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Entomologia Experimentalis Et Applicata 150: 217–225, 2014 217 218 Murphy Et Al DOI: 10.1111/eea.12155 Host ontogeny determines parasitoid use of a forest caterpillar Shannon M. Murphy1*, Teresa M. Stoepler2§, Kylee Grenis1 & John T. Lill2 1Department of Biological Sciences, University of Denver, Denver, CO, USA, and 2Department of Biological Sciences, George Washington University, Washington, DC, USA Accepted: 5 November 2013 Key words: complementary predation, niche partitioning, ontogenetic niche, size-structured parasitism, trophic interaction, Euclea delphinii,Limacodidae,Lepidoptera,Hymenoptera,Diptera Abstract For most organisms, patterns of natural enemy-mediated mortality change over the course of devel- opment. Shifts in enemy pressure are particularly relevant for organisms that exhibit exponential growth during development, such as juvenile insects that increase their mass by several orders of magnitude. As one of the dominant groups of insect herbivores in most terrestrial plant communi- ties, larval lepidopterans (caterpillars) are host to a diverse array of parasitoids. Previous research has described how the frequency of herbivore parasitism varies among host plants or habitats, but much less is known about how parasitism pressure changes during host development. To test whether the two major parasitoid taxa, wasps and flies, differentially attack shared hosts based on host develop- mental stage, we simultaneously exposed early- and late-instar Euclea delphinii Boisduval (Lepido- ptera: Limacodidae) caterpillars to parasitism in the field. We found strong evidence that parasitoids partition hosts by size; adult female wasps preferentially parasitized small caterpillars, whereas adult female flies preferred to attack large caterpillars. Our results demonstrate that host ontogeny is a major determinant of parasitoid host selection. Documenting how shifts in enemy pressure vary with development is important to understanding both the population biology and evolutionary ecology of prey species and their enemies. The ontogeny of both the consumer and its resource Introduction organisms (e.g., prey for predators or hosts for parasites or A central question in evolutionary ecology is how consum- herbivores) is predicted to play a central but often over- ers partition shared resources (Schoener, 1974; Amarasek- looked role in mediating patterns of resource use, compe- are, 2000; de Roos et al., 2008). Potential axes of resource tition, and the risk of natural enemy-mediated mortality partitioning include time (Adams & Thibault, 2006), space (Werner & Gilliam, 1984; Relyea, 2005). Many consumers (Fonseca & Benson, 2003), differences in behavior show marked shifts in resource use during development (Nagamitsu & Inoue, 1997), and complementary tradeoffs (Werner & Gilliam, 1984). Such ontogenetic dietary shifts in key life-history traits or morphologies related to have been observed in diverse animal taxa, including resource use (Toft, 1985; Brown, 1989; Bonsall et al., 2002; insects (Klecka & Boukal, 2012), marine invertebrates Grant & Grant, 2006). Although often difficult to disen- (Graham & Kroutil, 2001), frogs (Trakimas et al., 2011), tangle empirically, the specific mechanisms of partitioning fish (Davis et al., 2011), and sharks (Lowe et al., 1996). A have important implications for how ecological communi- related but less studied phenomenon occurs when con- ties are structured (Bonsall et al., 2002, 2004; Finke & Sny- sumers stratify their consumption by the ontogenetic der, 2008). stages of their resource organisms (complementary preda- tion; Miller et al., 2010). When confronted with prey or hosts exhibiting ontogenetic variation in their accessibility, *Correspondence: Shannon M. Murphy, 2101 E. Wesley Ave, Mudd quality, or defenses, even fully developed consumers show Hall 309, Department of Biological Sciences, University of Denver, strong preferences for particular stage(s) of prey/host spe- Denver, CO 80208, USA. E-mail: [email protected] cies generally considered to be a part of their diet (Werner § Present address: Alson H. Smith Jr. Agricultural Research and & Gilliam, 1984). Such size- or stage-specific selectivity Extension Center, Virginia Tech, Winchester, VA, USA can have important consequences for the evolutionary © 2014 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 150: 217–225, 2014 217 218 Murphy et al. ecology of resource organisms, which are subject to vary- than that of the host(s). Experimental investigations of ing competitor and natural enemy communities over the how the parasitoid ‘pressure’ exerted by entire assemblages course of their ontogeny. For example, ontogenetic color of parasitoids changes over host ontogeny are needed to change in a variety of animals (Booth, 1990) has been help interpret