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Chrysolina Quadrigemina) Onto Native St Spillover of a biological control agent (Chrysolina quadrigemina) onto native St. Johnswort (Hypericum punctatum) Jessica L. Tingle1, Susan C. Cook-Patton2 and Anurag A. Agrawal3 1 Department of Biology, University of California, Riverside, Riverside, CA, United States 2 Science & Technology Policy Fellow, American Association for the Advancement of Science, Washington, D.C., United States 3 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, United States ABSTRACT Biological control agents may have unintended effects on native biota, particularly species that are closely related to the target invader. Here, we explored how Chrysolina quadrigemina, a beetle introduced to control the invasive weed Hypericum perforatum, impacts native H. punctatum in Tompkins County, New York, USA. Using a suite of complementary field surveys and experimental manipulations, we examined beetle preference for native and exotic Hypericum species and whether beetle herbivory influences the spatial distribution of H. punctatum. We found that the introduced beetle readily consumes native H. punctatum in addition to its intended target, and that H. punctatum at our field sites generally occurs along forest edges despite higher performance of experimental plants in more open habitats. However, we found no evidence that the beetle limits H. punctatum to forest edge habitats. Subjects Ecology, Entomology, Plant Science Keywords Biological control, Hypericum, St. Johnswort, St. John's Wort, Chrysolina, Klamathweed beetle, Invasive, Herbivory Submitted 16 January 2016 INTRODUCTION Accepted 13 March 2016 Published 31 March 2016 Invasions by exotic species can negatively impact native communities through altered Corresponding author species interactions and ecosystem processes (Mack et al., 2000). One explanation for the Jessica L. Tingle, spread of invasive species is the enemy release hypothesis, which posits that invaders have [email protected] higher performance than natives do because they escape from specialist enemies like Academic editor herbivores or pathogens when they move to a new range (Keane & Crawley, 2002; Vilà, Karen Esler Maron & Marco, 2005; Agrawal et al., 2005). Thus, a logical way to combat invasive species Additional Information and Declarations can be found on is through biological control, the practice of releasing specialist enemies, typically from the page 13 original range of the invader, to control the spread of the exotic species (McFadyen, 1998; DOI 10.7717/peerj.1886 Van Driesche et al., 2010). Copyright Ideal biological control agents are those that specialize on the target invader and do 2016 Tingle et al. not spill over onto non-target, native hosts (Chalak et al., 2010). However, because the Distributed under traits mediating plant-herbivore interactions, such as plant chemical defenses, are often Creative Commons CC-BY 4.0 phylogenetically conserved (Futuyma & Agrawal, 2009), most herbivores readily utilize several closely related plants (Jaenike, 1990; Pearse & Altermatt, 2013). This tendency poses OPEN ACCESS How to cite this article Tingle et al. (2016), Spillover of a biological control agent (Chrysolina quadrigemina) onto native St. Johnswort (Hypericum punctatum). PeerJ 4:e1886; DOI 10.7717/peerj.1886 a challenge for the selection of biological control agents because specialist insects that are released to control invasive plant species may exploit closely related natives, particularly if those natives co-occur with the invasive plant (Louda et al., 2003). The exotic beetle Chrysolina quadrigemina has successfully controlled exotic St. Johnswort, Hypericum perforatum, in California (Van Driesche et al., 2010), but in the eastern United States, it may have unintended and negative effects on a congeneric and co-occurring native, H. punctatum. The exotic plant is a Eurasian species that became a pest after its introduction to North America (Bourke, 2000). The beetle was introduced in 1943 as an attempt to control the weed, and is a classic case of successful biological control (Huffaker, 1959; Van Driesche et al., 2010). In addition to directly consuming the plant, the beetle also acts as a vector for the pathenogenic fungus Colletotrichum gloeosporioides, which may additionally help to control the exotic H. perforatum (Morrison, Reekie & Jensen, 1998). Our study was motivated by an observation of C. quadrigemina feeding on the native H. punctatum in the field (Fig. 1). We formed three hypotheses. First, that C. quadrigemina readily consumes the native H. punctatum. Second, that C. quadrigemina negatively affects the abundance or natural distribution of H. punctatum. Third, that because the beetle prefers open, sunny areas (Fields, Arnason & Philogène, 1990; Van Driesche et al., 2010), the native Hypericum might face greater herbivory pressure in those locations and therefore be relegated to shaded areas. This phenomenon has been observed in California, where the beetle's preference for sunny environments resulted in a 99% reduction of the exotic H. perforatum in open areas, but not in shaded areas (Van Driesche et al., 2010). To test these hypotheses, we combined field surveys with experimental manipulations, including a feeding assay testing beetle preference for the two species of Hypericum, a survey of the natural distribution of Hypericum, an experiment testing the effect of distance from forest edge on plant size and beetle damage, and a 2 × 2 factorial field experiment testing the effects of sun and shade on beetle damage. Specifically, we asked (1) do beetles preferentially exploit the native or exotic Hypericum species, (2) is beetle herbivory concentrated in sunny areas, and (3) does beetle herbivory limit the distribution of H. punctatum and H. perforatum? METHODS Study organisms The genus Hypericum contains nearly 500 species spread throughout temperate parts of the world (Nürk & Blattner, 2010). This study focused on two species that co-occur in old-fields in central New York: the invasive H. perforatum and its native congener, H. punctatum. Both are perennials. H. perforatum is native to Europe, western Asia, and northern Africa, but arrived in the United States no later than the 17th century (Josselyn, 1672). One well- studied defensive chemical in Hypericum species is hypericin (Avato & Guglielmi, 2004; Smelcerovic et al., 2007), a compound that has increased toxicity in the presence of visible light (i.e., phototoxicity), with an action spectrum peak between 540 and 610 nm (Fields, Arnason & Philogène, 1990). In addition to its effect on invertebrate herbivores, hypericin is also toxic for grazing livestock (Bourke, 2000), which prompted the introduction of Chrysolina quadrigemina as a biological control agent for H. perforatum in the 1940s Tingle et al. (2016), PeerJ, DOI 10.7717/peerj.1886 2/17 Figure 1 Chyrsolina quadrigemina feeding on native Hypericum punctatum (photo: SCP). (Andres, 1985). The native range of C. quadrigemina overlaps with that of H. perforatum in the Mediterranean region, where it consumes only H. perforatum and H. tomentosum and oviposits on H. perforatum (Wilson, 1943). Despite ingestion of phototoxic hypericin, adult Chrysolina quadrigemina expose themselves to sunlight by perching high up on Hypericum stems during the day (Fields, Arnason & Philogène, 1990). In laboratory experiments, however, the beetles have demonstrated negative phototropism (Wilson, 1943). Location We conducted our field experiments in former agricultural fields belonging to Cornell University, Ithaca NY. To determine the natural distribution of Hypericum, we collected data in 5 fields (Durland Bird Sanctuary, 42◦2601900N, 76◦2305400W; Freese Road, 42◦280200N, 76◦2603800W; Neimi Road West, 42◦300100N, 76◦260700W; Neimi Road East, 42◦300100N, 76◦260300W; and Whipple North, 42◦29032:1300N, 76◦25040:8800W). We established the transect experiment and sun/shade experiment in fields surrounding an experimental field station (Dryden NY, 42◦2705100N, 76◦2604000W). Feeding assays To determine whether beetles preferred the native or exotic Hypericum species, we conducted feeding assays. In July 2011, we collected adult beetles from wild Hypericum plants, stored them in containers with a damp paper towel, and starved them for 24 h prior Tingle et al. (2016), PeerJ, DOI 10.7717/peerj.1886 3/17 to feeding trials. We tracked whether the beetles were collected on H. punctatum (N D 17) or H. perforatum (N D 8). We collected as many beetles as possible for the feeding trials before they began their late-summer period of inactivity, and although we attempted to collect equal numbers of beetles from each plant species on three days over the course of one week, we did not manage to find as many beetles on H. perforatum during the second and third days of collection. For each trial (N D 25), we paired undamaged stems of equal length from greenhouse grown Hypericum plants, placing them in a water tube and inserting these into a soil-filled pot, 10 cm in diameter. We placed one beetle on the soil surface between the two stems, encased the pots in mesh bags for 2.5 h, and recorded which plant, if any, the beetle chose to eat by the end of the trial. All trials occurred within an outdoor shade tent. To determine whether the beetles preferred the native or exotic Hypericum, we analyzed feeding preference with a χ-square test. We excluded trials in which the beetles made no choice (N D 11), using only data in which the beetle fed on one of the two plants offered (N D 14). Beetles never
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