- Email: [email protected]
Evaluation of chrysanthemum flower model trap to attract two Frankliniella thrips (Thysanoptera: Thripidae)
Journal of Asia-Pacific Entomology 11 (2008) 171–174
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j a p e
Short Communication
Evaluation of chrysanthemum flower model trap to attract two Frankliniella thrips (Thysanoptera: Thripidae) Bishwo Prasad Mainali, Un Taek Lim ⁎ School of Bioresource Sciences, Andong National University, Andong 760-749, Republic of Korea
a r t i c l e
i n f o
Article history: Received 19 May 2008 Revised 2 July 2008 Accepted 3 July 2008 Keywords: Frankliniella occidentalis Frankliniella intonsa Artificial flower Visual attraction Yellow sticky trap
a b s t r a c t Frankliniella occidentalis Pergande and F. intonsa Trybom (Thysanoptera: Thripidae) are anthophilous insect pests of many crops worldwide. We evaluated a flower model trap mimicking the chrysanthemum flower as a new method to attract the thrips in the laboratory and a strawberry greenhouse. Both choice and no-choice tests in the laboratory showed that the chrysanthemum flower model trap attracted significantly more adult F. occidentalis and F. intonsa compared to yellow sticky trap. Up to 4.1 times more of F. occidentalis and 5.4 times more of F. intonsa were caught in the flower model trap in the strawberry greenhouse. The flower model trap would be a good addition to the integrated thrips management, although at present it is more expensive than the yellow sticky trap. © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2008 Published by Elsevier B.V. All rights reserved.
Introduction Frankliniella occidentalis Pergande and F. intonsa Trybom (Thysanoptera: Thripidae) are ubiquitous, polyphagous pests of vegetables, fruits and ornamental crops. Direct feeding as well as tospovirus transmission by the thrips causes economic loss worldwide (Lewis, 1997; Nagata and Peters, 2001). In particular, F. occidentalis has become a serious pest in numerous crops such as pepper, cucumber, and strawberry in Korea since the thrips was first found in Jeju island in 1993 (Lee et al., 2001). Thrips are difficult to control due to their high reproductive rate, cryptic habit, and resistance to many insecticides (Jacobson, 1997; Herron and James, 2005). As an approach that can integrate various thrips control tactics, use of trap crops has been suggested (Yudin et al., 1988; Pearsall, 2000; Buitenhuis and Shipp, 2006; Matsuura et al., 2006; Shelton and Badenes-Perez, 2006). Trap crops are defined as plant stands that are deployed to attract, divert, intercept, and/or retain targeted insects or the pathogens they vector in order to reduce damage to the main crop (Shelton and Badenes-Perez, 2006). Therefore, it distracts the pests from locating the main crop, resulting in less damage and concentrating them into the trap crop where they can be more effectively controlled (Shelton and Badenes-Perez, 2006; Cook et al., 2007). Adult F. occidentalis and F. intonsa preferentially orient toward and land on flowering plants though they may feed on non-flowering plants (Yudin et al., 1988; Vernon and Gillespie, 1990; Blumthal et al., 2005). Based on the observations of thrips behavior, Yudin et al. (1988) suggested flower-
⁎ Corresponding author. Fax: +82 54 823 1628. E-mail address: [email protected] (U.T. Lim).