natural patterns of ontogenetic shifts in par- hypothesized to result from stage- and/or size-specific dif- ticular morphologies, physiologies, or behaviors hypothe- ferences in predation pressure. sized to be linked to natural enemy avoidance (Relyea, Relative body size is a primary determinant of resource/ 2005; Grant, 2007; Frankfater et al., 2009). consumer relationships (Miller & Rudolf, 2011). Funda- Through collection and rearing of 11 species of co- mental changes in physiology, behavior, and morphology occurring slug caterpillars (Limacodidae: Lepidoptera), during growth and development alter the quality of Stoepler et al. (2011) recently found support for the resource organisms for consumers (Werner & Gilliam, hypothesis that the two dominant parasitoid taxa, wasps, 1984; Roger et al., 2001; Wilder et al., 2010). For example, and flies, partition their shared hosts based on caterpillar ontogeny affects resource allocation to growth and defense size (a proxy for developmental stage) in the field. Specifi- in both plants (Boege & Marquis, 2005; Quintero & Bow- cally, across a range of shared host species, wasp parasi- ers, 2012) and animals (Dudycha & Lynch, 2005; Boggs, toids were predominantly reared from small caterpillars 2009). Overall natural enemy-mediated mortality risk may collected from the field as early instars, whereas fly parasi- decrease as resource organisms grow and develop if the toids were reared most commonly from larger caterpillars primary consumers are gape-limited (Urban, 2007) or pre- collected as late instars. However, because this study com- fer smaller prey (Roger et al., 2001) or may increase if con- bined data from several limacodid caterpillar species, sam- sumers prefer larger prey or only recognize larger prey as pling dates, and seasons, the range of host sizes potential food items (Li & Jackson, 1996; Quinn & Kinni- simultaneously available to the local parasitoid commu- son, 1999; Westerbom et al., 2006). Alternatively, overall nity was uncontrolled, leaving unclear whether parasitism risk of natural enemy-mediated mortality may remain rel- records accurately reflect the true host preferences of these atively constant if the composition of consumer commu- parasitoids. nities turns over during the growth and development of Here, we report the results of a series of manipulative the resource organism (Miller et al., 2010; Schellekens experiments designed to test the hypothesis that natural et al., 2010). Patterns of such ontogenetic succession enemy taxa differ in their attack rates and/or consumption (Fonseca & Benson, 2003) are perhaps best documented in of a shared resource: caterpillars of the spiny oak slug [Eu- the plant-herbivore literature, where herbivorous insect clea delphinii Boisduval (Lepidoptera: Limacodidae)]. By communities often shift with the ontogeny of their host simultaneously exposing small and large E. delphinii cater- plants (Le Corff & Marquis, 1999; Basset, 2001; Thomas pillars (Figure 1) to natural enemies on a small subset of et al., 2010). Although there have been several recent reviews and models exploring the role of ontogeny in mediating interspecific interactions (e.g., Boege & Marquis, 2006; Barton & Koricheva, 2010; Thomas et al., 2010; Miller & Rudolf, 2011), there is still a clear need for more empirical investigations, particularly for host-para- site and host-parasitoid systems. Parasitoids are a dominant component of the natural enemy community for many herbivorous insects (Godfray, 1994) and often specialize on hosts of a particu- lar developmental stage (Waage & Hassell, 1982), resulting in size-structured host use by parasitoid species. Although size- and stage-specific parasitism has been noted for particular species (often insect pests; Neveu et al., 2000; Hegazi & Khafagi, 2005; Chong & Oetting, 2006; Rehman & Powell, 2010), generalizations regarding differential par- asitoid host use, and the mechanism(s) underlying it, Figure 1 A pair of small (early instar) and large (late instar) remain elusive. In addition, most of these agriculturally Euclea delphinii caterpillars depicted prior to being exposed to based studies approach the question from the perspective parasitoid attack in the field. Note the difference in color of the parasitoid (i.e., determining what range of host patterning and physical armature (stinging spines) between the sizes/stages a particular parasitoid species targets) rather instars. Size-specific parasitism 219 host plants, we test our hypothesis that ontogeny mediates shrubs throughout its range (Epstein, 1988; Wagner, 2005; natural enemy attack by the resident limacodid parasitoid Lill, 2008; Murphy et al., 2011). community. Euclea delphinii caterpillars are used as hosts by a community of parasitoid species that are specific to Field
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