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What Determines Host Range in Parasitoids? an Analysis of a Tachinid Parasitoid Community

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What Determines Host Range in Parasitoids? an Analysis of a Tachinid Parasitoid Community Oecologia (2003) 135:629–638 DOI 10.1007/s00442-003-1235-2 COMMUNITY ECOLOGY John O. Stireman · Michael S. Singer What determines host range in parasitoids? An analysis of a tachinid parasitoid community Received: 21 November 2002 / Accepted: 25 February 2003 / Published online: 9 April 2003 Springer-Verlag 2003 Abstract Despite the vast diversity of parasitic insects study suggest that ecological factors are important and their importance in natural and agricultural commu- determinants of host use in these parasitoids and although nities, our knowledge of what determines their patterns of phylogenetic history may influence the range of hosts association with hosts remains sparse. Unlike most used, its power to explain the ecological or taxonomic parasites that tend to be specialized, parasitoid flies in character of hosts used appears limited. the family Tachinidae exhibit a broad spectrum of host- specificity, with many species attacking a wide range of Keywords Specialization · Polyphagy · Ecological hosts. This variability in host-specificity makes them a determinant · Lepidoptera · Tachinidae useful model for examining the ecological and historical factors that determine host associations. We analyzed data collected from a 5-year rearing program of Lepidoptera in Introduction southern Arizona to investigate the factors that influence tachinid-host associations. After controlling for a strong Patterns of host use in parasitic insects have been the effect of sample size, a significant portion of the focus of an enormous amount of research by behavioral remaining variance in host range was explained by ecologists, evolutionary biologists, and community ecol- differences among phylogenetic groups of tachinids and/ ogists (Price 1980; Futuyma and Moreno 1988; Jaenicke or their correlated reproductive strategies. Relatively 1990; Kawecki 1998). Much of this interest has centered specialized tachinids tended to be associated with around the goals of understanding how the diverse monophagous or narrowly oligophagous hosts and at- communities of these insects are maintained in ecological tacked them at relatively high frequencies, a pattern we time and space and how they have diversified over suggest is related to host location efficiency. Cluster evolutionary time (e.g., Ehrlich and Raven 1964; Laban- analysis indicated that host abundance, gregariousness, deira et al. 1994). Although we have made great strides in food-plant type, and morphology are all important identifying and understanding ecological patterns of food- determinants of tachinid host use. Little concordance plant associations in phytophagous insects (Strong et al. was found between how tachinid species cluster accord- 1984; Singer and Parmesan 1993; Novotny et al. 2002) ing to characteristics of their hosts and their estimated and their evolutionary development (Farrell and Mitter phylogenetic relationships. Together, the results of this 1994; Futuyma and Mitter 1996; Nosil 2002), the patterns of host range of another diverse and ecologically impor- tant guild of parasitic insects, the parasitoids, remain J. O. Stireman III ()) much less well known. The number of studies exploring Department of Ecology and Evolutionary Biology, University of Arizona, the evolutionary and ecological determinants of host use Tucson, AZ, 85721, USA in parasitoids is growing (e.g., see Hawkins 1994; e-mail: [email protected] Hawkins and Sheehan 1994), but for most groups we have little idea of the relative importance of ecological M. S. Singer habitat, processes of host location, physiological interac- Interdisciplinary Program in Insect Science, tions with hosts, host defenses, or phylogenetic history in University of Arizona, Tucson, AZ, 85721, USA influencing parasitoid host ranges. Although determining parasitoid host ranges is pla- Present address: gued with difficulties (Shaw 1994), it appears that most J. O. Stireman III, Department of Botany, parasitoids attack only a narrow range of hosts (Herting Iowa State University, 1971–1982; Memmott et al. 2000). The two principal Ames, IA, 50011, USA 630 factors that limit host ranges in parasitoids are thought to 3. Which ecological, behavioral, and physical character- be host taxonomy and host ecology (Askew and Shaw istics of hosts are most important in determining the 1986). The effect of host taxonomic affinity is believed to local patterns of host use? be related primarily to physiological (and morphological) defenses of hosts that may require specific adaptations of By exploring these questions we hope to expand our their parasitoids (Vinson and Iwantsch 1980; Godfray understanding of the determinants