ing weeds as trap crops for the management of F. occidentalis in lettuce, which does not flower under normal cultivation practices. Blumthal et al. (2005) investigated flower preference of F. occidentalis using four different colored flowers and suggested the yellow transvaal daisy as a potential trap crop. Buitenhuis and Shipp (2006) used flowering chrysanthemum as a trap crop to attract and retain F. occidentalis in a potted chrysanthemum greenhouse. However, the flowers of trap crop may supplement nutrition for dispersing thrips that would re-colonize the main crop. Therefore, quick removal of flowering trap crop from the greenhouse is needed before the buildup of the thrips population (de Jager et al., 1993; Buitenhuis and Shipp, 2006). Shelton and Badenes-Perez (2006) discussed other limitations of trap cropping such as cost of setting aside land for trap crop and species specificity. To reduce the potential risks and/or costs implemented by using a real flowering plant as a trap crop, we suggest using a chrysanthemum flower model, a stem of sticky artificial flower mimicking yellow chrysanthemum flower, as a new method to trap anthophilous thrips. The trap was evaluated on two thrips, F. occidentalis and F. intonsa, by comparing with a commonlyused yellow sticky trap in the laboratory and a commercial strawberry greenhouse. Materials and methods Rearing of thrips Both F. occidentalis and F. intonsa were collected from a strawberry greenhouse located in Songchun, Andong, Korea in 2006 and were reared in a plastic container (24 cm × 17 cm × 8 cm) with a lid having two holes (diameter = 6 cm) covered with fine mesh fabric (196 mesh
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2008 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.aspen.2008.07.003
172
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
count, Saatilene Hitech, Zurich Co., Como, Italy) at the center. Thrips were provided with leaves of red kidney bean plants, Phaseolus vulgaris L., as a food source. Eight excised stems with cotyledonous leaves were rooted on water-soaked cotton. A mixture of pure honey and pine tree pollen was streaked along the main vein of each leaf by using a paint brush. The container was kept at 28°C and 16: 8 (L: D)h photoperiod in a growth chamber, and water was added daily during the rearing period. Thirty newly emerged adult thrips were transferred to a new plastic container with the food sources for the reproduction of the next generation. Design of chrysanthemum flower model trap Artificial yellow chrysanthemum flowers (45009A, International Artificial Flowers Co., Kimhae, Korea) were modified as a flower model trap. Details of designing the flower model trap is described in Mainali and Lim (2008). Choice tests (flower model trap vs. yellow sticky trap) For each thrips species of F. occidentalis and F. intonsa, 60 adult females were released on red kidney bean with cotyledonous leaves grown on a pot (10 cm×12 cm) inside an acrylic cage (30 cm×30 cm×30 cm). The cage was ventilated through windows on three sides covered with mesh fabric was incubated at 28 °C in the growth chamber. After the acclimatization of the released adult thrips for 2h, the flower model trap and a yellow sticky trap were placed opposite to each other, both facing toward the kidney bean plant at an equal distance from the plant. The height of traps was maintained just above the leaves. Five replications were made
Fig. 2. Mean number of F. occidentalis (FO) and F. intonsa (FI) trapped by flower model trap (FMT) and yellow sticky trap (YST) in a strawberry greenhouse. Sampling was replicated twice for the periods of 30 April–3 May (A) and 10 May–13 May (B). See text for statistics.
for each thrips species. Number of adult thrips caught was counted daily for the period of 1 week. No-choice tests In no-choice test, each flower model trap or yellow sticky trap was placed lateral to a red kidney bean plant in the acryl cage. Same experimental conditions as described in the choice test were provided. Fifty adult females of each thrips species were released and the number of adult thrips caught was counted daily for a period of 1 week. For each thrips species this procedure was replicated five times. Comparisons in greenhouse
Fig. 1. Number of thrips trapped by flower model trap (FMT) and yellow sticky trap (YST) for 1 week at 28 °C in a growth chamber. See text for statistics.
Comparisons between the flower model trap and the yellow sticky trap were conducted in a commercial strawberry greenhouse at Songchun, Andong. The greenhouse (74 m × 7.5 m) was divided into 35 plots each measuring 1 m × 10 m, and from those, 20 plots were randomly chosen. One flower model trap and one sticky trap were placed at a distance of 1.2m apart facing each other in the center of the selected plot. The comparison tests were conducted twice from 30 April to 3 May and from 10 May to 13 May in 2007. Both the flower model traps and the yellow sticky traps were collected after 3 days and brought to the laboratory for the identification of the adult thrips caught. The adult thrips caught in the sticky surface were extracted by using xylene and ethylene glycol and identified under a stereomicroscope according to Mound and Kibby (1998).
