Responses of Stored-Product Anobiidae to Pheromone Lures and Plant-Derived Volatiles R

J. Appl. Entomol.

Responses of stored-product Anobiidae to pheromone lures and plant-derived volatiles R. M. Mahroof1 & T. W. Phillips2

1 Department of Biological and Physical Sciences, South Carolina State University, Orangeburg, USA 2 Department of Entomology, Kansas State University, Manhattan, USA

Keywords Abstract Lasioderma serricorne, Stegobium paniceum, Anobiidae, attractant, Coleoptera, host odour, Experiments were conducted in different locations to investigate trapping responses of adult Stegobium paniceum and Lasioderma serricorne (Col., An- obiidae) to different commercially available or prototype fabrications of Correspondence their female-produced sex pheromones. The results showed that the Rizana M. Mahroof (corresponding author), number of S. paniceum captured in traps baited with the commercially Department of Biological and Physical available lures was signiﬁcantly higher than those captured in traps bai- Sciences, South Carolina State University, 300 College Street NE, Orangeburg, SC 29117, ted with the prototype stegobinone lures. The three commercially avail- USA. E-mail: [email protected] able brands of serricornin lures investigated were equally effective in capturing L. serricorne. In a related study, we conducted a 9-week trap- Received: June 25, 2007; accepted: October ping experiment to determine if responses of L. serricorne to serricornin 24, 2007. can be enhanced by the presence of host plant odours. Traps were baited with serricornin alone, serricornin plus dried red chilli (Capsicum doi: 10.1111/j.1439-0418.2007.01251.x frutescens L.) or red chilli alone. The results showed that the number of beetles captured in traps baited with a combination of serricornin and chilli volatiles were signiﬁcantly higher than in traps baited with pheromone or chilli volatiles alone, indicating that potential exist for improved monitoring or mass trapping of L. serricorne by combining pheromone with plant-derived volatiles present in Capsicum spp.

system that provides information on species and Introduction density of insects, foci of infestation, routes of insect The drugstore beetle, Stegobium paniceum (L.) (Col., entry and changes in pest population over time Anobiidae) and the cigarette beetle, Lasioderma serri- (Burkholder 1990; Mueller et al. 1990; Phillips corne (F.) (Col., Anobiidae), are major pests on a 2006). Synthetic pheromones are commonly used as wide variety of dry and durable stored agricultural lures in traps to monitor insect activities, to detect products (Howe 1957; Lefkovitch 1967; Bry et al. the presence of infestations, to estimate population 1974; Brar and Chahal 1980; Kohno et al. 1983; densities and to determine treatment efﬁcacy. The Jacob and Ushakumary 1991). These two stored- sex pheromone of S. paniceum, stegobinone [2,3-di- product Anobiidae are found throughout the tropical hydro-2,3,5-trimethyl-6-(1-methyl-2-oxobutyl)-4H- and subtropical parts of the world, and thrive well in pyran-4-one] (Kuwahara et al. 1975) and the warm buildings in temperate countries (Powell 1931; sex pheromones of L. serricorne, anhydroserricor- Howe 1957; Lefkovitch 1967). Challenges in utilizing nin (2,6-diethyl-3,5-dimethyl-3,4-dihydro-2H-pyran) currently available management practices for these and serricornin (4,6-dimethyl-7-hydroxynonan-3- insect pests, such as resistance development to one) (Burkholder 1970) are produced by adult methoprene (Benezet and Helms 1994) and phos- females and responded to by adult males. Synthetic phine (Zettler and Keever 1994) in L. serricorne, war- L. serricorne pheromone lures are widely used for rant more effective pest management approaches. detecting hidden infestations in dry food-processing The foundation to a successful integrated pest man- facilities, warehouses, retail and grocery stores, and agement programme is an effective monitoring other dry storages (Faustini 1985; Mueller et al.

