FOREST ENTOMOLOGY
A Comparison of Electrophysiologically Determined Spectral Responses in Six Subspecies of Lymantria DAMON J. CROOK,1 HELEN M. HULL-SANDERS, EMILY L. HIBBARD,
AND
VICTOR C. MASTRO
USDA-APHIS-PPQ CPHST, Otis Laboratory, Building 1398, Otis Air National Guard Base, Buzzards Bay, MA 02542
J. Econ. Entomol. 107(2): 667Ð674 (2014); DOI: http://dx.doi.org/10.1603/EC13464
ABSTRACT The spectral sensitivity of the compound eye in three gypsy moth species from six different geographical regions (Lymantria dispar asiatica Vnukovskij [Asian gypsy moth], Lymantria dispar japonica Motschulsky [Japanese gypsy moth], and Lymantria dispar dispar L. [North American gypsy moth]) was tested electrophysiologically in the wavelength region 300 Ð700 nm. For all moths examined, a maximum response occurred in the 480 Ð520-nm range (blue-green region) with a shoulder peak occurring at 460 nm. A smaller, secondary peak was observed for both sexes at the 340 Ð380-nm range, which is in the region considered behaviorally maximal in night-ßying insects. No peaks in sensitivity were observed between 520 and 700 nm (red region) for any of the moths tested. Based on our retinal recording data, a short wavelength blocking Þlter with a transition wavelength near 500 nm should reduce gypsy moth attraction to artiÞcial lighting sources. This would help reduce the number of Lymantria-infested ships traveling to and from foreign ports. KEY WORDS electroretinogram, spectral sensitivity, gypsy moth, Lymantria
The gypsy moth (Lymantria dispar L.) is one of the most devastating pests of deciduous forests of the United States. L. dispar feed on ⬎500 species of plants, primarily broad-leafed trees, ornamental shrubs, and especially oaks (Campbell and Schlarbaum 1994). Adult females of the invasive European gypsy moth are not capable of ßight, but since its accidental release in Medford, MA, in 1868 or 1869, L. dispar has spread to occupy most of the hardwood forests in the eastern United States. It has spread west to Minnesota and north and east to Nova Scotia and New Brunswick, Canada (Pogue and Schaefer 2007). Isolated populations have occurred in other states, but have been eradicated by an intense and systematic pheromone trapping and spraying program. Each year ⬇US$12 million is spent on gypsy moth control (Campbell and Schlarbaum 1994, Pimentel et al. 2005). The Asian varieties of gypsy moth, known as “Asian gypsy moth,” pose an even greater risk to native forests because unlike the European variety, the Asian gypsy moth females are active ßiers (up to 100 km; Rozkhov and Vasilyeva 1982). The Asian gypsy moth is deÞned by the U.S. Department of Agriculture (USDA) as “any biotype of Lymantria dispar (sensu lato) possessing female ßight capability” (Pogue and Schaefer 2007). Flight ability and a broader range of hosts, including conifers (Baranchikov and Sukachev 1989, Turova 1992), give Asian gypsy moth the potential to establish and spread more quickly across North America (USDA 2003). Since 1991, repeated incursions into 1
Corresponding author, e-mail:
[email protected].