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
Statistical analyses Numbers of thrips caught on the flower model trap and the yellow sticky trap were compared between F. occidentalis and F. intonsa using an extension of the Kruskal–Wallis ranks test proposed by Scheirer (1976). Data from the strawberry greenhouse were analyzed with a paired t-test. Results Choice tests The flower model trap attracted 2.6 and 3.2 times more adult thrips compared to the yellow sticky trap for F. occidentalis and F. intonsa, respectively (H = 12.360, d.f. = 1, 19, P = 0.0004; Fig. 1). Daily mean numbers of F. occidentalis caught were 4.3 in the flower model trap and 1.6 in the yellow sticky trap while those of F. intonsa were 2.2 and 0.7, respectively. Significant difference in attractiveness between the two species was also found (H = 4.321, d.f. = 1, 19, P = 0.0376), although no interaction between the trap kinds and thrips species was found (H = 0.006, d.f. = 1, 19, P = 0.9397). No-choice tests No-choice tests also showed higher numbers of adult thrips on the flower model trap compared to the yellow sticky trap (H = 13.720, d.f. = 1, 19, P = 0.0002), even though we found no differences between the two thrips species in the number of adult thrips attracted to traps (H = 3.571, d.f. = 1, 19, P = 0.0588) and no interaction between trap type and thrips species (H = 0.006, d.f. = 1, 19, P = 0.9397) (Fig. 1). The flower model trap attracted 1.7 and 1.8 times more adult thrips compared to the yellow sticky trap for F. occidentalis and F. intonsa, respectively. Daily mean numbers of F. occidentalis caught were 5.4 in the flower model trap and 3.2 in the yellow sticky trap while those of F. intonsa were 4.0 and 2.3, respectively. Comparisons in greenhouse In the first trial when the thrips population was low in the greenhouse, the flower model trap caught more adult thrips than the yellow sticky trap (F. occidentalis t =3.149, d.f. = 9, P = 0.0053; F. intonsa t = 2.800, d.f. = 19, P = 0.0114; Other unidentified thrips t = 6.097, d.f. = 19, P b 0.0001; Fig. 2A). The total number of adult F. occidentalis and F. intonsa caught by the flower model trap was about 2.1 and 4.1 times higher than that caught by the yellow sticky trap, respectively. The proportion of female F. occidentalis and F. intonsa caught was 0.40 and 0.42 on the flower model trap and 0.29 and 0.25 on the yellow sticky trap, respectively. In the second trial the flower model trapped adult F. occidentalis and F. intonsa 4.1 and 5.4 times more compared to the yellow sticky trap (F. occidentalis t =6.548, d.f. = 19, P b 0.0001; F. intonsa t = 12.22, d.f. =19, P b 0.0001; Other unidentified thrips t =4.232, d.f. = 19, P = 0.0005; Fig. 2B). The proportion of female F. occidentalis and F. intonsa was 0.75 and 0.64 on the flower model trap and 0.72 and 0.61 on the yellow sticky trap, respectively. The highest numbers of adult thrips were found in F. occidentalis in both trials. Although about 42% of the thrips in the first trial and 21% in the second trial were not identified, only 2% of the unidentified thrips appeared to be different from either F. occidentalis or F. intonsa. Thrips classified as unidentified were those that could not be extracted without damaging the body parts.