J. Appl. Entomol. 132 (2008) 161–167 ª 2008 The Authors Journal compilation ª 2008 Blackwell Verlag, Berlin 161 Evaluation of attractants for stored-product Anobiidae R. M. Mahroof and T. W. Phillips

1990; Phillips et al. 2000; Campbell et al. 2002; Pa- supply stores belonged to the same retail chain, were padopolou and Buchelos 2002; Arbogast et al. 2003; similar in product layout, but differed in floor Nansen et al. 2004). Unlike synthetic L. serricorne dimension. In pet store 1, in addition to the main pheromone lures, commercial fabrications of S. pani- store floor area (1263.5 m2 with a ceiling height of ceum are less available because of challenges posed 10.7 m), a storage area (995.0 m2 with a ceiling by the lack of an effective or high-quality procedure height of 10.7 m) was present to the south of the for synthesizing stegobinone. building. Two entrance doors were located to the Host volatiles can play a major role in affecting west and north of the building and two windows behaviour of both male and female insects as direct were present to the north and west of the main store attractants, oviposition stimulants or as potential area. To the south of the storage area was a loading synergists to sex and aggregation pheromones. The dock garage door. Pet store 2 (1467.9 m2 with a ceil- phenomenon of combining host-related volatiles and ing height of 10.7 m) had two separate storage areas synthetic pheromones to improve potency of attrac- (83.6 m2 and 557.4 m2), with a main door to the tants used in traps have been well documented in south and the dock door to the east and no win- several bark and sap beetles (Lin et al. 1992; Landolt dows. and Phillips 1997), but studies on the synergistic Flight activity of S. paniceum was monitored using effects of pheromones and host-related volatiles in four Allure diamond sticky trapsTM (Whitmire stored-product insects have not received much Micro-Gen Labs, St Louis, MO). An Allure trapTM attention (Chambers 1990). Plant-derived volatiles has diamond-shaped openings at both ends, has have been used in limited occasions, as a bait to a sticky interior surface (140 cm2) with a dimension monitor stored-product insect population densities of 15.0 · 18.0 cm. Traps were baited with the phero- (Phillips 1997). A recent report by Mahroof and mone lures CSP1-type1, CSP1-type2, CSP1-type3 Phillips (2007) showed that adult L. serricorne were and CSP2, which are different fabrications of stegobi- strongly attracted to volatiles from dried chilli pepper none, the female-produced sex pheromone of S. pa- (Capsicum frutescens L.). We are, however, unaware niceum. Type1, type2 and type3 versions of CSP1 of any published report on the synergistic effect of represent low, medium and high pheromone con- combining plant-derived volatiles with serricornin centrations respectively. The release formulations of on trapping L. serricorne. the code-numbered lures are provided in table 1. Our goals in this study were to determine the relative efficacy of commercially available or prototype fabrications of pheromone lures for S. paniceum and Table 1 Various synthetic sex pheromones for stored-product Anobii- L. serricorne, and to investigate if the efficacy of dae showing their release methods L. serricorne lures can be enhanced when combined with host-derived volatiles. The brands of commer- Insect Lure cial S. paniceum and L. serricorne lures used in the species designation Release methods Comments study were selected based on their availability and cost-effectiveness. The prototype lures were used in Stegobium CSP1 Rubber septa with Product under the study in order to evaluate the optimal dosage of paniceum absorbed pheromone development CSP2 Pheromone reservoir Commercially stegobinone or serricornin required to develop an releasing through available efficient lure. permeable membrane Lasioderma CLS 1 Rubber septum with Commercially serricorne absorbed pheromone available Materials and Methods CLS 2 Polyethylene vial Commercially releasing through available Trapping S. paniceum using different commercially permeable wall fabricated stegobinone CLS 3 Pheromone reservoir Commercially releasing through available The study was conducted in two retail pet supply permeable membrane stores for eight continuous weeks from November to CLS 4 Rubber septa with Laboratory made, December 2005. Most of the products sold in these absorbed pheromone technical grade stores were feed for cats, dogs, small animals and serricornin birds, and these stores were infested with different CLS 5 Rubber septa Product under stored-product insect pests, including S. paniceum, with absorbed development pheromone before the study was conducted. The two retail pet

J. Appl. Entomol. 132 (2008) 161–167ª 2008 The Authors 162 Journal compilation ª 2008 Blackwell Verlag, Berlin R. M. Mahroof and T. W. Phillips Evaluation of attractants for stored-product Anobiidae