North America have been documented (Pogue and Schaefer 2007). These incursions are most often the result of gravid females attracted to lights at Asian ports where females deposit eggs on cargo and ships. The ships then unload their cargo at North American ports, such as Tacoma (WA), Portland (OR), and Vancouver (BC), where the neonates hatch and disperse (Wallner et al. 1995). Cost of controlling these incursions by state and federal emergency suppression efforts has been estimated in millions of dollars (Wallner et al. 1995, Pogue and Schaefer 2007). Visual orientation has been found to be a component of male sexual behavior in gypsy moths (Charlton and Carde´ 1990, Willis et al. 1994). The visual capabilities of Lymantria, particularly the Asian varieties, may be under evolutionary pressure, and therefore may have subtle differences between sexes and populations. Although previous studies have shown Lymantria attraction to light sources, most studies have focused on the daily activity rhythms that may inßuence ßight and male mating behavior (Wallner et al. 1995, Charlton et al. 1999). Understanding the visual receptor sensitivity of an insect allows for the evaluation of the stimuli that evoke a behavioral response (Mazokhin-Porshnyakov 1969, Brown and Cameron 1977). The simplest way to determine the spectral responses of an insect visual receptor system is to record the combined responses of several receptors using an electroretinogram (ERG). This information allows for the delimitation of the detectable range of colors to the insect being studied (Steiner et al. 1987)
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and leads to the possible evaluation of stimuli that might evoke a behavioral response. ERG recordings offer a good method of comparing spectral sensitivity curves of many closely related insect species (Eguchi et al. 1982). ERG-determined peaks have been shown to correspond to speciÞc spectral cell types (Autrum and von Zwehl 1964, Goldsmith and Fernandez 1968, Nosaki 1969, Laughlin et al. 1980). By studying the receptor sensitivity of the visual system, it is possible to evaluate the available stimuli that might evoke a behavioral response (Brown and Cameron 1977). For invasive insect pests such as the emerald ash borer, Agrilus planipennis Fairmaire, information gained from ERG recordings has proven particularly useful in the development of an effective, colored monitoring trap (Crook et al. 2009). The aim of this research was to survey the spectral responsiveness of males and females in several populations of L. dispar using electrophysiological methods (ERG) and compare the results with reported behavioral responses. Based on those Þndings it is hoped that recommendations and modiÞcations to lighting in ports and on ships could be made to help reduce the risk of further incursions into other countries. Materials and Methods Insects. Moths were laboratory-reared from egg masses that had been Þeld collected and subsequently colonized from multiple Asiatic regions. Moths were reared in quarantine at the USDA insect containment facility at Otis Air National Guard Base, Buzzards Bay, MA. Chinese (Asian gypsy moth) Lymantria dispar asiatica Vnukovskij was reared from eggs collected in Panshan, Tianjin, China, on 8 October 2007. Korean (Asian gypsy moth) L. dispar asiatica was reared from eggs collected in Pyeon Chang, Korea on 5 August 2009. Japanese (Japanese gypsy moth) Lymantria dispar japonica Motschulsky was reared from eggs collected from Northern Japan (Iwate district) on 18 October 2005. Russian Central (Asian gypsy moth) Lymantria dispar asiatica L. was reared from eggs collected in central Russia (Dalnerechensk) on 25 November 2005. Russian Port (Asian gypsy moth) L. dispar asiatica was reared from eggs collected in the Primorsky coastal region of Russia (Nakhodka, Vladivostok, Slavyanka, and Vostochny) on 25 November 2005. North American (North American gypsy moth) L. dispar dispar were obtained from an Otis laboratory colony of North American gypsy moth (⬎60 generations). All gypsy moth strains were reared on a wheat-germ diet developed by Bell et al. (1981) and held in a quarantine walk-in chamber within the Otis facility. The chamber was maintained at 21Ð23⬚C, 65% relative humidity, and a photoperiod of 16:8 (L:D) h. Larvae hatching from eggs were placed directly on diet and left in 6-oz plastic cups (Sweetheart Cup Company Inc., Owings Mills, MD) until pupae developed. Pupae were sexed and separated into individual cups. Neo-
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nate to adult emergence occurred within ⬇40 Ð 45 d. Adults used for recording experiments were 1Ð2 d old. ERG Recordings. The ERG system used in this study (similar to that described by Crook et al. (2009)) consisted of a lamp that delivered light stimuli to the compound eye of a moth via a monochromator, liquid light guide cable, and focusing lens. The entire system described below was purchased from Photon Technology International, Birmingham, NJ. The light source was a 75-W Xenon short arc lamp in a housing unit (model A-1010-B), connected to a tunable high intensity illuminator (model L-201). This was powered by a power supply (model 220B) and an igniter (model LPS 221). Monochromatic light output between 300 and 700 nm was obtained by passing light from the lamp through a monochromator (model 