173
morphology, although the different reflectance pattern between the two traps might also affect it (Mainali and Lim, 2008). Visual location of plants by herbivores, parasitoids or predators has received no more than marginal or scattered attention (Prokopy and Owens, 1983). Terry (1997) reviewed the studies that describe the recognition of flower morphology by the thrips Thrips palmi Karny in Dendrobium orchids (Hata et al., 1991) and F. occidentalis in chrysanthemum (Broadbent and Allen, 1995; de Jager et al., 1995). Response to shape by thrips was studied by Moreno et al. (1984) who found that Scirtothrips citri Moulton prefer triangular, elliptical, and rectangular shapes over circular and square ones. Perception of visual cues has been also found in other insects such as hawkmoths (Raguso and Willis, 2002) and bees (Galizia et al., 2004). Flowers serve as mating sites for male and female F. occidentalis (Kirk, 1985; Terry, 1997; Kiers et al., 2000), and their pollen and nectar have nutritional value for female reproduction (Kirk, 1984; de Jager et al., 1993; Gerin et al., 1999; Wäckers et al., 2007). Hence, within-plant abundance of the flower thrips has been reported to be highest in flowers (Reitz, 2002; Hansen et al., 2003; Buitenhuis and Shipp, 2006). Approaches of plant visual attraction that could be used for pest management have been proposed. Prokopy (1975) developed an apple sphere model mimicking ripe apple to attract sexually mature apple maggots, Rhagoletis pomonella Walsh. Katsoyannos and Papadopoulos (2004) also evaluated sticky coated yellow spheres to attract the Mediterranean fruit fly, Ceratitis capitata Wiedemann. Management of insect pest using plant visual attractants like the apple spheres and the flower model in this study could be analogous to the process by which plant olfactory attractants are identified and employed (Prokopy and Owens, 1983). The retail price for the two traps was calculated to be 12.56 and 45.51 US dollars for 100 yellow sticky traps and flower model traps, respectively (exchange rate: 1,040 Korean won = 1 US dollar). Although the flower model trap costs 3.6 times more than yellow sticky trap, it attracts 4.1 times more of F. occidentalis and 5.4 times more of F. intonsa than the yellow sticky trap in the strawberry greenhouse, thus can save labor costs by reducing the number of traps needed to be installed. However, at a high thrips density, deploying many expensive traps would not be economically feasible for mass trapping. The flower model traps can be effectively used when thrips density is low by attracting or intercepting the thrips similar to the use of a real flowering crop used as trap crop, hence reduce initial infestation in the main crop (Buitenhuis and Shipp, 2006). Considering the fact that the strawberry plants in the greenhouse evaluation were all in the flowering stage, the attractiveness of the flower model trap would be higher when the main crop was not in flowering stage. Furthermore, the effectiveness of the flower model trap can be enhanced by the addition of attractive chemicals such as anisaldehyde or aggregation pheromone (Lewis, 1997; Terry, 1997; Hamilton et al., 2005). The flower model trap can also attract other pests such as whiteflies (Mainali and Lim, 2008), tephritid flies, and lepidopterans that preferentially orient toward flowering crops. However, a potential adverse effect of trapping beneficial arthropods such as bees and predatory bugs and mites should be considered before employing the flower model trap as a component of integrated thrips management. Acknowledgment This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2007-331F00010).
Discussion References The flower model trap attracted significantly more F. occidentalis and F. intonsa than regular yellow sticky trap in both laboratory and greenhouse tests. The flower model's attractiveness to these thrips can be explained by tempting visual cues of the trap, i.e., the flower
Blumthal, M.R., Cloyd, R.A., Spomer, L.A., Warnock, D.F., 2005. Flower color preferences of western flower thrips. HortTechnology 15, 846–853. Broadbent, B.A., Allen, W.R., 1995. Interactions within the western flower thrips/tomato spotted wilt virus/host plant complex on virus epidemiology. In: Parker, B.L.,
174
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