Pheromone lures used in all experiments were Within this space an inner room (9.8 m2) was within the active production period and had not located which was separated by two side walls and passed shelf-life. Each trapping site was divided into a door. Trapping was conducted using Storgard Thin- four blocks. Five traps were randomly deployed in line (Treće´), a rectangular-shaped sticky trap each block, of which four of the traps were baited designed for trapping L. serricorne. The trap measures with pheromone lures and the fifth was without 17.5 · 16 · 1.5 cm with an adhesive panel of a lure (control), giving a total of 20 traps per store. 150 cm2. The trap is suitable for hanging on ropes or The traps were suspended vertically on a string, placing underneath shelves, and is opened on three 1.8 m above the ground level, about 2 m between sides of the rectangle for insect entry. To evaluate the traps, and 3.0 m from the side walls, and placed the responses of L. serricorne to three commercially in such a way as to minimize interference from cus- fabricated serricornin lures (CLS1, CLS3 and CLS4) tomers and store personnel. Traps were checked and the fourth lure under development by the man- every 2 weeks during which the number of S. panice- ufacturer (CLS5; table 1), a randomized complete um captured were recorded. Pheromone lures and block design was used with five blocks (replicates). traps were replaced every 4 weeks. A preliminary Lure type CLS5 had three different concentrations statistical analysis was conducted using anova to test that were labelled as type1, type2 and type3 repre- for differences in distributions of the trapping data senting low, medium and high pheromone concen- between the two retail pet supply stores. The result trations respectively. The CLS2 lure was not showed that the number of beetles captured did not included in this experiment because of inadequate differ significantly between the sites. Thus, data from availability of lures. A trap without lure (blank trap) the two sites were pooled in subsequent statistical served as control. In each block, six traps with the analyses. different commercial pheromones and a blank trap were placed on the floor randomly, on a line, 1.5 m from each other and 2 m away from the walls. Four Trapping L. serricorne using different commercially blocks were deployed in the main area of the base- fabricated serricornin ment and the fifth block was the smaller inner room Two trapping experiments were carried out. The first located within the basement. was conducted from August to October 2005 in Laboratory-reared L. serricorne were released in the a multipurpose room at the Stored Products sites to establish populations for the trapping experi- Research and Education Center (SPREC) (3607¢N; ments. Details of the protocol used for rearing 09708¢W) at Oklahoma State University. The room L. serricorne used in this and subsequent experiments measured 8.5 m in length, 13.5 m in width and are provided in a previous report (Mahroof and Phil- a height of about 6.5 m. Trapping was carried out lips 2007). To establish L. serricorne population for using the Storgard II sticky traps (Treće´, Adair, trapping, we placed two jars containing different life OK), designed to capture flying insects with stages of L. serricorne placed in two randomly selected a 14.0 · 10.5 cm adhesive panel and diamond- locations, halfway between the traps and 2 m away shaped openings in either side. The room was from the walls. Each jar contained approximately divided into five blocks, with a minimum of 8 m 200 adult L. serricorne. Insect jars were replaced with between blocks. Four traps were randomly a fresh colony twice during the experiment, after 3 positioned in each block, of which three traps were and 6 weeks from the beginning of the experiment. baited with different commercial pheromone fabri- The traps were inspected weekly and the number of cations hereby designated as CLS1, CLS2 and CLS3 L. serricorne caught was recorded. The traps were (table 1). The fourth trap was left blank (control), monitored for 9 weeks during which time traps with giving a total of 20 traps per week. The traps were pheromone lures were rotated weekly to different suspended vertically on a string, 1.7 m above the positions, and traps were replaced every 3 weeks. ground level, at a distance of 2.0 m from the wall, Two HOBO data-logging units (Onset Computer and 1.5 m between each trap. Corporation, Bourne, MA) were used to measure A second L. serricorne trapping experiment was environmental conditions at SPREC and ASB. One conducted in the Animal Science Building (ASB) light bulb (750 W; high-pressure sodium lamp) was (3607¢N; 09705¢W) at Oklahoma state University kept illuminated throughout the day and night in from August to October 2005. The trapping was con- the multipurpose room at SPREC in order to comply ducted in the basement of a two-storey building, with the OSU safety requirements. The basement of measuring 21.6 m long, 16.5 m wide and 3.3 m tall. ASB was kept totally dark except when the traps

