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Behavioral Evidence for Host Transitions in Plant, Plant Parasite, and Insect Interactions

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Behavioral Evidence for Host Transitions in Plant, Plant Parasite, and Insect Interactions Environmental Entomology, 47(3), 2018, 646–653 doi: 10.1093/ee/nvy033 Advance Access Publication Date: 31 March 2018 Plant–Insect Interactions Research Behavioral Evidence for Host Transitions in Plant, Plant Parasite, and Insect Interactions Dale A. Halbritter,1,2,7 Denis S. Willett,3,4 Johnalyn M. Gordon,5 Lukasz L. Stelinski,3 and Jaret C. Daniels1,6 1Entomology and Nematology Department, University of Florida, 1881 Natural Area Dr, Gainesville, FL 32611, 2Present address: Invasive Plant Research Laboratory, USDA-ARS, 3225 College Avenue, Fort Lauderdale, FL 33314, 3Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL 33850, 4Center for Medical, Agricultural and Veterinary Entomology, USDA-ARS, 1600 SW 23rd Dr, Gainesville, FL 32608, 5Fort Lauderdale Research and Education Center, University of Florida, 3205 College Avenue, Davie, FL 33314, 6McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, 3215 Hull Road, Gainesville, FL 32611, and 7Corresponding author, e-mail: [email protected] Subject Editor: Jared Ali Received 3 November 2017; Editorial decision 26 February 2018 Abstract Specialized herbivorous insects have the ability to transition between host plant taxa, and considering the co-evolutionary history between plants and the organisms utilizing them is important to understanding plant insect interactions. We investigated the role of a pine tree parasite, dwarf mistletoe (Arceuthobium spp.) M. Bieb. Santalales: Viscaceae, in mediating interactions between Neophasia (Lepidoptera: Pieridae) butterflies and pine trees, the butterflies’ larval hosts. Mistletoe is considered the butterflies’ ancestral host, and the evolutionary transition to pine may have occurred recently. In Arizona, United States, we studied six sites in pine forest habitats: three in Neophasia menapia (Felder and R. Felder, 1859) habitat and three in Neophasia terlooii Behr, 1869 habitat. Each site contained six stands of trees that varied in mistletoe infection severity. Butterfly behavior was observed and ranked at each stand. Volatile compounds were collected from trees at each site and analyzed using gas chromatography- mass spectroscopy. Female butterflies landed on or patrolled around pine trees (i.e., interacted) more than males, and N. terlooii interacted more with pine trees than N. menapia. Both butterfly species interacted more with tree stands harboring greater mistletoe infection, and N. terlooii interacted more with heavily infected tree stands than did N. menapia. The influence of mistletoe onNeophasia behavior may be mediated by differences in tree volatiles resulting from mistletoe infection. Volatile profiles significantly differed between infected and uninfected pine trees. The role of mistletoe in mediating butterfly interactions with pines has implications for conservation biology and forest management, and highlights the importance of understanding an organism’s niche in an evolutionary context. Key words: butterfly, evolution, mistletoe, pine, volatile compound Specialized herbivorous insects can transition to different host biological communities and silviculture (Stevens and Hawksworth plant taxa through rapid genetic adaptation (Singer et al. 1993) 1970, Drummond 1982, Conklin 2000, Hoffman 2004). The pon- or via more gradual evolutionary processes (Dobler et al. 1996). derosa pine ecosystem occupies a significant portion of western Understanding the co-evolutionary history between plants and North America, ranging from extreme southwestern Canada to insects is key to understanding contemporary plant–insect interac- central Mexico (Little 1971) and the pines host dwarf mistletoes tions, especially when considering environmental stressors. Plant– (Hawksworth and Wiens 1996). Here, we investigate a tri-trophic insect interactions are critical to ecosystem function and developing interaction and a hypothesized host switch involving an insect her- successful habitat management strategies (Raffa et al. 2008, Soler bivore, its contemporary conifer host, and the mistletoe parasite in a et al. 2012). Other organisms can influence these interactions and ponderosa-pine dominated ecosystem. may contribute to host transitioning. For example, plant pathogens Pine butterflies in the genus Neophasia Behr, 1869 (Lepidoptera: can influence the attractiveness of the plants to herbivorous insects Pieridae) belong to the subtribe Aporiina and, in the New World, (McLeod et al. 2005, Mauck et al. 2010, Mann et al. 2012). Dwarf members of Aporiina are primarily mistletoe (Santalales) feeders and mistletoes, Arceuthobium spp. (M. Bieb. Santalales: Viscaceae), are are restricted to South America (Braby and Nishida 2010). However, flowering plants and parasites of conifers, and affect associated Neophasia and Eucheira Westwood, 1834 are two North American © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: [email protected]. 