Skinner, M., Lewis, T. (Eds.), Thrips Biology and Management. Plenum, New York, pp. 185–196. Buitenhuis, R., Shipp, J.L., 2006. Factors influencing the use of trap plants for the control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse potted chrysanthemum. Environ. Entomol. 35, 1411–1416. Cook, S.M., Khan, Z.R., Pickett, J.A., 2007. The use of push–pull strategies in integrated pest management. Annu. Rev. Entomol. 52, 375–400. de Jager, C.M., Butôt, R.P.T., de Jong, T.J., Klinkhamer, P.G.L., van der Meijeden, E., 1993. Population growth and survival of western flower thrips Frankliniella occidentalis (Thysanoptera, Thripidae) on different chrysanthemum cultivars. J. Appl. Entomol. 115, 519–525. de Jager, C.M., Butot, R.P.T., Klinkhamer, P.G.L., de Jong, T.J., Wolff, K., van der Meijden, E., 1995. Genetic variation in chrysanthemum for resistance to Frankliniella occidentalis. Entomol. Exp. Appl. 77, 277–287. Galizia, C.G., Kunze, J., Gumbert, A., Borg-Karlson, A., Sachse, S., Markl, C., Menzel, R., 2004. Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system. Behav. Ecol. 16, 159–168. Gerin, C., Hance, T.H., van Impe, G., 1999. Impact of flowers on the demography of western flower thrips Frankliniella occidentalis (Thysan., Thripidae). J. Appl. Entomol. 123, 569–574. Hamilton, J.G.C., Hall, D.R., Kirk, W.D.J., 2005. Identification of a male-produced aggregation pheromone in the western flower thrips Frankliniella occidentalis. J. Chem. Ecol. 31, 1369–1379. Hansen, E.A., Funderburk, J.E., Reitz, S.R., Ramachandran, S., Eger, J.E., McAuslane, H., 2003. Within-plant distribution of Frankliniella species (Thysanoptera: Thripidae) and Orius insidiosus (Heteroptera: Anthocoridae) in field pepper. Environ. Entomol. 35, 1035–1044. Hata, T.Y., Hara, A.H., Hansen, J.D., 1991. Feeding preference of melon thrips on orchids in Hawaii. HortScience 26, 1294–1295. Herron, G.A., James, T.M., 2005. Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Aust. J. Entomol. 44, 299–303. Jacobson, R.J., 1997. Integrated pest management in glasshouses. In: Lewis, T. (Ed.), Thrips as Crop Pests. CAB International, Wallingford, United Kingdom, pp. 639–666. Katsoyannos, B.I., Papadopoulos, N.T., 2004. Evaluation of synthetic female attractants against Ceratitis capitata (Diptera: Tephritidae) in sticky coated spheres and Mcphail type traps. J. Econ. Entomol. 97, 21–26. Kiers, E., De Kogal, W.J., Balkema-Boomstra, A., Mollema, C., 2000. Flower visitation and oviposition behaviour of Frankliniella occidentalis (Thysanoptera: Thripidae) on cucumber plants. J. Appl. Entomol. 124, 27–32. Kirk, W.D.J., 1984. Pollen-feeding in thrips (Insecta: Thysanoptera). J. Zool. 204, 107–117. Kirk, W.D.J., 1985. Aggregation and mating of thrips in flowers of Calystegia sepium. Ecol. Entomol. 10, 433–440.
Lee, G.S., Lee, J.H., Kang, S.H., Woo, K.S., 2001. Thrips species (Thysanoptera: Thripidae) in winter season and their vernal activities on Jeju island, Korea. J. Asia-Pacific Entomol. 4, 115–122. Lewis, T., 1997. Pest thrips in perspective. In: Lewis, T. (Ed.), Thrips as crop pests. CAB International, Wallingford, United Kingdom, pp. pp. 1–4. Mainali, B.P., Lim, U.T., 2008. Use of flower model trap to reduce the infestation of greenhouse whitefly on tomato. J. Asia-Pacific Entomol. 11, 65–68. Matsuura, S., Hoshino, S., Koga, H., 2006. Verbena as a trap crop to suppress thripstransmitted tomato spotted wilt virus in chrysanthemums. J. Gen. Plant Pathol. 72, 180–185. Mound, L.A., Kibby, G., 1998. Thysanoptera: An Identification Guide, 2nd. CAB International, Wallingford, United Kingdom. Moreno, D.S., Gregory, W.A., Tanigoshi, L.K., 1984. Flight response of Aphytis melinus (Humenoptera: Aphelinidae) and Scirtothrips citri (Thysanoptera: Thripidae) to trap color, size, and shape. Environ. Entomol. 13, 935–940. Nagata, T., Peters, D., 2001. An anatomical perspective of tospovirus transmission. In: Harris, K.F., Smith, O.P., Duffus, J.E. (Eds.), Virus–Insect–Plant Interactions. Academic Press, San Diego, CA., pp. 51–67. Pearsall, I.A., 2000. Flower preference behaviour of western flower thrips in the Similkameen Valley, British Columbia, Canada. Entomol. Exp. Appl. 95, 303–313. Prokopy, R.J., 1975. Apple maggot control by sticky red spheres. J. Econ. Entomol. 68, 197–198. Prokopy, R.J., Owens, E.D., 1983. Visual detection of plants by herbivorous insects. Annu. Rev. Entomol. 