulated fragmentation and area independently (Fahrig 2003). The separation of a given area into various smaller fragments will result in higher edge:area ratios. Species in areas with more edge per given area of habitat will be more likely to leave the habitat and enter the matrix, leading to higher emigration rates and lower population densities within the individual fragments (Fahrig 2002). Apart from habitat area and fragmentation, the type of vegetation within the matrix surrounding habitat patches can have a significant influence on insect herbivore density. Specialist and generalist herbivores may differ in their response to the matrix, because generalists are capable of using complementary resources not available to specialists (With and Crist 1995, Golden and Crist 1999, Haynes et al. 2007). Whereas monophagous insects may have a highly aggregated spatial distribution because they are distributed among patches of their host plant, generalists will be able to use secondary 2 host plants beyond the habitat patches, thus promoting cross-habitat foraging (Shmida and Wilson 1985, Rand et al. 2006). Generalist herbivores may use both the focal habitat as well as the matrix, and become distributed throughout the landscape as though it were a habitat continuum (Tscharntke et al. 2002). The presence of secondary hosts may also encourage these generalist herbivores to remain in habitat patches longer than those that are surrounded by a non-host matrix, leading to higher densities within these areas. Polyculture cropping systems are ideal for examining the effects of plant diversity and the spatial configuration of land-use practices on insect herbivores. Forage crops are often planted as mixtures, such as red clover (Trifolium pratense) with one or more grasses. It is known by practitioners that red clover attracts large numbers of insect herbivores that eventually lead to its decline. In this study, I examined the roles of habitat area, spatial arrangement, and complementary host plants (i.e. grasses) in determining herbivore densities. The dominant herbivores in my study system were three species of Cicadomorpha: the leafhoppers Agallia constricta Van Duzee and Ceratagallia agricola Hamilton, and the meadow spittlebug Philaenus spumarius (L.). Whereas C. agricola feeds principally on red clover (Hamilton 1998), P. spumarius and A. constricta are more generalized feeders. A. constricta is known to feed upon many herbaceous plants (Osborn 1928). P. spumarius is known to feed preferentially on legumes such as red clover, but it also feeds on a number of grasses and other plant species (Thompson 1994, Weaver and King 1954) and may also be considered a habitat generalist. The objective of this study was to determine how generalist and specialist insect herbivores responded to variations in landscape structure. To test this, I quantified the densities of these three insect herbivores in plots comprised of red clover habitat that differ independently in area (large vs. small), level of fragmentation (continuous vs. fragmented),
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