Community-Wide Impacts of Early Season Herbivory on Flower Visitors

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Community-Wide Impacts of Early Season Herbivory on Flower Visitors Ecological Entomology (2017), 42, 164–172 DOI: 10.1111/een.12372 Community-wide impacts of early season herbivory on flower visitors on tall goldenrod MITO IKEMOTO,1 TAKASHI Y. IDA,1,∗ SHUNSUKE UTSUMI2 and TAKAYUKI OHGUSHI1 1Center for Ecological Research, Kyoto University, Otsu, Japan and 2Field Science Center for Northern Biosphere, Hokkaido University Horokanai, Japan Abstract. 1. The flower visitor community consists not only of pollinators butalso of non-pollinators, such as florivores, thieves and predators that attack flower visitors. Although there is increasing evidence that early-season foliar herbivory influences pollinator visitation through changes in floral traits, few studies have explored indirect effects of foliar herbivory on community structure of the flower visitors. We examined how early-season foliar herbivory influences the flower visitor community established in late season. 2. We conducted an inoculation experiment using a lacebug (Corythucha marmorata), which is a predominantly herbivorous insect attacking leaves of tall goldenrod (Solidago altissima) in Japan. 3. Flower abundance significantly decreased when damaged by the lacebug. The numbers of pollinators, florivores and thieves were positively correlated with flower abundance, whereas predators were not. In response to flower abundance, florivores decreased on damaged plants. On the other hand, thieves increased on damaged plants, and pollinators and predators did not differ between damaged and undamaged plants. 4. When effects of flower abundance were excluded, foliar herbivory still influenced florivores negatively and thieves positively. This implies that factors besides flower abundance may have affected the numbers of florivores and thieves. 5. Community composition of flower visitors on damaged plants significantly differed from undamaged plants, although overall abundance, taxonomic richness and taxonomic evenness were unaffected by foliar herbivory in the early season. It is important to recognise that only evaluating species diversity and overall abundance may fail to detect the significant consequence of early-season herbivory on the flower visitor community. Key words. Community-wide effect, flower visitor, functional group, herbivory, non-pollinator. Introduction visitors on plant reproduction vary from positive via pollina- tion to negative via florivory/predation (Strauss & Irwin, 2004). Ecological communities are composed of many species with Pollinators increase plant reproductive success by transferring different functions. Flowers are among the important resource pollen, while florivores and floral larcenist, including thieves and bases for shaping communities of arthropods with a wide range robbers, reduce plant reproductive success by directly consum- of functions, such as pollinators, florivores, thieves and preda- ing viable gametes (e.g. stamen and pistil) and indirectly lower- tors that attack flower visitors. The functions of these flower ing attractiveness to pollinators (e.g. display and reward; Irwin et al., 2001; McCall & Irwin, 2006). In addition, predators on Correspondence: Mito Ikemoto, Center for Ecological Research, flowers often decrease plant fitness through interfering withpol- Kyoto University, 509-3-2, Hirano, Otsu, Shiga 520–2113, Japan. linator visitations (Muñoz & Arroyo, 2004; Goncalves-Souza E-mail: [email protected] et al., 2008). Although most of the studies exploring flower ∗Current address: Faculty of Science, Nara Women’s University, Nara 630–8506, Japan. visitor community focus on pollinators alone, non-pollinators 164 © 2016 The Royal Entomological Society Leaf herbivory alters flower visitor community 165 are very common on flowers (Castro et al., 2013; Zhang et al., Japan. It is an exotic insect from North America, and was first 2014). recorded in 2000 in Kobe, central Japan (Kato & Ohbayashi, Recent studies have shown that early-season herbivory on 2009). Corythucha marmorata can utilise several plant species, vegetative tissues affects temporally separated pollinator visi- including Asteraceae, Solanaceae and Convolvulaceae (Tsujino tations later in the season (Bronstein et al., 2007 for a review). et al., 2006). Both adults and nymphs pierce epidermis and feed Foliar herbivory in the early part of the season can decrease on mesophyll of S. altissima foliage, leading to changes in leaf flower number (Karban & Strauss, 1993; Lehtilä & Strauss, colour from green to yellow and withering leaves (Root, 1996). 