24106 N. Bunn Road, Prosser, WA, 99350, USA. Available online: 11 Jul 2011

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1 This article was downloaded by: [christelle guedot] On: 22 November 2011, At: 15:20 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK International Journal of Pest Management Publication details, including instructions for authors and subscription information: Trapping hop looper moths, Hypena humuli Harris (Lepidoptera: Erebidae), in hop yards with acetic acid and 3-methyl-1-butanol Peter J. Landolt a, Christelle Guédot a, James Hansen a, Lawrence Wright b & David G. James b a USDA, ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA, USA b Washington State University, Irrigated Agriculture Research and Extension Center, N. Bunn Road, Prosser, WA, 99350, USA Available online: 11 Jul 2011 To cite this article: Peter J. Landolt, Christelle Guédot, James Hansen, Lawrence Wright & David G. James (2011): Trapping hop looper moths, Hypena humuli Harris (Lepidoptera: Erebidae), in hop yards with acetic acid and 3-methyl-1- butanol, International Journal of Pest Management, 57:3, To link to this article: PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.

2 International Journal of Pest Management Vol. 57, No. 3, July September 2011, Trapping hop looper moths, Hypena humuli Harris (Lepidoptera: Erebidae), in hop yards with acetic acid and 3-methyl-1-butanol Peter J. Landolt a *, Christelle Gue dot a, James Hansen a, Lawrence Wright b and David G. James b a USDA, ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA, USA; b Washington State University, Irrigated Agriculture Research and Extension Center, N. Bunn Road, Prosser, WA 99350, USA (Received 3 November 2010; final version received 7 February 2011) Downloaded by [christelle guedot] at 15:20 22 November 2011 Hop looper moths, Hypena humuli Harris, in commercial hop yards (Humulus lupulus L.) were captured in traps baited with a combination of acetic acid plus 3-methyl-1-butanol (AAMB). The two chemicals were synergistic in attracting hop looper moths. In a comparison of the lure chemicals, most moths were trapped with AAMB as the lure, while very few moths were captured in traps baited with acetic acid alone or 3-methyl-1-butanol alone. Female and male hop looper moths were trapped with AAMB, with an overall sex ratio through the year of 44% females to 56% males. Moths were trapped in all months of the growing season, from April into October. From April through September, most females captured in traps were mated, whereas in October most females trapped had been unmated. Most of the mated females, we trapped contained one spermatophore, indicating a single mating. The numbers of moths trapped were low from April through June, and increased greatly in July, and at one site again in late August. AAMB-baited traps may be a useful tool for monitoring hop looper moths in commercial hop yards, to determine their presence, and potentially to assess the risk of damaging infestations. Keywords: Hypena humuli; hop looper; Humulus lupulus; hops; trapping; lure; monitoring 1. Introduction The hop looper, Hypena humuli Harris, is widely distributed in temperate North America (Holland 1968). The moth was originally placed in the family Noctuidae, subfamily Hypeninae (Hodges et al. 1983) but is now in the family Erebidae (but still subfamily Hypeninae) (Lafontaine and Schmidt 2010). The larvae feed on the foliage of Urtica spp. (nettles) and the taxonomically related crop Humulus lupulus L. (hops) (Robinson et al. 2002). In North America, it is a longstanding pest of hop vines grown for production of the cones that are used in the brewing of beer (Howard 1897; Hawley 1918; Grasswitz and James 2008). Larva numbers are controlled by the application of synthetic insecticides and Bacillus thuringiensis or Bt products (Grasswitz and James 2008; Barbour 2010). Grasswitz and James (2008) provided life-history information, including seasonal phenology, as part of an effort to improve pest management practices. In that study, the seasonal pattern of presence of adult moths was indicated by captures of the moths in light traps, which showed spring and summer flight periods. Traps are often used to determine the occurrence of agricultural pests, and in some cases to indicate the need for, or timing, of pest control measures. Presently, traps are not used for detecting or monitoring H. humuli as a pest of hops. Blacklight traps can be used to detect and monitor hop looper moths and document relative numbers (Grasswitz and James 2008), but this technique is not used by growers. Blacklight traps might not be useful for monitoring pest insects because of the relative expense of their purchase and operation, because they are not selective in attracting night-flying insects, and because lunar and other background lighting interferes with insect response to the blacklight of the trap (Yela and Holyoak 1997). Sex pheromones are used as attractants for trapping numerous species of pest moths (Mayer and McLaughlin 1991), but an attractive sex pheromone has