of host range in the 1994; Kraaijeveld et. al 1998). The proposal that phys- relatively poorly known tachinid parasitoids, which may iological defenses limit parasitoid host ranges is analo- in turn provide insight into the forces that shape host gous to arguments concerning the importance of associations in other parasitic insects. secondary chemicals in the specialization of phytopha- gous insects on food-plants (Dethier 1954; Ehrlich and Raven 1964). Ecological characteristics that influence Tachinid biology host use by parasitoids include the plants on which a host feeds (Vinson 1981; Askew 1994), the microhabitat in Female tachinids possess a wide variety of oviposition which it feeds (Weseloh 1993), and the host’s phenology strategies and morphological specializations involved in (Clausen 1940; Askew 1961). host attack that may influence the range of hosts they Flies in the family Tachinidae are unusual among attack. Some genera deposit unincubated eggs on the host parasitoids in the remarkably broad host ranges of many that must develop for several days before hatching species despite their endoparasitic lifestyle (Eggleton and (Clausen 1940). However, most species that deposit eggs Gaston 1992; Belshaw 1994). Tachinids appear to avoid on hosts possess uterine incubation such that the eggs physiological defenses of hosts by forming respiratory hatch quickly after oviposition. The necessity of expelling funnels through which they maintain contact with outside these developing offspring may lower thresholds for air (Clausen 1940; Eggleton and Gaston 1992), and this selecting hosts and lead to broad host ranges. Approxi- trait appears to be associated with relatively broad host mately 40% of species either deposit larvae on substrates ranges (Belshaw 1994). This may obviate the need for frequented by hosts (e.g., leaves of food plants) or deposit biochemical adaptation to particular host species and “microtype” eggs upon the food plant of the host that are permit polyphagy (Belshaw 1994). Tachinids may also be inadvertently ingested by the host (O’Hara 1985; Wood pre-adapted to tolerate defensive chemicals contained in 1987). In either case the adult fly does not contact the host hosts due to adaptations of their ancestors to other toxic and such “indirect” oviposition strategies may result in a environments (e.g., carrion; Gauld et al. 1992). large number of offspring dying before they encounter If tachinid host-use is not generally limited by host hosts. For this reason, these taxa may be more likely to physiological defenses, and the range of potential hosts attack hosts that feed gregariously where encounter that can support development is quite large, what then probabilities may be much higher. They may also be determines which hosts are actually used by a particular expected to possess broader host ranges due to opportu- species? Despite their relatively broad host ranges, most nistic attack of any host encountered due to the low tachinids use only a tiny fraction of potentially available probability of such encounters (Belshaw 1994). These hosts (Stireman and Singer 2003). The difference between hypotheses are also evaluated in this study. the potential host ranges and the much smaller realized host ranges in phytophagous insects and other parasitic insects has led several authors to suggest that ecological Materials and methods attributes of hosts may strongly influence host range for many species and the process of host location may play a Sampling methods significant role in determining patterns of host use Larval macrolepidoptera were sampled from 1996 to 2000 in (Bernays and Graham 1988; Feener and Brown 1997; southeastern Arizona within an area of approximately 9,000 km2. Janz and Nylin 1997; Lill et al. 2002; Perlman and Sampling was generally restricted to mesquite-oak savannas as well Jaenicke, in press). as associated riparian areas at elevations between ca. 1,000 and In this study the determinants of tachinid-host associ- 1,600 m. Sampling was conducted by walking haphazardly through the appropriate habitats and visually inspecting herbs, shrubs, and ations are explored using data from a 5-year rearing trees up to a height of approximately 3 m. Ultimate and penultimate program of Lepidoptera in southeastern Arizona. These instar caterpillars were preferentially sampled to allow maximum data are used to address three primary questions: exposure to parasitoids in nature. Either all of the individual caterpillars observed (of the appropriate size/age classes), or at least 1. How does the oviposition strategy and taxonomic 20 individuals per species per sampling site were collected. If a particular species was abundant, it was sampled from a variety of affiliation of tachinid species influence the range of individual food-plants. hosts they attack (i.e., what are the historical and/or Caterpillars were
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