101) with 1,200 lines per millimeter and 300 nm grating. Light settings for the monochromator were controlled by a controller-shutter system (model MD-1000) connected to a desktop computer running MoCo (version 1.1, Windows 2000/XP, Photon Technology International, Birmingham, NJ). The monochromator bilateral slit was set to a 1.25 mm open setting (giving a 5 nm reciprocal dispersion). Selected wavelengths of light passed from the monochromator into a liquid light guide, terminating in a symmetric-convex lens (precision Þgured for 1:1 imaging) that focused a columnar 0.5-cm-wide beam directly onto the mothÕs eye preparation at a distance of 5 cm. Preparation for ERG involved removing the insect head from the thorax. Antennae and palps were removed from the head along with any obstructing scales. An insect pin (size 000) was used to make a small hole on the dorsal surface of the head, directly between the compound eyes. The head was then attached to recording electrodes of an EAG probe (Syntech, Hilversum, The Netherlands) using conductive gel (Spectra 360, Parker Laboratories, FairÞeld, NJ). The recording probe tip was connected to the punctured opening, while the indifferent (ground) probe was attached Þrmly to the base of the cut head. Moth “head probe” preparations were connected to an IDACC-232 serial data acquisition controller (Syntech). Signals and recordings were stored and analyzed on a desktop computer equipped with EAG software (Syntech 2004, version 2.6). Ten individuals of each sex and each population were allowed to adapt to total darkness for ⱖ10 min before a spectral sensitivity run commenced. Insects remained in total darkness between stimulations and were held behind a black-out screen to prevent any external light sources into the room so as to minimize interference. Stimulating ßashes lasted 1 s. The time interval between ßash stimulations was 90 s to allow full recovery of the recording baseline. Two sets of ßash stimulation runs were performed for each sex of each moth population tested. Insects were stimulated using light wavelengths between 300 and 700 nm in 10 nm increments, presented randomly. A 360-nm reference wavelength was ßashed onto the moth preparation after four stimulations to maintain normalization assumptions. This allowed for the possible reduction
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Fig. 1. Response of the compound eye of L. dispar populations by origin and sex as measured by ERG to wavelengths of light between 300Ð700 nm. Origins include: China ⫽ Chinese (Asian gypsy moth) L. dispar asiatica; Japan ⫽ Japanese (Japanese gypsy moth) L. dispar japonica; Korea ⫽ Korean (Asian gypsy moth) L. dispar asiatica; Lab ⫽ North American (North American gypsy moth) Otis laboratory colony; Russia Central ⫽ Russian Central (Asian gypsy moth) L. dispar asiatica; Russian Port ⫽ Russian Port (Asian gypsy moth) L. dispar asiatica. Sexes are f ⫽ female and m ⫽ male. Response is given in percentage (%) based on the reference wavelength response calculated to be 100% at 340 nm.
(or in some cases, improvement) in responses over time as the insect receptors decayed. In a second test, insects were randomly stimulated with light wavelengths between 300 and 420 nm in 5 nm increments. A 600-nm reference wavelength was ßashed onto the moth preparation after four random stimulations (for data normalization). Data Analysis. Percentage wavelength responses were arcsine-transformed before analysis to conform to the assumptions of analysis of variance (ANOVA) using JMP 9.0 (SAS Institute 2010, SAS Institute, Cary, NC). ANOVA was performed using the following main effects on the optical response: light wavelength, origin of the population, sex and their interaction effects. Analyses that found no signiÞcant interactions (P ⬎ 0.10) were dropped from the model and pooled into the error term. TukeyÕs honest signiÞcant difference (HSD) mean separation test was used to determine signiÞcant differences between interacting means. Results Spectral sensitivity curves for males and females of all six moth varieties recorded between 300 Ð700 nm
are shown in Fig. 1. Spectral light wavelength, population origin, and sex of the moth all signiÞcantly affected the compound eyeÕs response and there were both signiÞcant two-way and three-way interactions (Table 1). A single curve, based on the C wave amplitude of the ERG response, is presented in Fig. 2. Maximum response of the gypsy moth compound eye Table 1. Effect of wavelength, sex, and pop origin on eye response (arcsin-transformed), tested by ANOVA Source of variation
df
MS
F
P
A) 300Ð700 nm Wavelength 20 68.2045 579.8558 ⬍0.0001 Sex 1 3.4935 29.7007 ⬍0.0001 Origin 5 1.4672 12.4739 ⬍0.0001 Wavelength ⫻ sex 20 0.4105 3.4901 ⬍0.0001 Wavelength ⫻ origin 100 0.1856 1.5783 0.0003 Sex ⫻ origin 5 1.7571 14.9385 ⬍0.0001 Wavelength ⫻ sex ⫻ origin 100 0.2360 2.0070 ⬍0.0001 Error 2,352 0.1172 B) 300Ð420 nm Wavelength 24 6.0534 72.8766 ⬍0.0001 Sex 1 2.6971 21.4698 ⬍0.0001 Origin 5 2.9950 36.0564 ⬍0.0001 Sex ⫻ origin 5 1.2007 14.452 ⬍0.0001 Error 3,256 0.0831
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Fig. 2. Response of the compound eye of female (f) and male (m) L. dispar populations as measured by ERG to wavelengths of light between 300Ð700 nm. Response is given in percentage (%) based on the reference wavelength response calculated to be 100% at 340 nm.