not been identified for the hop looper. A chemical attractant in a trap could provide a valuable and inexpensive means for monitoring hop loopers in hop yards, and so potentially improve pest management. Acetic acid with 3-methyl-1-butanol (AAMB) may have the potential for luring and trapping hop looper moths. This combination of chemicals is part of the composition of odorants emitted by a fermented solution of molasses (Utrio and Eriksson 1977), and is attractive to a number of species of noctuid, pyralid, erebid, and other moths (Landolt 2000; Landolt and Hammond 2001; To th et al. 2002, 2010; Landolt et al. 2006). Small numbers of Hypena californica Behr and an unidentified Hypena sp. were captured in traps baited with this lure in Alaska (Landolt et al. 2006). Small numbers of H. humuli were captured in traps baited with AAMB in a riparian habitat in Washington *Corresponding author. peter.landolt@ars.usda.gov ISSN print/issn online Ó 2011 Taylor & Francis DOI: /

3 184 P.J. Landolt et al. state in 2007 and 2008 (P.J. Landolt unpublished observations), but were not captured in traps with the same lure in similar locations in 1999 (Landolt and Hammond 2001). These observations suggest, but do not experimentally demonstrate, attractiveness of AAMB to Hypena species. We report here experiments to test the hypotheses that both sexes of the hop looper moth are attracted to AAMB lures, and that the combination of chemicals is necessary and synergistic for that attraction. We also demonstrate the seasonal presence of the moth in hop yards using the same lure, and we document the mating status of female moths that have responded to that lure. 2. Materials and methods Lures were made as described by Landolt and Alfaro (2001), using 8 ml polypropylene vials (Nalg Nunc Co., Rochester, NY, USA). Each vial contained two cotton balls and 5 ml of active ingredient, either acetic acid or 3-methyl-1-butanol (Aldrich Chemicals, Milwaukee, WI, USA). Each vial had a 3-mm diameter hole in the lid for emission of evaporated attractant. Universal moth traps (Agrisense Ltd, Pontypridd, UK) were used for all tests. Traps were a multicoloured design, with a white bucket covered by a yellow cone and topped with a green lid. Lures (vials) were suspended within the bucket of the trap by a fine wire folded over the top of the bucket. A 2.5-cm 2 piece of Vaportape 1 (Hercon Environmental Inc., Emigsville, PA, USA) was stapled to the side of the interior of the bucket to kill captured moths. An experiment was conducted to determine moth response to acetic acid and 3-methyl-1-butanol, presented alone and together in traps. The four trap treatments were: (1) control trap with no chemical lure, (2) trap baited with a vial releasing acetic acid, (3) trap baited with a vial releasing 3-methyl-1-butanol, and (4) trap baited with two vials, one releasing acetic acid and the other releasing 3-methyl-1-butanol (AAMB). Traps were suspended from stakes at a height of 0.7 m, about 10 m apart, in a commercial hop yard near Moxee, Yakima County, Washington. A randomized complete block experimental design was used, with the four trap treatments randomized within each of six replicate blocks. Traps were checked weekly, at which time captured insects were removed. Lures were replaced at intervals of 2 weeks, and the experiment was maintained from 24 March to 1 June A second experiment documented season long captures of hop looper moths in traps baited with AAMB. Lures were made and presented as described above, with each chemical released from a separate vial within the trap. Six traps were maintained in a commercial hop yard in Yakima County, Washington, near Moxee, from 24 March to 26 October These traps were 40 m apart. A second set of six AAMBbaited traps, each paired with an unbaited control trap, was maintained from 13 April to 26 October 2010 in commercial hop yards near Prosser, Benton County, Washington. Vaportape was replaced every 4 weeks and lures were replaced every 2 weeks. Unbaited traps were placed 10 m from treated traps, with a minimum distance between pairs of traps of 6 km. Up to 30 female hop looper moths (or all females trapped when fewer than 30 were collected) from traps at the Moxee site were dissected each week, to assess their mating status and mating frequency. The number of spermatophores present each female s bursa was determined in these dissected females (spermatophores are nutrient-rich nuptial gifts from males donated during copulation). Trap catch data for females and males from the first experiment were subjected to an ANOVA, and means for lure treatments were separated using Tukey s Honestly Significant Difference Test (DataMost 1995). Both the mean and the standard error of the mean values were calculated for males and for females trapped in the second experiment, for each week of the season, and for the Yakima County and Benton County sites. The numbers of moths captured in Benton County traps were summed through the year for each trap, and trap catch data were square roottransformed before analysis by paired Student