28, 337–364. Reitz, S.R., 2002. Seasonal and within plant distribution of Frankliniella thrips (Thysanoptera: Thripidae) in north Florida tomatoes. Fla. Entomol. 85, 431–439. Raguso, R.A., Willis, M.A., 2002. Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Maduca sexta. Anim. Behav. 64, 685–695. Scheirer, C.J., 1976. The analysis of ranked data derived from completely randomized factorial designs. Biometrics 32, 429–434. Shelton, A.M., Badenes-Perez, F.R., 2006. Concepts and applications of trap cropping in pest management. Annu. Rev. Entomol. 51, 285–308. Terry, I., 1997. Host selection communication and reproductive behavior. In: Lewis, T. (Ed.), Thrips as Crop Pests. CAB International, Wallingford, United Kingdom, pp. 65–118. Vernon, R.S., Gillespie, D.R., 1990. Spectral responsiveness of Frankliniella occidentalis (Thysanoptera: Thripidae) determined by trap catches in greenhouses. Environ. Entomol. 19, 1229–1241. Wäckers, F.L., Romeis, J., Van Rijn, P., 2007. Nectar and pollen feeding by insect herbivores and implications for multitrophic interaction. Annu. Rev. Entomol. 52, 301–323. Yudin, L.S., Tabashnik, B.E., Cho, J.J., Mitchell, W.C., 1988. Colonization of weeds and lettuce by thrips (Thysanoptera: Thripidae). Environ. Entomol. 17, 522–526.
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j a p e
Short Communication
Evaluation of chrysanthemum flower model trap to attract two Frankliniella thrips (Thysanoptera: Thripidae) Bishwo Prasad Mainali, Un Taek Lim ⁎ School of Bioresource Sciences, Andong National University, Andong 760-749, Republic of Korea
a r t i c l e
i n f o
Article history: Received 19 May 2008 Revised 2 July 2008 Accepted 3 July 2008 Keywords: Frankliniella occidentalis Frankliniella intonsa Artificial flower Visual attraction Yellow sticky trap
a b s t r a c t Frankliniella occidentalis Pergande and F. intonsa Trybom (Thysanoptera: Thripidae) are anthophilous insect pests of many crops worldwide. We evaluated a flower model trap mimicking the chrysanthemum flower as a new method to attract the thrips in the laboratory and a strawberry greenhouse. Both choice and no-choice tests in the laboratory showed that the chrysanthemum flower model trap attracted significantly more adult F. occidentalis and F. intonsa compared to yellow sticky trap. Up to 4.1 times more of F. occidentalis and 5.4 times more of F. intonsa were caught in the flower model trap in the strawberry greenhouse. The flower model trap would be a good addition to the integrated thrips management, although at present it is more expensive than the yellow sticky trap. © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2008 Published by Elsevier B.V. All rights reserved.
Introduction Frankliniella occidentalis Pergande and F. intonsa Trybom (Thysanoptera: Thripidae) are ubiquitous, polyphagous pests of vegetables, fruits and ornamental crops. Direct feeding as well as tospovirus transmission by the thrips causes economic loss worldwide (Lewis, 1997; Nagata and Peters, 2001). In particular, F. occidentalis has become a serious pest in numerous crops such as pepper, cucumber, and strawberry in Korea since the thrips was first found in Jeju island in 1993 (Lee et al., 2001). Thrips are difficult to control due to their high reproductive rate, cryptic habit, and resistance to many insecticides (Jacobson, 1997; Herron and James, 2005). As an approach that can integrate various thrips control tactics, use of trap crops has been suggested (Yudin et al., 1988; Pearsall, 2000; Buitenhuis and Shipp, 2006; Matsuura et al., 2006; Shelton and Badenes-Perez, 2006). Trap crops are defined as plant stands that are deployed to attract, divert, intercept, and/or retain targeted insects or the pathogens they vector in order to reduce damage to the main crop (Shelton and Badenes-Perez, 2006). Therefore, it distracts the pests from locating the main crop, resulting in less damage and concentrating them into the trap crop where they can be more effectively controlled (Shelton and Badenes-Perez, 2006; Cook et al., 2007). Adult F. occidentalis and F. intonsa preferentially orient toward and land on flowering plants though they may feed on non-flowering plants (Yudin et al., 1988; Vernon and Gillespie, 1990; Blumthal et al., 2005). Based on the observations of thrips behavior, Yudin et al. (1988) suggested flower-
⁎ Corresponding author. Fax: +82 54 823 1628. E-mail address: [email protected] (U.T. Lim).
