Buddleja davidii Franch. (Loganiaceae), is native to China and Japan, but is a common ornamental shrub planted throughout much of North America and Europe. The shrub has abundant and colorful flowers that occur as 15 to 40 cm long racemic clusters. Flower color varies from white to pink, red, blue, and purple. The flower is strongly fragrant. It is attractive to butterflies (Corbett 2000) and is recommended in horticultural plantings as a source of nectar for butterflies.

Moths were initially observed orienting to butterfly bush flowers on the campus of Washington State University, Pullman, Washington, USA in late afternoon (P. J. Landolt, unpublished data). We hypothesize that moth visitation at these flowers may result from their response to flower odor. The odor chemistry of these flowers, reported by Andersson et al. (2002), is very complex and includes 31 compounds. Antennal responses for several species of butterflies to B. davidii floral scent were reported, narrowing down the list of compounds that could be butterfly attractants (Andersson 2003; Andersson & Dobson 2003). It is not yet known which chemicals in the butterfly bush flowers might be detected by or attractive to moths.

Some species of moths often visit flowers for nectar, and some of these species arrive at flowers following upwind attraction to floral odors. This behavior is particularly pronounced and well studied for pest species of noctuids in the subfamily Plusiinae. The cabbage looper moth Trichoplusia ni (Hübner), for example, visits or responds to odors of flowers of bladderflower, Araujia sericofera (Brot.) (Cantelo & Jacobson 1979), glossy abelia, Abelia grandiflora (Andre) (Grant 1971), night blooming jessamine, Cestrum nocturnum (Heath et al. 1992), and Japanese honeysuckle Lonicera japonica (Thunb.) (Pair & Horvat 1997). The alfalfa looper Autographa californica (Speyer) responds to flowers of Oregon grape, Berberis aquifolium (Prursh.) (Landolt & Smithhisler 2003), and the silver Y moth Autographa gamma (L.) is attracted to odors of flowers of creeping thistle, Cirsium arvense (L.), butterfly orchid, Platanthera bifolia (L.), soapwort, Saponaria officianalis (L), and others (Plepys 2001; Plepys et al. 2002b). Isolation and identification of the principal constituents of the odors of these flowers have provided a set of attractive chemicals for several major pest species of moths. For example, phenylacetaldehyde from flowers of bladderflower (Cantelo & Jacobson 1979) is attractive to a number of species of moths, and phenylacetaldehyde, benzyl alcohol, 2-phenylethanol, and benzaldehyde, isolated and identified from flowers of A. grandiflora, are attractive to cabbage looper moths (Haynes et al. 1991). The use of some of these floral attractants as lures holds promise for monitoring and surveying moths (Lopez et al. 2000; Landolt et al. 2006) or for management of pest species of moths (Camelo et al. 2007).

We report here studies to determine if moths are consistently visiting butterfly bush flowers and, if so, to identify those moths. We also determined the compounds that consistently make up the odor of those flowers and report antennal responses of cabbage looper and alfalfa looper moths to floral compounds emitted. This work addresses in part the hypothesis that moths are visiting butterfly bush flowers as a result of attraction to flower odor, and provides the identification of a set of chemicals that are putative attractants for moths that can be evaluated as such in future studies.

Methods and Materials

In May 2002, butterfly bush plants were purchased from Richard Owen Nursery (Bloomington, IL) and were planted on the grounds of the USDA, ARS Yakima Agricultural Experiment Station, near Donald, Yakima County, Washington, USA. These plants received regular irrigation from lawn sprinklers from mid Apr to mid Oct. Plants were 1 to 2 m tall when studies were initiated in Jul, 2003. Blooming occurred from Jun into Oct of 2003 and 2004. Bushes did not receive fertilizer or pesticide applications.

Results

Two hundred ninety three moths were captured in traps over butterfly bush flowers (Table 1). The greatest numbers were cabbage looper (52%) and alfalfa looper moths (24%). Other pest moths captured were the true armyworm Pseudaletia unipuncta (Haworth), the corn earworm, bertha armyworm, Mamestra configurata (Walker), Lacanobia subjuncta (Barnes & MacDunnough), clover looper, Caenurgina erechtea (Cramer), and the celery leaftier, Udea rubigalis (Guenee). In total, 12 species of Noctuidae, 6 species of Pyralidae, 2 species of Geometridae, and 1 tortricid species were captured in the traps. In addition, we caught 28 butterflies, 33 honeybees Apis mellifera L., 22 other bees and wasps, 277 syrphid flies, 133 other Diptera, 17 Hemiptera, 13 lacewings, 5 beetles, 9 earwigs, 3 damsel flies, and 10 spiders.

Nine compounds were present consistently in all 9 flower odorant samples and not in foliage odor samples (Table 2). Those compounds are 4-oxoisophorone (2,6,6-trimethyl-2-cyclohexene-1,4-dione); benzaldehyde; (E,E)-α-farnesene; 6-methyl-5-hepten-2-one; hexyl acetate; oxoisophorone oxide (1,3,3-trimethyl-7-oxabicyclo [4.1.0]-heptan-2,5-dione); dihydrooxoisophorone (2,6,6-trimethyl-1,4-cyclohexadione), β-cyclocitral, and (Z)-cinnamaldehyde (Fig. 1, chemical structures). These 9 compounds were initially identified by mass spectral data and the structures of 6 of these were then confirmed by comparing retention times and spectral data of those compounds with those of synthetic standards. Synthetic samples were not available for oxoisophorone oxide and dihydrooxoisophorone and those structural assignments are tentative. Mean amount of odorants emitted per floret was 57.4 ± 6.0 ng/h (mean ± S.E.). Flower clusters or racemes averaged 371 ± 38.7 florets, and mean amount of volatiles per raceme was then 21.3 ± 2.2 μg/h (mean ± S.E.). Amounts of chemicals collected were quite variable, indicated by the large standard errors for mean amounts of individual chemicals in Table 2. The limit of detection was estimated to be 0.1 ng per analysis, which was 60 ng per collection (0.1 ng/μL × 600 μL/sample).

Five of the floral compounds identified triggered consistent antennal responses in female cabbage looper moths (Table 2). These 5 compounds were benzaldehyde, 4-oxoisophorone, dihydrooxoisophorone, oxoisophorone oxide, and (E,E)-α-farnesene. Antennal responses to benzaldehyde, 4-oxoisophorone, and (E,E)-α-farnesene were confirmed by exposing female cabbage looper antennae to the corresponding standards. Three of the floral compounds, benzaldehyde, oxoisophorone oxide, and 4-oxoisophorone, elicited consistent antennal responses with male alfalfa looper moths (Table 2).

Discussion

Although known for “attractiveness” to day-active butterflies (Corbet 2000), the flowers of the butterfly bush also were visited consistently by night-flying Lepidoptera. The list of moths trapped indicates that a diversity of species of moths visits these flowers. However, most of the moths trapped were 2 pest species of Noctuidae in the subfamily Plusiinae; the cabbage looper and the alfalfa looper. Because our sampling was conducted in Jul and Aug and at 1 site, we expect that various numbers and additional species of moths would visit butterfly bush flowers at other times of the season and at other locations. Several species of Plusiinae, including the cabbage looper, alfalfa looper, and silver Y moth have been reported as frequent visitors at flowers of other plants. Cabbage looper moths have been observed at flowers of A. grandiflora (Grant 1971), alfalfa looper moths were collected at flowers of Oregon grape (Landolt & Smithhisler 2003), and the silver Y moth is an abundant visitor at flowers of Silene latifolia (Brantjes 1976).

Other pestiferous moth species that were trapped over butterfly bush flowers were the corn earworm and the true armyworm. The corn earworm moth feeds at flowers (Hendrix et al. 1987; Lindgren et al. 1993) and responds to odors of flowers such as Japanese honeysuckle Lonicera japonica, and Gaura drummondii (Beerwinkle et al. 1996; Pair & Horvat 1997; Lopez et al. 2000) and is also attracted to odors of fermented sugar baits (Ditman & Cory 1933). The true armyworm has not been reported as a frequent flower visitor, but was captured in traps baited with acetic acid and 3-methyl-1-butanol, a feeding attractant derived from fermented molasses solutions (Utrio & Eriksson 1977; Landolt & Higbee 2002).

We hypothesize that moths locate flowers of butterfly bush from some distance by flying upwind in response to the flower odor. Initial observations in late afternoon of moths at butterfly bush flowers indicated plume-tracking behavior (zigzagging upwind flights) at distances up to 2 M downwind of flower racemes, but these moths were not identified. We found that these flowers produce a high amount of odorants that might attract moths. Moth attraction to chemicals emitted by flowers is well documented. For example, many moths are attracted to bladderflower, and to phenylacetaldehyde, which is produced by bladderflower (Cantelo & Jacobson 1979). The cabbage looper moth is a frequent visitor at flowers of A. grandiflora (Grant 1971), which produces the cabbage looper attractants phenylacetaldehyde, benzaldehyde, 2-phenylethanol, and benzyl alcohol (Haynes et al. 1991). Alfalfa loopers visit flowers of Oregongrape, which produces a blend of odorant chemicals including the alfalfa looper attractants phenylacetaldehyde and β-myrcene (Landolt et al. 2001, Landot et al. 2006; Landolt & Smithhisler 2003). Other examples include moth attraction to flowers of L. japonica which produces phenylacetaldehyde, linalool, and cis-jasmone (Pair & Horvat 1997), C. nocturnum which produces benzaldehyde, benzyl acetate, and phenylacetaldehyde (Heath et al. 1992), S. latifolia which produces phenylacetaldehyde and lilac aldehydes (Dötterl 2004; Dötterl et al. 2006), and Platanthera bifolia which produces lilac aldehydes (Plepys et al. 2002a).

Five of the 9 compounds found in the odor of butterfly bush flowers elicited antennal responses in cabbage looper and 3 compounds in alfalfa looper moths, suggesting differences in antennal receptor sensitivity between moth species. Previous studies with butterflies and butterfly bush scents showed antennal responses to the same chemicals these moths responded to, although selective antennal responses to those compounds also were observed between butterfly species (Andersson 2003; Andersson & Dobson 2003). Differences in antennal responses between moth species could also indicate gender differences, with female cabbage looper being responsive to more compounds than male alfalfa looper, as suggested with the butterfly Heliconius melpomene (Andersson & Dobson 2003). Four-oxoisophorone and oxoisophorone oxide were the only 2 compounds that were found to consistently elicit antennal responses in both moth species as well as in the 4 butterfly species when testing butterfly bush scent samples (Andersson 2003; Andersson & Dobson 2003). Four-oxoisophorone is not only eliciting antennal responses in Lepidoptera species, but is active for bees (Dötterl et al. 2005).

Four-oxoisophorone was identified previously and in the present study as the most abundant compound emitted by butterfly bush flowers (Andersson et al. 2002; Andersson 2003). This compound is found also in floral scents of Primula farinosa (Gaskett et al. 2005), Lumnitzera racemosa (Azuma et al. 2002), Salix atrocinerea (Dötterl et al. 2005), and other plants (Knudsen et al. 2006). Two other compounds in the odor of butterfly bush, benzaldehyde and (E,E)-α-farnesene, are odorants for other moth-visited flowers. Benzaldehyde was found in odor of other plant species including C. nocturnum (Heath et al. 1992), A. grandiflora (Haynes et al. 1991), S. latifolia (Jürgens et al. 2002), and B. aquifolium (Landolt & Smithhisler 2003). (E,E)-α-farnesene was found in the floral odor of Japanese honeysuckle (Schlotzhauer et al. 1996). An additional butterfly bush flower odorant, cinnamaldehyde, which did not stimulate antennal responses in our study, is found in odor of flowers of S. latifolia (Jürgens et al. 2002), and G. drummondi (Teranishi et al. 1991).

Three to 5 of the 9 compounds produced by butterfly bush flowers are biologically relevant compounds for alfalfa looper and cabbage looper moths. Although it is not completely known which of these compounds may be involved in attracting night-flying moths, some are already known to be behaviorally active for the cabbage looper, alfalfa looper, and other moths. Benzaldehyde was attractive to cabbage looper moths in a flight tunnel assay (Haynes et al. 1991; Heath et al. 1992), but was not attractive to alfalfa looper moths when field-tested by Landolt et al. (2001) in Washington, or to soybean looper moths, Pseudoplusia includens (Walker), when field-tested by Meagher (2002) in Florida. Further research will be needed to determine which of these chemicals elicit upwind attraction responses in moths such as the cabbage looper and alfalfa looper.