s t-test, to compare baited and unbaited traps. Voucher specimens of male and female hop looper moths have been deposited in the James Entomological Collection, Washington State University, Pullman, WA. 3. Results At Moxee, for the test of chemical attraction and synergy, the numbers of male and female hop looper moths captured in traps baited with AAMB were significantly greater than the numbers in unbaited control traps and traps baited with acetic acid alone or baited with 3-methyl-1-butanol alone (Table 1). At Prosser, mean ( + SE) numbers of female hop looper moths per AAMB traps for the year ( ) were significantly greater by Student s t-test than numbers captured in unbaited traps ( ) (t ¼ 3.18, P ¼ 0.01, df ¼ 10). Similarly, males Table 1. Mean (+ SE) numbers of male and female hop loopers captured in traps baited with acetic acid (AA) and 3-methyl-1-butanol (MB); Yakima County, April/June UNBAITED AA MB AA þ MB Male b b b a Female b b b a 1 Means in a row followed by the same letter are not significantly different by Tukey s Honestly Significant Difference Test at P ¼ For male data, ANOVA F 29 ¼ 6.05, P ¼ For female data, ANOVA F 29 ¼ 8.87, P ¼

4 International Journal of Pest Management 185 captured in AAMB traps ( ) were greater than in control traps ( ) (t ¼ 2.93, P ¼ 0.015, df ¼ 10). At Moxee and Prosser, both male and female hop looper moths were captured in traps baited with AAMB in all weeks from the first week of April through October (Figure 1). These numbers were relatively small in the spring (April June), with much higher numbers trapped in July (Figure 1). At Moxee, much higher numbers were seen again in late August into early September (Figure 1A), whereas at Prosser, only a weak increase in numbers of moths trapped was apparent in late August (Figure 1B). Overall, many more hop looper moths were trapped at the Moxee site. From April through September, female hop looper moths captured in traps at Moxee were generally mated (95%, n ¼ 334), with a mean spermatophore number of 1.1 per mated female (n ¼ 316) (Figure 2). Figure 1. Mean ( + SE) numbers of male and female hop looper moths per AAMB trap per week throughout the 2010 field season near Moxee, Yakima County, WA (A) and near Prosser, Benton County, WA (B). Solid bars are male moths trapped and open bars are female moths trapped.

5 186 P.J. Landolt et al. Downloaded by [christelle guedot] at 15:20 22 November 2011 Figure 2. Percentages of females captured in AAMB traps that had been mated (crosshatched bars) or unmated (solid bars), for each month of the growing season. Mating status was assessed by examination of spermatophores in females. Numbers above bars for each month are the numbers of females dissected for that month. Moxee, WA. Mated females possessed either one (85.8%, n ¼ 271), or two (14.2%, n ¼ 45) spermatophores, and none possessed greater than two. Females captured in October however were generally unmated (95%, n ¼ 41) (Figure 2). 4. Discussion These results demonstrate attractiveness of the AAMB lure to both male and female hop looper moths. We interpret the capture of moths in traps to be the result of oriented flight to the odour source within the trap, a form of attraction. This is the first species of Hypena experimentally shown to respond to the AAMB lure, although small numbers of Hypena species were captured previously in traps with the same lure (Landolt et al. 2006; P.J. Landolt unpublished observation). This work follows reports of several other species of moths trapped with the same two compounds (Landolt 2000, 2005; Landolt and Higbee 2002; To th et al. 2010). The comparison of acetic acid, 3-methyl-1-butanol, and the combined AAMB lure showed that neither of the chemicals alone is attractive, and that both chemicals are necessary for trapping of hop looper moths. This finding is similar to that shown for several pest noctuid species (Landolt 2000; Landolt and Higbee 2002) and for the pyralid Pyralis farinalis L. (meal moth) (Landolt 2005). Both sexes of hop looper moths were consistently captured in traps baited with AAMB. This occurred for the test of synergy, but also throughout the field season in commercial hop yards. Again, this finding is similar to that reported for other pest moth species trapped with AAMB lures (Landolt 2000; Landolt and Higbee 2002; To th et al. 2010). Dissection of female moths to determine the presence of spermatophores (as an indicator of mating) showed an interesting pattern. Most females collected April to October were mated, and most females collected in October were unmated, in spite of the trapping of males in October. A somewhat similar pattern was noted by Grasswitz and James (2008) for hop looper moths captured near Prosser in blacklight traps. Throughout the season, most hop looper moths in light traps were mated, with the exception of moths collected in late summer. They interpreted this finding as evidence that unmated females overwinter. Hop looper moths have been found in caves and other sheltered locations during winter months (Kikukawa 1982; Godwin 1987), but