J. Appl. Entomol. 132 (2008) 161–167 ª 2008 The Authors Journal compilation ª 2008 Blackwell Verlag, Berlin 163 Evaluation of attractants for stored-product Anobiidae R. M. Mahroof and T. W. Phillips were checked and serviced weekly. The mean tem- treatments and two controls arranged randomly. perature, relative humidity (RH), and light intensity Traps were suspended vertically on a string, 1.7 m (LI) at SPREC averaged from two HOBO units for off the floor and at a distance of 2.0 m from the side 9 weeks were 30.0 Æ 0.1C, 52.3 Æ 0.5%, walls, with about 1.5 m between traps. Laboratory- 5.4 Æ 2.0 lux (n = 761) respectively. Mean tempera- reared L. serricorne were released every 3 weeks, as ture and RH at ASB during the study period were described above. Traps were checked every week at 26.0 Æ 0.1C and 56.6 Æ 0.1% respectively. which time the number of insects caught per trap was recorded, and each trap rotated clockwise. All lures and traps were replaced every 3 weeks. In the Responses of L. serricorne to pheromone and host-plant statistical analysis we included only 6 weeks of trap volatiles catch data. Data from week 5, 7 and 9 were not Experiments were also conducted at SPREC from Jan- included in the analyses because trap catches were uary to March 2006 to investigate responses of nil during these 3 weeks. Mean temperature and RH L. serricorne to Storgard II sticky traps baited with during the study period were 27.3.0 Æ 0.4C pheromone lures alone, pheromone plus host-plant (n = 750) and 50.6 Æ 0.3% (n = 750) respectively. volatiles or host-plant volatiles alone. The plant Mean LI was 5.3 Æ 1.8 lux (n = 761). materials used in the study was dried red chilli (C. frutescens, Dicotyledon: Solanaceae; Bolner’s Fiesta Statistical analyses Product Inc., San Antonio, TX). There were six experi- mental treatments: the first consisted of traps baited Experiments were conducted as randomized complete with 1 mg of synthetic pheromone lures alone. The block design, with lure types serving as treatments lures used in the study were fabricated in our labora- and replications serving as blocks. Data from each tory. Briefly, synthetic serricornin (nonan-3-one, 4-6- block within two trapping weeks for S. paniceum and dimethyl-7-hydroxy; 95% pure; Bedoukian Research, within a trapping week for L. serricorne were pooled Inc., Danbury, CT) was diluted in double-distilled prior to analyses. Time (weekly or biweekly record- hexane (Reagent grade ACS; Pharmco, Brookfield, ings) was considered as a random effect and treat- CT) to a final concentration of 0.2 mg/ll, of which ments as fixed effects. Prior to data analysis, count

5 ll of the pheromone solution was impregnated into data were transformed to log10(X + 1) scale to satisfy rubber septa (No. 11.5; Fisher, Pittsburgh, PA). The the assumption of normality and homogeneity of var- rubber septa were first cleaned by soaking in hexane iance (Zar 1984). Data were subjected to anova by for 12 h, then in dichloromethane for 12 h, and then using the mixed procedure of sas (SAS Institute drying in a fume hood for 24 h. The second treatment 2003). lsmeans were used for separating treatment consisted of traps baited with 5 g of ground dried red mean values at a = 0.05 level. Actual mean values chilli packed in a plastic meshed pouch (5 cm long, and SEMs are presented in the text and figures. 3.7 cm wide and 3.0 mm mesh). Chilli peppers were pulverized with a mechanical grinder, and sifted using Results an 850-lm meshed sieve (U.S. No. 20; Seedburo Equipment Co., Chicago, IL). In a third treatment, we Trapping S. paniceum using different commercially fab- applied 5 ml of filtered chilli extracts, at a concentra- ricated stegobinone tion of 1 g equivalent per ml of hexane, to a no. 3 cotton dental roll (3.75 cm long and 1.25 cm wide) (Tidi Significant differences (F = 5.49; d.f. = 4, 14; Brand, Neenah, WI). The impregnated dental wicks P = 0.0072) were observed between mean number of were placed in the middle floor of the sticky traps. The S. paniceum catches in traps comprising various chilli extracts used in the study were extracted with treatments in the retail pet stores. With the exception double-distilled n-hexane as described by Mahroof of CSP2, the number of S. paniceum captured in traps and Phillips (2007). The fourth and fifth treatments baited with any of the three types of CSP1 lures was consisted of traps baited with 5 g of chilli powder plus similar to observations in unbaited traps (fig. 1). 1 mg of synthetic serricornin and traps baited with 5 ml of chilli extract plus 1 mg serricornin respec- Trapping L. serricorne using different commercially tively. Blank traps and traps baited with wicks loaded fabricated serricornin with 5 ml of n-hexane served as controls. Traps were arranged in a randomized complete Significant differences (F = 4.6; d.f. = 3, 31; P = block design with four blocks, each consisting of five 0.0089) were observed between number of

J. Appl. Entomol. 132 (2008) 161–167ª 2008 The Authors 164 Journal compilation ª 2008 Blackwell Verlag, Berlin R. M. Mahroof and T. W. Phillips Evaluation of attractants for stored-product Anobiidae

18 35 a 16 30 a 14 25 12 20 10 8 15 a a L. serricorne S. paniceum 6 10 4 Mean (+ SE) number of Mean (+ SE) number of 5 2 b b b b b 0 0 Blank CLS1 CLS2 CLS3 Blank CSP2 Fig. 2 Mean number (ÆSE) of adult L. serricorne captured at the Stored Products Research and Education Center at Oklahoma State CSP1 type 1 CSP1 type 2 CSP1 type 3 University in traps baited with different commercial fabrications of Fig. 1 Mean number (ÆSE) of adult S. paniceum captured in retail pet serricornin. Mean values were based on n = 9. Mean numbers with supply stores in traps baited with different commercial fabrications of different letters are signiﬁcantly different (P £ 0.05, LS means). stegobinone. Mean values were based on n = 4. Mean numbers with different letters are signiﬁcantly different (P £ 0.05, LS means).

18 a 16 L. serricorne captured in the pheromone traps com- 14 pared with the blank traps at SPREC. Pheromone- 12 baited traps captured, on average, eight times more ab 10 a L. serricorne than the blank traps (ﬁg. 2). However, the number of beetles captured in traps baited with 8 ab ab

L. serricorne 6 CLS1, CLS2 or CLS3 was not signiﬁcantly different b (P > 0.05) from each other. Similar to observations 4 Mean (+ SE) number of at SPREC, the number of L. serricorne captured at 2 c ASB were signiﬁcantly (F = 8.4; d.f. = 6, 55; 0 P = 0.0001) higher in pheromone-baited traps than CLS1 CLS3 CLS4 in blank traps. The results also showed that traps Blank baited with CLS5 type1 and CLS type 3 captured the

highest and lowest numbers of L. serricorne, respec- CLS5 type 1 CLS5 type 2 CLS5 type 3 tively; and trap catches between these two lure types Fig. 3 Mean number (ÆSE) of adult L. serricorne captured at the Ani- were significantly different from each other (fig. 3). mal Science Building at Oklahoma State University in traps baited with different commercial fabrications of serricornin. Mean values were Responses of L. serricorne to pheromone and host-plant based on n = 9. Mean numbers with different letters are significantly different (P £ 0.05, LS means). volatiles The trapping experiment conducted at SPREC combining pheromones with host odours showed signifi- Discussion cant differences (F = 4.21; d.f. = 6, 30; P = 0.0034) among treatments (fig. 4). Traps baited with serricor- We noted significant variation in the efficacy of nin plus red chilli volatiles captured about three to S. paniceum lures that are commercially available or four times more beetles than traps baited with pher- products that are in the process of development. omone or chilli volatiles alone. An average of one to CSP2 is a relatively better lure to trap S. paniceum two beetles per week were captured in traps baited because of the relatively high number of adults with pheromone, chilli powder or chilli extract caught in traps with CSP2. If the pheromone lures alone. Statistical analysis confirmed that the number are attractive, then lures draw insects from of L. serricorne captured was not significantly differ- a distance, and insects will be trapped rather rapidly ent (P > 0.05) among the three treatments. in high numbers. It is noteworthy to state that only