1997), flower size (Strauss et al., 1996; Mothershead & Marquis, Thus, lacebug feeding causes chlorosis, thereby decreasing rates 2000) and pollen production (Quesada et al., 1995; Strauss et al., of gas exchange and photosynthesis due to parenchyma damage 1996). Furthermore, herbivory can change chemical compounds (Buntin et al., 1996). of flowers, such as volatile organic compounds (Kessler et al., 2011), and alkaloids in nectar (Adler et al., 2006). These stud- ies demonstrated that herbivore-induced changes in floral traits Experimental design decrease pollinator visits due to decreased attraction to pollina- tors. However, few studies have explored such indirect effects We conducted a field experiment in 2010 at a common garden of foliar herbivory on a whole flower visitor community, includ- in the Center for Ecological Research of Kyoto University (CER; ing pollinators and non-pollinators (i.e. florivores, thieves and 34∘58′N, 135∘57′E) in Otsu, central Japan. To examine the predators) (but see Smith et al., 2015). It is well known that flo- effects of early-season herbivory on floral traits and community ral traits influence visitations of pollinators and non-pollinators structure of associated arthropods, we conducted an inoculation similarly (e.g. Adler & Bronstein, 2004; Irwin et al., 2004; experiment using S. altissima and C. marmorata. We used plants Strauss & Whittall, 2006) or differently (Junker & Blüthgen, from five genotypes, collected from a natural habitat within 2008). As leaf herbivory can change a wide variety of floral 15 km of CER during spring 2008, and which since then had traits, as mentioned earlier, the early-season leaf herbivory may been grown in the common garden until 2010. From 26 April have a significant impact on abundance and/or species diversity to 2 May in 2010, we divided rhizomes into 7 cm segments and of pollinators and non-pollinators, thereby altering community planted each segment in a pot (10 cm in diameter). In total, 307 structure of flower visitors through changes in floral traits. ramets from five genets were grown in the greenhouse from 26 In this study, we examined whether early-season foliar April to 4 July. herbivory by the lacebug, Corythucha marmorata Uhler On 3–4 July, we selected 130 plants and transplanted (Hemiptera: Tingidae), can influence flower visitor communi- them individually into bigger pots (20 cm in diameter). We ties on tall goldenrod, Solidago altissima Linnaeus (Asteraceae). randomly assigned half of the plants to the lacebug her- In particular, we focused on the indirect effects via flower abun- bivory treatment, and the other half were herbivory-free as dance, because changes in flower abundance are well known a control. All of the plants were transferred to four field to change the number of flower visitors on Solidago plants cages (1.8 m × 1.8 m × 2.0 m), which were covered with a fine (Genung et al., 2010; Ikemoto et al., 2011; Smith et al., 2015). non-woven fibre cloth with high light transmissibility (Mor- Specifically, we addressed the following two questions: (i) ishita Inc., Osaka, Japan). Each of two cages was assigned to does foliar herbivory indirectly influence the arthropod visits herbivory treatment or control, and then each cage had 32 or via changes in flower abundance; (ii) do the effects of foliar 33 potted plants. On 5 July, four lacebugs (random mixture herbivory vary among functional groups of flower visitors (i.e. of adults and nymphs) were inoculated to each plant in the pollinators, florivores, thieves and predators), and thus change herbivory treatment. The lacebugs were collected from wild the flower visitor community structure? populations found on naturally growing tall goldenrods around CER. They could move freely between plants within the field cage. During the treatment, 18 inoculated and 28 uninoculated Materials and methods plants received accidental damage, and they were removed from cages. Subsequently, we obtained 47 damaged and 37 undam- Tall goldenrod, Solidago altissima L., is a perennial herb and aged plants. The herbivory level (i.e. proportion of damaged was introduced to Japan from North America around 1900, leaves of each of the experimental plants) did not differ between and thereafter spread throughout Japan (Fukuda, 1982). The the two cages (mean ± SD = 60.4 ± 25.5%; generalised linear growing season in Japan is from March until October, with model, F1, 45 = 0.01, P = 0.93). Furthermore, such herbivory plants flowering from October until November, and setting seed intensity is within the range of natural herbivory (24.3–86.0%) from November to December. It is self-incompatible, with a in nearby areas of the experimental garden (M. Ikemoto, highly diverse suite of insect pollinators, including species such unpublished). Hereafter, we refer to lacebug-inoculated and as Hymenoptera, Diptera and Coleoptera (Werner et al., 1980; uninoculated plants as ‘damaged plants’ and ‘undamaged Gross & Werner, 1983). A panicle inflorescence is formed by plants’, respectively.
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