there are no assessments of the mating status of female hop looper moths in such sites. The trapping of numbers of females of a pest species such as the hop looper suggests pest management applications that are not possible with most moth sex pheromones which are attractive exclusively to males. Monitoring of females might, for example, provide a better assessment of risk to the crop from the offspring of the subsequent generation, better determination of the timing of egg laying, and/or improved estimates of moth population density, compared to monitoring of males. Such a lure might also be useful in an attract-and-kill formulation to remove females from a population along with their eggs. This approach has been explored and the feasibility tentatively proven for the same lure used against Lacanobia subjuncta

6 (Barnes and McDunnough) as an apple pest (Landolt 2003), and using a floral-based feeding attractant against the alfalfa looper moth Autographa californica (Speyer) (Camelo et al. 2007). The AAMB lure may have potential in an attract-and-kill system for hop looper management. The patterns of captures of hop looper moths in AAMB traps throughout the 2010 season was not inconsistent with that reported by Grasswitz and James (2008) using blacklight traps. However, the numbers of moths trapped and the seasonality of their captures varied considerably between the Moxee and Prosser sites. At this time, we do not know what might have caused these differences. Combined trapping observations (including Grasswitz and James 2008) indicate possibly three flights or generations; one in spring and two in summer. Such a pattern would coincide with larval numbers through the season seen by Grasswitz and James (2008), which also indicated three generations. Our results indicate potential for the AAMB lure to be used in traps for monitoring flight activity and relative abundance of hop loopers in commercial hops yards. However, considerable research would be required to determine appropriate response thresholds or economic injury levels for hop looper, based on captures of moths in these traps. The AAMB lure is attractive to many species of moths, including numbers of crop pests and other nonpest species that can nonetheless be quite abundant. This raises concern over the difficulty of sorting captured moths in order to identify and document those species that are of interest. In the studies we report here, nontarget moths were not counted but were relatively scarce (none to several per trap per week). We suggest that this apparent specificity of the trap and lure for hop loopers was likely due to relatively weed-free conditions of the hop yards and the locations of the traps, which were well located within the hop yards. Placement of feeding attractant traps such as the one reported along field edges and in areas with abundant non-crop vegetation would likely exacerbate the problem of non-target moths being trapped, as indicated by the diversity of moths captured in past studies with this lure in locations with high plant diversity (Landolt and Hammond 2001; Landolt et al. 2006). Acknowledgments Technical assistance was provided by Jewel Brumley, Daryl Green, Marina Meixner, and Marina Mirales. Roy Farms, John I. Haas, Wyckoff Farms, and Olsen Brothers Ranches kindly provided access to their hop yards for the trapping experiments. References Barbour JD Hop looper and bertha armyworm. In: Gent DH, Barbour JD, Dreves AJ, James DG, Parker R, Walsh DB, editors. Field guide to integrated management in hops. 2nd ed. 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New York (NY): Dover Publ. p Hodges RW, Dominick T, Davis DR, Ferguson DC, Franclemont JG, Munroe EG, Powell JA Check List of the Lepidoptera of America North of Mexico. London and the Wedge Entomological Foundation. Washington (DC): E. W. Classey Ltd. p. xxiv þ 284. Howard LO Some insects affecting the hop plant. Bull. US Dept. Agric. New Series. 7: Kikukawa S An overwintering site of the hop looper, Hypena humuli (Harris). Entomol News. 93:108. Lafontaine JD, Schmidt BC Annotated check list of the Noctuoidea (Insecta, Lepidoptera) of North America north of Mexico. ZooKeys. 40: Landolt PJ New chemical attractants for trapping Lacanobia subjuncta, Mamestra configurata, and Xestia c- nigrum (Lepidoptera: Noctuidae). J Econ Entomol. 93: Landolt PJ Lacanobia moths: Why monitor them when you can just kill them? Proc Wash. State Hort Assoc. 98(2002): Landolt PJ Trapping the meal moth, Pyralis farinalis L. (Lepidoptera: Pyralidae) with acetic acid and 3- methyl-1-butanol. 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7 188 P.J. Landolt et al. To th M, Szaruka n I, Dorogi B, Gulya s A, Nagy P, Rozgonyi Z Male and female noctuid moths attracted to synthetic lures in Europe. J Chem Ecol. 36: Utrio P, Erikkson K Volatile fermentation products as attractants for macrolepidoptera. Ann Zool Fennici. 14: Yela JL, Holyoak M Effects of moon light and other meteorological factors on light and bait trap catch of noctuid moths (Lepidoptera: Noctuidae). Environ Entomol. 26: