The behavioral response of Lasioderma serricorne (Coleoptera: Anobiidae) to citronellal, citral, and rutin
© The Author(s) 2016
Received: 21 February 2016
Accepted: 9 June 2016
Published: 21 June 2016
The behavioral response of Lasioderma serricorne adults to citronellal, citral, and rutin was investigated by using the area preference method. The L. serricorne adults were exposed to citronellal, and citral at the rate of 1:10, 1:50, 1:100 and 1:1000 (citronellal: ethanol, v/v) for 1, 2, 12 and 24 h, to rutin at the rate of 10, 30 and 90 g/m2 for 1, 2, 12 and 24 h, respectively. The citronellal and citral had attractive activity at the low rates and repellent potential at the high rates. The highest behavioral response values of L. serricorne adults to citronellal and citral were −88.89 % at the rate of 1:100 and 100.00 % at the rate of 1:50 respectively. Rutin had strong repellent effectiveness on L. serricorne adults, which significantly increased with increasing rates with the highest behavioral response values 100.00 % at the rate of 90 g/m2 after 12 h exposure. These data suggest that the citronellal, citral, and rutin have great potential for preventing stored products from L. serricorne infestation.
The cigarette beetle, Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae) ranks as one of the most serious pests of stored products in the world (Kim et al. 2003). The cigarette beetle was first found in the tomb of Tutankhamun (Alfieri 1931) and Rameses II (Steffan 1982). The earliest records of the cigarette beetle associated with tobacco appeared in France in 1848 (Runner 1919) and in the United States of America in 1886 (Tenhet and Bare 1951). The L. serricorne larvae usually cause damage by eating tobacco and penetrate deep into tobacco mass, resulting in small round holes in the tobacco and its products.
Phosphine has been used for the control of L. serricorne population since 1950s. However, its repeated and intensive use has resulted in serious negative issues including insecticide resistance, insecticide residue, insect resurgence, and lethal effects on non-target organisms (Jovanović et al. 2007). Development and application of environment-friendly control strategies and integrated pest management (IPM) systems have recently been considered to be the only sustainable solution to combat the increasing insecticide-resistant insects (Kim et al. 2003).
Behavioral manipulation is an important insect control method based on insect behavioral responses to special environmental factors. Particularly, the repellents and attractants have been often applied to manipulate insect behaviors, which can effectively prevent crops and stored products from insect infestation. Most of stored product insects, such as Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) (Campbell 2012), Tribolium confusum (Coleoptera: Tenebrionidae) (Athanassiou et al. 2006), Sitophilus granarius (L.) (Coleoptera, Dryophthoridae) (Germinara et al. 2012a, b), Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) (Trematerra et al. 2013), Sitophilus oryzae (Coleoptera: Curculionidae) (Kumar et al. 2004), Ahasverus advena (Waltl) (Coleoptera: Cucujidae) (Wakefield et al. 2005), and Oryzaephilus surinamensis (Coleoptera: Silvanidae) (Mowery et al. 2004) respond preferentially to the volatiles of cereal grains, processed products, or pheromone. Some compounds have been verified to have potent potential as attractants or repellents for practical application.
Citronellal is a monoterpenoid with distinctive lemon scent. Some researches have showed that citronellal has insect repellent properties, especially against mosquitoes (Kim et al. 2005). Citral has a strong sweet lemon odor with strong antimicrobial qualities (Onawunmi 1989), repellent effects against Callosobruchus maculatus (Ke et al. 1992), and pheromonal effect (Robacker and Hendry 1977). Rutin is one of the phenolic compounds found in many plants, including the fruits and rinds of peaches Prunus persica Linn and apples Serica orientalis Motschulsky, especially the tartary buckwheat plant Fagopyrum tataricum Gaertn belonging to family Polygonaceae (Kreft et al. 1999). Some plants containing rutin were used as repellents for preventing the stored products from insect infestation in China (Meng et al. 2003; Yu 2009). However, little is known about the behavioral response of L. serricorne adults to citronellal, citral, and rutin so far. Therefore, the aim of the present work was to evaluate the behavioral response of L. serricorne adults to citronellal, citral, and rutin.
Cultures of the cigarette beetle, L. serricorne, were maintained in the laboratory without exposure to any insecticide at the Institute of Stored Product Insects of Henan University of Technology. They were reared on a sterilized diet (wheatfeed/yeast, 95:5, w/w) at 27 ± 2 °C, 75 ± 5 % relative humidity, and a 12:12 light:dark photoperiod. Healthy, unsexed 3–5-day old adults were randomly chosen for bioassays.
Preparation of the reagents
Citronellal is also called “rhodinal” or “3,7-dimethyloct-6-en-1-al”, and its molecular formula is C10H18O. Citral is also called “3,7-dimethyl-2,6-octadienal” or “lemonal”, and its molecular formula is C10H16O. Rutin’s molecular formula is C27H30O16. Citronellal, citral, and rutin of more than 96 % purity were obtained from Shanghai Jingchun Industry Ltd.
The behavioral response of L. serricorne adults to citronellal, citral, and rutin was evaluated by using the area preference method. Test areas consisted of Whatman No.1 filter paper cut in half (Ф12.5 cm). A series of citronellal or citral was respectively dissolved in ethanol (analytical purity) at the rate of 1:10, 1:50, 1:100 and 1:1000 (citronellal or citral: ethanol, v/v). Then the corresponding 500 µl solution was evenly applied on half-filter paper discs using a micropipette, respectively. The other half of the remaining filter paper was treated with 500 µl ethanol alone and used as a control. The filter papers were air-dried for about 5 min to evaporate the solvent completely and full discs were subsequently remade by attaching treated halves to untreated halves with clear adhesive tape. Each remade filter paper disc was tightly fixed onto the bottom of a petri dish (Ф12.5 cm) daubed with polytetrafluoroethylene (PTFE)on the inside wall to prevent the insects from escaping. For the rutin, the appropriate amount of powder was evenly spreaded on the half filter paper (Ф12.5 cm) according to the rate of 10, 30 and 90 g/m2. The other half of the remaining filter paper was untreated as a control. Twenty unsexed L. serricorne adults were then released at the center of the filter paper disc. The petri dishes were subsequently covered and kept in incubators at 27 ± 2 °C, 75 ± 5 % relative humidity, and a 12:12 light:dark photoperiod.
Each treatment was replicated three times and the number of insects present on the control (Nc) and treated (Nt) areas of the discs was recorded after 1, 2, 12 and 24 h, respectively.
The positive behavioral response value (+) means repellent activity against the L. serricorne adults, and the negative behavioral response value (−) means attractive activity to the L. serricorne adults. The higher absolute value of BRV, the stronger repellent or attractive activity.
The behavioral response value was determined and their absolute values of BRV were transformed to arcsine square-root values before subjecting to two-way analysis of variance (ANOVA) with BRV as response variable, and rate and exposure time as fixed effects. The mean behavioral response values were compared and separated by Scheffe’s test at p = 0.05 level. These analyses were performed using SPSS version 16.0 software.
Behavioral response of L. serricorne adults to citronellal at the rate of 1:10, 1:50, 1:100 and 1:1000 (citronellal: ethanol, v/v) after 1, 2, 12 and 24 h exposure period, respectively
Exposure time (h)
−24.87 ± 3.38c
−53.97 ± 5.23d
−16.93 ± 1.58b
−77.78 ± 7.62b
−88.89 ± 10.99d
−77.27 ± 4.44c
−68.52 ± 3.38c
−81.48 ± 5.26b
5.86 ± 1.89b
8.44 ± 1.31b
22.75 ± 3.51a
27.02 ± 2.83a
52.38 ± 3.91a
52.38 ± 5.91a
25.11 ± 1.85a
44.44 ± 4.44a
Two-way ANOVA analysis for the behavioral response of L. serricorne adults to citronellal at the rate of 1:10, 1:50, 1:100 and 1:1000 (citronellal: ethanol, v/v) after 1, 2, 12 and 24 h exposure period, respectively
Rate × exposure time
Behavioral response of L.serricorne adults to citral at the rate of 1:10, 1:50, 1:100 and 1:1000 (citral: ethanol, v/v) after 1, 2, 12 and 24 h exposure period, respectively
Exposure time (h)
−24.87 ± 3.39c
−53.97 ± 5.23c
−16.93 ± 1.32d
−77.78 ± 2.78c
30.16 ± 1.57b
51.85 ± 1.52b
9.99 ± 4.90c
37.61 ± 3.36b
96.30 ± 3.70a
100.00 ± 0.00a
73.68 ± 6.19a
67.72 ± 5.58a
82.08 ± 4.01a
74.67 ± 4.53ab
48.72 ± 3.71b
27.22 ± 1.48b
Two-way ANOVA analysis for the behavioral response of L. serricorne adults to citral at the rate of 1:10, 1:50, 1:100 and 1:1000 (citral: ethanol, v/v) after 1, 2, 12 and 24 h exposure period, respectively
Rate × exposure time
Behavioral response of L.serricorne adults to rutin at the rate of 10, 30 and 90 g/m2 after 1, 2, 12 and 24 h exposure period, respectively
Exposure time (h)
41.88 ± 4.27a
40.49 ± 1.60b
9.83 ± 3.14b
88.66 ± 3.58a
40.49 ± 1.60a
71.90 ± 5.23a
94.55 ± 3.21a
87.96 ± 7.23a
56.65 ± 5.93a
74.67 ± 4.53a
100.00 ± 0.00a
100.00 ± 0.00a
Two-way ANOVA analysis for the behavioral response of L. serricorne adults to rutin at the rate of 10, 30 and 90 g/m2 after 1, 2, 12 and 24 h exposure period, respectively
Rate × exposure time
The behavioral response of insects to compounds depends on insect species, developmental stages, strains, rates, compound components, application methods and special environmental factors (Kanzaki 1996; Watson and Barson 1996; Fields et al. 2001). Some compounds which can significantly attract insects, particularly sex pheromones, have been developed as attractants for monitoring programs (Burkholder and Ma 1985; Trematerra 2012), or as attracticides (Nansen and Phillips 2004). Some compounds which can significantly repel insects have been developed as repellants for insect disinfestation, especially in insect-resistant packaging. Many materials such as synthetic pyrethroids, citronella, natural botanical antifeedants, (E)-2-hexenal, silicagel, and protein-enriched pea flour have been verified to effectively protect packaging materials against stored product insects and some of them are being applied on packaging materials for their effectiveness against insect penetration (Bloszyk et al. 1990; Wong et al. 2005; Germinara et al. 2012a, b).
The citronellal, citral, and rutin are safe, because they extensively exist in the citrus fruits and other fruit plants which are usually used as cosmetics, flavoring agents and traditional herbal medicines (Onawunmi 1989; Li et al. 2015; Randazzo et al. 2016; Stoldt et al. 2016). The present research results demonstrates that citronellal and citral can greatly attract L. serricorne adults at lower rates, and repel L. serricorne adults at higher rates. Moreover, rutin significantly repels L. serricorne adults. Provided with a proper formulation, rate, and reasonable application strategy, citronella, citral, and rutin may be used to effectively prevent L. serricorne infestations. Meanwhile, the effectiveness of the citronellal, citral, and rutin against L. serricorne larvae deserves to be further investigated in the future, because the L. serricorne larvae usually results in the most serious loss due to their mass feeding and harmful metabolite (Mahroof and Phillips 2014). The effect of L. serricorne adults and larvae long-term contacting the citronellal, citral, and rutin also needs to be researched, because this will affect the behavioral response of L. serricorne adults and larvae.
In summary, citronellal, citral, and rutin have great potential as repellents or attractants for managing L. serricorne adults at suitable formulations and rates in practice, and a proper formulation, rate, and reasonable application strategy for each compound deserves to be further investigated as soon as possible.
JL was the project leader and was responsible for the experimental design and writing the manuscript. SL performed most of the experiments. Both authors read and approved the final manuscript.
This research was supported by the National Research Plan for the High-tech R & D Program during the Twelfth Five-year Plan Period (National 863 plan, No. 2012AA101705-2), Key Technologies R & D Program of the Education Department of Henan Province (No. 16A210017), Basic and Cutting-edge Technology Research Projects of Henan Province (No. 152300410078) and the Collaborative Innovation Center of Grain Storage and Security in Henan Province.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
- Alfieri A (1931) Les insectes de la tombe de Tutankhamun. Bull Soc R Entomol Egypt 15:188–189Google Scholar
- Athanassiou CG, Kavallieratos NG, Trematerra P (2006) Responses of Sitophilus oryzae (Coleoptera: Curculionidae) and Tribolium confusum (Coleoptera: Tenebrionidae) to traps baited with pheromones and food volatiles. Eur J Entomol 103:371–378View ArticleGoogle Scholar
- Bloszyk E, Nawrot J, Harmatha J, Drozda D, Chmielewitz Z (1990) Effects of antifeedants of plant origin in protection of packaging materials against storage insects. J Appl Entomol 110:96–100View ArticleGoogle Scholar
- Burkholder WE, Ma M (1985) Pheromones for monitoring and control of stored-product insects. Annu Rev Entomol 30:257–272View ArticleGoogle Scholar
- Campbell JF (2012) Attraction of walking Tribolium castaneum adults to traps. J Stored Prod Res 51:11–22View ArticleGoogle Scholar
- Fields PG, Xie YS, Hou X (2001) Repellent effect of pea (Pisum sativum) fractions against stored-product insects. J Stored Prod Res 37:359–370View ArticleGoogle Scholar
- Germinara GS, Conte A, Cristofaro AD, Lecce L, di Palma A, Rotundo G, del Nobile MA (2012a) Electrophysiological and behavioral activity of (E)-2-hexenal in the granary weevil and its application in food packaging. J Food Prot 75:366–370View ArticleGoogle Scholar
- Germinara GS, Cristofaro AD, Rotundo G (2012b) Bioactivity of short-chain aliphatic ketones against adults of the granary weevil, Sitophilus granarius (L.). Pest Manag Sci 68:371–377View ArticleGoogle Scholar
- Jovanović Z, Kostić M, Popović Z (2007) Grain-protective properties of herbal extracts against the bean weevil Acanthoscelides obtectus Say. Ind Crop Prod 26:100–104View ArticleGoogle Scholar
- Kanzaki R (1996) Behavioral and neural basis of instinctive behavior in insects: odor-source searching strategies without memory and learning. Robot Auton Syst 18:33–43View ArticleGoogle Scholar
- Ke ZG, Nan YS, Lu LX (1992) Preliminary research on the controlling effects of essential oils against Callosobruchus maculatus. Plant Prot 1:20–21Google Scholar
- Kim S, Park C, Ohh MH, Cho HC, Ahn YJ (2003) Contact and fumigant activity of aromatic plant extracts and essential oils against Lasioderma serricorne (Coleoptera: Anobiidae). J Stored Prod Res 39:11–19View ArticleGoogle Scholar
- Kim JK, Kang CS, Lee JK, Kim YR, Han HY, Yun HK (2005) Evaluation of repellency effect of two natural aroma mosquito repellent compounds, citronella and citronellal. Entomol Res 35:117–120View ArticleGoogle Scholar
- Kreft S, Knapp M, Kreft I (1999) Extraction of rutin from buckwheat (Fagopyrum esculentum Moench) seeds and determination by capillary electrophoresis. J Agric Food Chem 47:4649–4652View ArticleGoogle Scholar
- Kumar PP, Mohan S, Balasubramanian G (2004) Effect of whole-pea flour and a protein-rich fraction as repellents against stored-product insects. J Stored Prod Res 40:547–552View ArticleGoogle Scholar
- Li RY, Wu XM, Yin XH, Long YH, Li M (2015) Naturally produced citral can significantly inhibit normal physiology and induce cytotoxicity on Magnaporthe grisea. Pestic Biochem Physiol 118:19–25View ArticleGoogle Scholar
- Mahroof RM, Phillips TW (2014) Mating disruption of Lasioderma serricorne (Coleoptera: Anobiidae) in stored product habitats using the synthetic pheromone serricornin. J Appl Entomol 138:378–386View ArticleGoogle Scholar
- Meng CY, Guo L, Li YX, Liu DY, Gao WY (2003) Source, application, and extraction methods of rutin. Acad Period Changchun Coll Trad Chin Med (Chin J) 19(2):61–64Google Scholar
- Mowery SV, Campbell JF, Mullen MA, Broce AB (2004) Response of Oryzaephilus surinamensis (Coleoptera: Silvanidae) to food odor emanating through consumer packaging films. Environ Entomol 33:75–80View ArticleGoogle Scholar
- Nansen C, Phillips TW (2004) Attractancy and toxicity of an attracticide for the Indianmeal moth, Plodia interpunctella (Lepidoptera: Pyralidae). J Econ Entomol 97:703–710View ArticleGoogle Scholar
- Onawunmi GO (1989) Evaluation of the antimicrobial activity of citral. Lett Appl Microbial 9:105–108View ArticleGoogle Scholar
- Randazzo W, Jiménez-Belenguer A, Luca S, Perdones A, Moschetti M, Palazzolo E, Guarrasi V, Vargas M, Germanà MA, Moschetti G (2016) Antilisterial effect of citrus essential oils and their performance in edible film formulations. Food Control 59:750–758View ArticleGoogle Scholar
- Robacker DC, Hendry LB (1977) Neral and geranial: components of the sex pheromone of the parasitic wasp, Itoplectis conquisitor. J Chem Ecol 3:563–577View ArticleGoogle Scholar
- Runner GA (1919) The tobacco beetle: an important pest in tobacco products. Bull US Dept Agric 737:49–51Google Scholar
- Steffan JR (1982) Ĺentomofaune de la momie de Rameses II. Annales de la Soc Ent de France 18:531–537Google Scholar
- Stoldt AK, Derno M, Das G, Weitzel JM, Wolffram S, Metges CC (2016) Effects of rutin and buckwheat seeds on energy metabolism and methane production in dairy cows. J Dairy Sci 99:2161–2168View ArticleGoogle Scholar
- Tenhet JN, Bare CO (1951) Control of insects in stored and manufactured tobacco. Bull US Dept Agric 869:1–32Google Scholar
- Trematerra P (2012) Advances in the use of pheromones for stored-product protection. J Pest Sci 85:285–299View ArticleGoogle Scholar
- Trematerra P, Ianiro R, Athanassiou CG, Kavallieratos NG (2013) Behavioral responses of Sitophilus zeamais Motschulsky adults to conditioned grain kernels. J Stored Prod Res 53:77–81View ArticleGoogle Scholar
- Wakefield ME, Bryning GP, Collins LE, Chambers J (2005) Identification of attractive components of carob volatiles for the foreign grain beetle, Ahasverus advena (Waltl) (Coleoptera: Cucujidae). J Stored Prod Res 41:239–253Google Scholar
- Watson E, Barson G (1996) A laboratory assessment of the behavioural responses of three strains of Ovyzaephilrcs surinamensis (L.) (Coleoptera: Silvanidae) to three insecticides and the insect repellent N,N-diethyl-m-toluamide. J Stored Prod Res 32:59–67View ArticleGoogle Scholar
- Wong KY, Signal FA, Campion SH, Motion RL (2005) Citronella as an insect repellent in food packaging. J Agric Food Chem 53:4633–4636View ArticleGoogle Scholar
- Yu HY (2009) Survey of preventing stored product insects from infesting archives in ancient China. Lantai World (Chin J) 1:49–50Google Scholar