J. Appl. Entomol. 132 (2008) 161–167 ª 2008 The Authors Journal compilation ª 2008 Blackwell Verlag, Berlin 165 Evaluation of attractants for stored-product Anobiidae R. M. Mahroof and T. W. Phillips

5 Results from the experiments in which we baited a traps with synthetic serricornin alone, pheromone 4 ab plus volatiles from red chilli, or chilli volatiles alone showed that traps baited with pheromone plus chilli 3 volatiles were signiﬁcantly more attractive to L. serricorne than traps baited with synthetic pheromone or bc chilli volatiles alone. To our knowledge this is the 2 bc

L. serricorne ﬁrst published report indicating a synergistic effect of bc 1 synthetic pheromone and plant volatiles. These ﬁnd- Mean (+ SE) number of ings could help complement the current manage- c c 0 ment programme for L. serricorne by exploiting the synergistic effects of combining synthetic pheromones with plant-derived volatiles to improve mass Blank trapping of the pest or to improve the sensitivity of n-hexane Pheromone Chili extract the trap. Greater trapping sensitivity might be more Chili powder of an advantage when chances of catching insects are low. The use of an attractant in traps most often improves trap performance by increasing the chance Pheromone+chili extract

Pheromone+chili powder of detecting low-density insect infestations, e.g. in localities where the pest has not yet established itself Fig. 4 Mean number (ÆSE) of adult L. serricorne captured at the and the population is still low or where the insect Stored Products Research and Education Center at Oklahoma State University in traps baited with serricornin alone, Capsicum products activity is suspected but not yet detected. In this sit- alone, or in combinations. Mean values were based on n = 6. Mean uation an improved pheromone lure by combining numbers with different letters are significantly different (P £ 0.05, LS a host plant-derived volatile may substantially means). increase the chances of detecting L. serricorne. Our results showed further that, specifically the chilli extract when combined with the pheromone, was very few brands of commercially fabricated stegobi- more attractive than the chilli powder alone or chilli none are currently available in the market for moni- extract alone, and suggest that traps with host mate- toring and as a result monitoring and trapping of rials extracted with a suitable solvent to concentrate S. paniceum are relatively limited when compared volatile compounds, and then combined with the with L. serricorne monitoring. pheromone may be a alternative than the fresh host Our studies showed that commercial pheromone materials or their extracts alone. lures from different manufacturers, or lures made in In summary, our studies clearly showed that vari- our laboratory using the technical grade serricornin, ous types of lures loaded with serricornin are attrac- are effective in monitoring populations of L. serricor- tive to L. serricorne, but not all lures loaded with ne. Synthetic serricornin used by different manufac- stegobinone are attractive to S. paniceum. There is turers seems equally attractive for a given type of potential for improving lures for S. paniceum, and for trap design. Variations observed in response of gaining improved trap sensitivity for L. serricorne by L. serricorne to sex pheromone lures between SPREC combining host volatiles like those from Capsicum and ASB may be due to variations in the trap spp. designs, beetle populations released, or environmental conditions experienced between the two loca- Acknowledgements tions. Movement and flight of insects were influenced by the indoor ambient temperature, rela- We acknowledge several commercial vendors for tive humidity conditions and light availability (Hag- providing Anobiidae sex pheromone lures and traps, strum et al. 1996; Trematerra and Sciarretta 2004), and appreciate Margie D. Barton for her technical and therefore variation in ambient conditions at assistance during the S. paniceum trials. We thank SPREC and ASB may have affected the trap catches Drs Xingwei Hou and Carmen Greenwood for their between the two experiments. comments on the earlier draft of this manuscript. It is a known fact that the efficacy of pheromone We specially acknowledge two anonymous reviewers lures may be enhanced by combination with host for their constructive comments to improve this odours (Chambers 1990; Landolt and Phillips 1997). manuscript.

J. Appl. Entomol. 132 (2008) 161–167ª 2008 The Authors 166 Journal compilation ª 2008 Blackwell Verlag, Berlin R. M. Mahroof and T. W. Phillips Evaluation of attractants for stored-product Anobiidae

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