occurred in the 480 Ð520-nm range (blue-green region) with a shoulder peak occurring at 460 nm (Fig. 2). No peaks in sensitivity were observed between 520 and 700 nm for any of the moths tested. However, a smaller, secondary peak was observed for both sexes at the 340 Ð380-nm range (Fig. 2), which is in the region considered behaviorally maximal in night-ßying insects (Mikkola 1972). Spectral sensitivities for all six moth varieties (male and female) recorded between 300 Ð 420 nm are shown in Figs. 3 and 4. There were no signiÞcant interactions between wavelength and sex or origin; therefore, the terms were removed from the model and pooled into the error term. Although the overall response to wavelength varied signiÞcantly in the 300 Ð 420-nm range (F ⫽ 72.8766; df ⫽ 24, 3256; P ⬍ 0.001; Table 1), across subspecies, female mean response to light wavelength was consistently higher than male response (F ⫽ 2.6971; df ⫽ 1, 3256; P ⬍ 0.0001), with the largest differences between means occurring at 345 nm (5.80727 ⫾ 0.04042 SE females; 5.68763 ⫾ 0.03375 SE males) and 355 nm (5.82442 ⫾ 0.04042 SE females; 5.72445 ⫾ 0.03375 SE males). Across sexes, the North American laboratory population had the highest response and the Russian central population tended to have the lowest response, with the largest differences between means occurring at 375 nm (206.778 ⫾ 10.862 SE laboratory; 145.727 ⫾ 5.0913 SE Russian central) and 395 nm (207.037 ⫾ 10.862 SE laboratory; 143.909 ⫾ 5.0913 SE Russian
central). For female moth recordings between 300 Ð 420 nm, Japanese (Japanese gypsy moth) L. dispar japonica had signiÞcantly higher responses than the Þve other female moth species tested (Fig. 4). Female Japanese (L. dispar japonica), Chinese (L. dispar asiatica), and Korean (L. dispar asiatica) moths all gave signiÞcantly higher responses (between 300 Ð 420 nm) than the two Russian (L. dispar asiatica) female moth species. For recordings made on male moths between 300 Ð 420 nm, North American (North American gypsy moth) L. dispar dispar had signiÞcantly higher responses than the Þve other male moth strains tested (Fig. 4). The absolute size of the ERG response varied in different preparations. The ERG responses for males and females of each of the moth strains are shown in Table 2. All moth responses had a general increase in sensitivity from 300 nm up to 350 nm. Responses peaked and plateaued between 350 nm and 400 nm. Discussion There have been numerous electrophysiological, microspectrophotomerical, and biochemical studies conducted in the last century on insect vision systems. Lepidoptera have a color vision system in which three or four types of spectral receptors cover the wavelength region from the ultraviolet (UV) to ⬇700 nm, irrespective of whether they were diurnal or nocturnal (Ho¨ glund and Struwe 1970, Eguchi et al. 1982).
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Fig. 3. Response of the L. dispar compound eye across populations separated by sex as measured by ERG for wavelengths of light between 300 and 420 nm. Origins include: China ⫽ Chinese (Asian gypsy moth) L. dispar asiatica; Japan ⫽ Japanese (Japanese gypsy moth) L. dispar japonica; Korea ⫽ Korean (Asian gypsy moth) L. dispar asiatica; Lab ⫽ North American (North American gypsy moth) Otis laboratory colony; Russia Central ⫽ Russian Central (Asian gypsy moth) L. dispar asiatica; Russian Port ⫽ Russian Port (Asian gypsy moth) L. dispar asiatica. Sexes are f ⫽ female and m ⫽ male. Response is given in percentage (%) based on the reference wavelength response calculated to be 100% at 600 nm.
The response curves we observed are very similar to a study done on L. dispar by Brown and Cameron (1977). They reported ERG responses that had low sensitivity in the UV region, higher sensitivity from 480 to 590 nm and essentially no sensitivity in the red region. They also examined the visual screening pigments of male gypsy moths and found them to have low absorption in the UV and red regions and high absorption from 400 to 600 nm. Other ERG studies on Lepidoptera usually show a maximum response in the blue-green to yellow range of the spectrum (490 Ð570 nm). However, the behavioral maximum normally occurs within the UV range (340 Ð380 nm; Mikkola 1972, Eguchi et al. 1982) despite the response to the UV range usually being 4 Ð5 times less sensitive (Mazokhin-Porshnyakov 1969, Mikkola 1972). Our results indicated that there was a third “shoulder” peak occurring at 460 nm, which is identical to the response reported by Eguchi et al. (1982) in a study that examined 35 species of Lepidoptera. This maximum at 460 nm (blue) may represent an independent color receptor tuned to the max-
imum spectral component of light from blue sky (Eguchi et al. 1982). Lymantria have a typical superposition eye (Brown 1974). This type of eye design allows for as many as 2,000 lenses to collect light for a single photoreceptor (Warrant 2006). All six Lymantria studied exhibited the same wavelength speciÞc peaks between 300 Ð700 nm indicative of trichromatic color vision systems. Wallner et al. (1995) suggested that even though Lymantriidae are generally nocturnal, L. dispar may have bimodal spectral sensitivity, activity, and pheromone response rhythms. Color vision in arthropods is mostly trichromatic, that is, using equidistant receptor peaks for a multipurpose vision system (Barlow 1982, Vorobyev 1997, Kelber 2006). The most common type of trichromacy in arthropods uses UV receptors stimulated with wavebands of light ⬵ 350 nm, blue receptors sensitive to ⬵ 450 Ð 480 nm, and green receptors with maximally sensitive to ⬵ 500 Ð550 nm (Kevan and Backhaus 1998). This trichromatic color vision system is found in bivalves, isopods, some spiders, and crustaceans along
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Fig. 4. Response of the compound eye of L. dispar populations by origin and sex as measured by ERG to wavelengths of light between 300Ð420 nm. Origins include: China ⫽ Chinese (Asian gypsy moth) L. dispar asiatica; Japan ⫽ Japanese (Japanese gypsy moth) L. dispar japonica; Korea ⫽ Korean (Asian gypsy moth) L. dispar asiatica; Lab ⫽ North American (North American gypsy moth) an Otis laboratory colony; Russia Central ⫽ Russian Central (Asian gypsy moth) L. dispar asiatica; Russian Port ⫽ Russian Port (Asian gypsy moth) L. dispar asiatica. Sexes are f ⫽ female and m ⫽ male. Letters above the bars indicate signiÞcant differences (P ⬍ 0.05) based on TukeyÕs HSD.
with many insects that include Orthoptera (Gryllus bimaculatus De Geer), Coleoptera (Notonecta glauca L., Coccinella sp., Dineutes ciliatus Forsberg), Hymenoptera (Melipona quadrifasciata [Lepeletier], Apis mellifera L., Osmia rufa L.), as well as Lepidoptera (especially nocturnal moths and some butterßies [see Eguchi et al. 1982 for review]) (Kelber 2006). Nocturnal animals tend to have fewer receptor types. For example, night-ßying hawkmoths have three receptor types compared with diurnal butterßies that have Þve. At starlight intensities to which the human eye would be color blind, the nocturnal hawkmoth, Deilephila elpenor L., is still able to use chromatic signals (Johnsen et al. 2006). Their crepuscular vision appears to be more complex than simply pooling signals from their three spectral channels. The photoreceptors of a single ommatidium apparently absorb too few photons for reliable discrimination to occur. Spatial or temporal summation must improve sensitivity enough to allow color vision to be possible between dusk and Table 2.
starlight (Kelber et al. 2002, Land and Osorio 2003). The multiple pigment system shared by the six Lymantria subspecies may act to maximize photon capture across a broad wavelength range during dim light conditions, while at the same time allowing color perception in brighter light conditions (Eguchi et al. 1982). UV light traps are frequently used for collecting and sampling insects and are known to attract both male and female L. dispar (Brown and Cameron 1977, Baranchikov and Sukachev 1989, Turova 1992, Wallner et al. 1995). Marked gypsy moth females have been recaptured at UV lamps 3.5 km from their release site (Baranchikov and Sukachev 1989). Introductions of the Asian strain of gypsy moth L. dispar into North America have previously occurred because of the attraction of gravid females to commercial lighting in Russian Far East ports (Anonymous 1992). Egg masses were deposited on cargo and ships and subsequently transported to the Northern American ports of Ta-
Range of response (mV) of Asian gypsy moth populations by sex at 360 and 500 nm Population
China L. dispar asiatica Korea L. dispar asiatica Japan L. dispar japonica Russia (central) L. dispar asiatica Russia (port) L. dispar asiatica North AmericaÐlaboratory L. dispar dispar
Sex
Response (mV) @360 nm
Response (mV) @500 nm
Female Male Female Male Female Male Female Male Female Male Female Male
0.92Ð40.68 2.82Ð23.86 0.79Ð47.51 2.78Ð48.28 1.23Ð27.43 0.25Ð44.19 3.63Ð25.42 4.85Ð23.17 5.01Ð25.42 6.03Ð31.30 0.49Ð14.07 6.03Ð31.30
1.99Ð30.08 3.67Ð38.08 1.41Ð79.52 7.80Ð58.74 3.12Ð49.33 0.19Ð45.54 6.99Ð48.67 11.05Ð47.57 4.39Ð40.53 6.80Ð56.28 1.85Ð21.62 6.80Ð47.07
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coma (WA), Portland (OR), and Vancouver (BC), where the eggs hatched and dispersed. It is estimated that the resulting eradication program in 1992 cost an estimated US$25 million (Wallner et al. 1995). Similar invasive incursions of lymantriid moths could be greatly reduced by modifying lights used in ports and onboard ships so that they are less attractive to gravid females. Wallner et al. (1995) examined attraction of three lymantriid species to ßuorescent blacklight, mercury vapor, and high-pressure sodium lamps in Russia. They also tested attraction to lamps that had been modiÞed with Þlters that eliminated light wavelengths ⱕ 480 nm. They found that L. dispar, Lymantria mathura Moore, and Lymantria monacha L. were attracted to all light sources tested (without Þlters). When light sources were covered with Þlters the hourly capture rate was signiÞcantly reduced for L. mathura and L. monacha. L. dispar hourly capture rates were signiÞcantly reduced for mercury vapor laps and somewhat reduced for high-pressure sodium lamps. Our retinogram data on lymantriid moths from different regions parallels Brown and CameronÕs (1977) ERG responses of L. dispar males, and thus supports the behavioral responses showed by Wallner et al. (1995). A short wavelength blocking Þlter with a transition wavelength ⬵ 500 nm should reduce attractancy to moths while providing adequate illumination for human activity (Wallner et al. 1995). We support the recommendation made by Wallner et al. (1995) that lighting systems in Far East ports should be Þltered to help reduce the number of Lymantria infested ships traveling to foreign ports.
Acknowledgments This research was funded by the U.S. Department of AgricultureÐThe Animal and Plant Health Inspection ServiceÐ Plant Protection and Quarantine ÐThe Center for Plant Health Science and Technology research program. We thank Joe Francese for reviewing an earlier draft of the manuscript. We also thank the two anonymous reviewers for comments on the manuscript.
References Cited Anonymous. 1992. Battling a new intruder: the Asian gypsy moth. Natl. Geogr. Mag. 182: 12. Autrum, H., and V. von Zwehl. 1964. Die spektrale empÞndlichkeit enzelner Sehzellen des Bienenauges. Zeitschrift Fur Vergleichende Physiologie 48: 357Ð384. Baranchikov, Y. N., and V. N. Sukachev. 1989. Ecological basis of the evolution of host relationships in Eurasian gypsy moth populations, pp. 319 Ð338. In W. E. Wallner and K. A. McManus (Tech. Coord.), Proceedings, Lymantriidae: a comparison of features of New and Old World tussock moths: June 26 ÐJuly 1, 1988, No. 123, New Haven, CT. Barlow, H. B. 1982. What causes trichromacy? A theoretical analysis using comb-Þltered spectra. Vision Res. 22: 635Ð 643. Bell, R. A., D. C. Owens, M. Shapiro, and J. R. Tardif. 1981. Development of mass rearing technology, pp. 599 Ð 633. In C. C. Doane and M. L. McManus (eds.), The gypsy moth:
673
research toward integrated pest management. United States Forest Service Technical Bulletin 1584. Brown, E. A. 1974. Vision in Porthetria dispar (L.) males: Physiological spectral sensitivity and behavioral implications. M.Sc. thesis in Entomology, p. 38. The Pennsylvania State University, PA. Brown, E. A., and A. E. Cameron. 1977. Studies of the compound eye of Lymantria dispar (Lepidoptera: Lymantriidae) males, and behavioral implications. Can. Entomol. 109: 255Ð260. Campbell, F. T., and S. E. Schlarbaum. 1994. Fading Forests: North American trees and the threat of exotic pests. Natural Research Defense Council, New York, NY. Charlton, R. E., and R. T. Carde´. 1990. Factors mediating copulatory behavior and close-range mate recognition in the male gypsy moth, Lymantria dispar (L.). Can. J. Zool. 68: 1995Ð2004. Charlton, R. E., R. T. Carde´, and W. E. Wallner. 1999. Synchronous crepuscular ßight of female Asian gypsy moths: relationships of light intensity and ambient and body temperatures. J. Insect Behav. 12: 517Ð531. Crook, D. J., J. A. Francese, K. E. Zylstra, I. Fraser, A. J. Sawyer, D. W. Bartels, D. R. Lance, and V. C. Mastro. 2009. Laboratory and Þeld response of the emerald ash borer (Coleoptera: Buprestidae), to selected regions of the electromagnetic spectrum. J. Econ. Entomol. 102: 2160 Ð2169. Eguchi, E., K. Watanabe, T. Hariyama, and K. Yamamoto. 1982. A comparison of electrophysiologically determined spectral responses in 35 species of Lepidoptera. J. Insect Physiol. 28: 675Ð 682. Goldsmith, T. H., and H. R. Fernandez. 1968. Comparative studies of crustacean spectral sensitivity. Zeitschrift fu¨ r vergleichende Physiologie 60: 156 Ð175. Ho¨ glund, G., and G. Struwe. 1970. Pigment migration and spectral sensitivity in the compound eye of moths. Zeitschrift fu¨ r vergleichende Physiologie 67: 229 Ð237. Johnsen, S., A. Kelber, E. Warrant, A. M. Sweeney, E. A. Widder, R. L. Lee, Jr., and J. Herna´ ndez-Andre´s. 2006. Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J. Exp. Biol. 209: 789 Ð 800. Kelber, A. 2006. Invertebrate colour vision, pp. 250 Ð290. In E. Warrant and D. E. Nilsson (eds.), Invertebrate vision. Cambridge University Press, New York, NY. Kelber, A., A. Balkenius, and E. Warrant. 2002. Scotopic colour vision in nocturnal hawkmoths. Nature 419: 922Ð 925. Kevan, P. G., and W.G.K. Backhaus. 1998. Color vision: ecology and evolution in making the best of the photic environment, pp. 163Ð183. In W.G.K. Backhaus, R. Kliegl, and J. S. Werner (eds.), Color vision perspectives from different disciplines. Walter de Gruyter and Co., Berlin. Land, M. F., and D. Osorio. 2003. Colour vision: colouring the dark. Curr. Biol. 13: R83ÐR85. Laughlin, S. B., A. D. Blest, and S. Stowe. 1980. The sensitivity of receptors in the posterior median eye of the nocturnal spider, Dinopis. J. Comp. Physiol. A 141: 53Ð 66. Mazokhin-Porshnyakov, G. A. 1969. Insect vision. In T. H. Goldsmith (translation ed.), Plenum Press, New York, NY. Mikkola, K. 1972. Behavioral and electrophysiological responses of night-ßying insects, especially Lepidoptera, to near-ultraviolet and visible light. Ann. Zool. Fenn. 9: 225Ð 254. Nosaki, H. 1969. Electrophysiological study of color encoding in the compound eye of crayÞsh, Procambarus clarkia. Zeitschrift Fur Vergleichende Physiologie 6: 318 Ð323.