646 Downloaded from https://academic.oup.com/ee/article-abstract/47/3/646/4957024 by University of Florida user on 07 June 2018 Environmental Entomology, 2018, Vol. 47, No. 3 647 aporiine genera that feed on conifers and madrone (Arbutus) (L. southern range limit of N. menapia and the northern range limit Ericales: Ericaceae) trees, respectively. This break in phylogenetic of N. terlooii (Fig. 1). We focused on habitats for N. menapia and conservatism via the exploitation of new larval host plants may N. terlooii in Arizona at the southern and northern range boundaries have facilitated the northward expansion of these two genera, along of each butterfly species, respectively. with adaptation to colder climates. When combined, the geographic From July through mid-August, adult N. menapia spend sunny ranges of Neophasia menapia (Felder and R. Felder, 1859) and days patrolling pine trees in search of mates and trees suitable for ovi- Neophasia terlooii Behr, 1869 span 30 degrees of latitude in western position. In northern Arizona, we observed N. menapia ovipositing North America, which overlap considerably with the ponderosa pine on Rocky Mountain ponderosa pine (ponderosa pine, henceforth), ecosystem (for butterfly distributions, see: Scott 1986, Bailowitz and Pinus ponderosa ssp. scopulorum (Engelmann) (Pinales: Pinaceae), Brock 1991, Lotts and Naberhaus 2015). Central Arizona marks the but a considerably greater diversity of conifers is utilized in the rest of Fig. 1. Geographic distribution of the six sites in Arizona, each containing six tree stands. The blue shaded area indicates the distribution of Neophasia menapia at the county level. The red shaded area indicates the distribution of N. terlooii at the county level. The area in purple indicates the county where both species can be found, with the river marking the dividing line. The inset map shows the entire range of N. menapia in blue and that of N. terlooii in red. Arizona is purple because it contains both butterfly species. With the exception of a small area in SW Texas, inset distribution data are at the state or province scale. Distribution data were obtained from Lotts and Naberhaus (2015). NJ = North Jacob Lake, SC = Schultz Pass, MO = Mormon Lake, BF = Barfoot Park, SW = Sawmill Canyon, and CR = Carr Canyon. Downloaded from https://academic.oup.com/ee/article-abstract/47/3/646/4957024 by University of Florida user on 07 June 2018 648 Environmental Entomology, 2018, Vol. 47, No. 3 its range (see Discussion). N. terlooii has two flights per year, one in lengthwise through the center of each site. Each stand consisted of late spring/early summer and the primary flight, which is in October. two to six trees, where the two most distant trees in a stand were at Like its congener, N. terlooii patrols pine trees in search of mates and most 15 m apart from each other. Each stand was set apart from the trees suitable for oviposition. In the Arizona sky islands, we observed surrounding forest such that the tree crowns within the stands were N. terlooii ovipositing on Apache pine, Pinus englemannii Carrière, not touching the tree crowns of the surrounding forest matrix. The Arizona pine, P. ponderosa ssp. arizonica (Engelmann), ponderosa tree crowns within each stand were in contact. pine, and southwestern white pine, Pinus strobiformis Engelmann. Each site contained three stands that had visible dwarf mistletoe Southwestern dwarf mistletoe, Arceuthobium vaginatum subsp. infection and three stands with little to no visible infection. Stands eryptopodium (Engelmann) occurs throughout Arizona and para- were scored for infection on a scale from 0 to 6, with 0 being unin- sitizes ponderosa pine, Apache pine, and Arizona pine (Olsen 2003). fected and 6 being heavily infected. Scoring methods followed those Dwarf mistletoes induce a stress response that causes trees to alter of Hawksworth (1977), where the live crown of each tree in a stand their biochemistry (Nebeker et al. 1995). Stressed trees produce was divided into thirds, each third was visually scored as either 0 volatile chemicals such as monoterpenes, which have been shown (no visible infections), 1 (50% or less of the branches infected), or 2 to attract wood-boring insects (Costello et al. 2008). Four primary (greater than 50% of branches infected), and the sum of the thirds chemical isolates are emitted by infected Pinus contorta (Douglas was the score for the tree. We summed the scores of each tree in a ex Loudon)
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