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JOURNAL OF ECONOMIC ENTOMOLOGY
Pimentel, D., R. Zuniga, and D. Morrison. 2005. Update of the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52: 273Ð288. Pogue, M. G., and P. W. Schaefer. 2007. A review of selected species of Lymantria Hu¨ bner [1819] (Lepidoptera: Noctuidae: Lymantriinae) from subtropical and temperate regions of Asia, including the descriptions of three new species, some potentially invasive to North America, pp. 223. Forest Health Technology Enterprise Team Technology Transfer FHTET-2006 Ð 07. Rozkhov, A. S., and T. G. Vasilyeva. 1982. Gypsy moth in Middle and Eastern Siberia, pp. 4 Ð19. In Neparny Shelkoprayo v srednai i Vostochnoi Sibiti. Novosibirsk: Nauka, Russian Academy of Sciences, Siberian Branch, Novosibirsk. SAS Institute. 2010. JMP version 8.0.2. SAS Institute, Cary, NC. Steiner, A., P. Ru¨ diger, and R. Gemperlein. 1987. Retinal receptor types in Aglais urticae and Pieris brassicae (Lepidoptera), revealed by analysis of the electroretinogram obtained with Fourier interferometric stimulation (FIS). J. Comp. Physiol. 160: 247Ð258. Syntech. 2004. EAG Software version 2.6. Hiversum, The Netherlands. Turova, G. 1992. Peculiarities of gypsy moth biology in the Far East, pp. 117Ð124. In Problems of rational forest man-
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agement in the Far East. Far East Forestry Institute, Khabarovsk. [USDA] U.S. Department of Agriculture. 2003. Asian Gypsy Moth. U.S. Dep. Agric. Plant Protection and Quarantine Factsheet April 2003. (http://www.aphis.usda. gov/publications/plant_health/content/printable_ version/fs_phasiangm.pdf). Vorobyev, M. 1997. Costs and beneÞts of increasing the dimensionality of colour vision system, pp. 280 Ð289. In C. Taddei-Ferretti (ed.), Biophysics of photoreception: molecular and phototransductive events. Woted ScientiÞc, Singapore. Wallner, W. E., L. M. Humble, R. E. Levin, Y. N. Baranchikov, and R. T. Carde´. 1995. Response of adult Lymantriid moths to illumination devices in the Russian Far East. J. Econ. Entomol. 88: 337Ð342. Warrant, E. J. 2006. Invertebrate vision in dim light, pp. 83Ð126. In E. Warrant and D. E. Nilsson (eds.), Invertebrate vision. Cambridge University Press, New York, NY. Willis, M. A., C. T. David, J. Murlis, and R. T. Carde´. 1994. Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind ßight of male gypsy moths (Lymantria dispar) in a forest (Lepidoptera: Lymantriidae). J. Insect Behav. 7: 385Ð 409. Received 21 October 2013; accepted 29 December 2013.