ing weeds as trap crops for the management of F. occidentalis in lettuce, which does not flower under normal cultivation practices. Blumthal et al. (2005) investigated flower preference of F. occidentalis using four different colored flowers and suggested the yellow transvaal daisy as a potential trap crop. Buitenhuis and Shipp (2006) used flowering chrysanthemum as a trap crop to attract and retain F. occidentalis in a potted chrysanthemum greenhouse. However, the flowers of trap crop may supplement nutrition for dispersing thrips that would re-colonize the main crop. Therefore, quick removal of flowering trap crop from the greenhouse is needed before the buildup of the thrips population (de Jager et al., 1993; Buitenhuis and Shipp, 2006). Shelton and Badenes-Perez (2006) discussed other limitations of trap cropping such as cost of setting aside land for trap crop and species specificity. To reduce the potential risks and/or costs implemented by using a real flowering plant as a trap crop, we suggest using a chrysanthemum flower model, a stem of sticky artificial flower mimicking yellow chrysanthemum flower, as a new method to trap anthophilous thrips. The trap was evaluated on two thrips, F. occidentalis and F. intonsa, by comparing with a commonlyused yellow sticky trap in the laboratory and a commercial strawberry greenhouse. Materials and methods Rearing of thrips Both F. occidentalis and F. intonsa were collected from a strawberry greenhouse located in Songchun, Andong, Korea in 2006 and were reared in a plastic container (24 cm × 17 cm × 8 cm) with a lid having two holes (diameter = 6 cm) covered with fine mesh fabric (196 mesh
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2008 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.aspen.2008.07.003
172
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
count, Saatilene Hitech, Zurich Co., Como, Italy) at the center. Thrips were provided with leaves of red kidney bean plants, Phaseolus vulgaris L., as a food source. Eight excised stems with cotyledonous leaves were rooted on water-soaked cotton. A mixture of pure honey and pine tree pollen was streaked along the main vein of each leaf by using a paint brush. The container was kept at 28°C and 16: 8 (L: D)h photoperiod in a growth chamber, and water was added daily during the rearing period. Thirty newly emerged adult thrips were transferred to a new plastic container with the food sources for the reproduction of the next generation. Design of chrysanthemum flower model trap Artificial yellow chrysanthemum flowers (45009A, International Artificial Flowers Co., Kimhae, Korea) were modified as a flower model trap. Details of designing the flower model trap is described in Mainali and Lim (2008). Choice tests (flower model trap vs. yellow sticky trap) For each thrips species of F. occidentalis and F. intonsa, 60 adult females were released on red kidney bean with cotyledonous leaves grown on a pot (10 cm×12 cm) inside an acrylic cage (30 cm×30 cm×30 cm). The cage was ventilated through windows on three sides covered with mesh fabric was incubated at 28 °C in the growth chamber. After the acclimatization of the released adult thrips for 2h, the flower model trap and a yellow sticky trap were placed opposite to each other, both facing toward the kidney bean plant at an equal distance from the plant. The height of traps was maintained just above the leaves. Five replications were made
Fig. 2. Mean number of F. occidentalis (FO) and F. intonsa (FI) trapped by flower model trap (FMT) and yellow sticky trap (YST) in a strawberry greenhouse. Sampling was replicated twice for the periods of 30 April–3 May (A) and 10 May–13 May (B). See text for statistics.
for each thrips species. Number of adult thrips caught was counted daily for the period of 1 week. No-choice tests In no-choice test, each flower model trap or yellow sticky trap was placed lateral to a red kidney bean plant in the acryl cage. Same experimental conditions as described in the choice test were provided. Fifty adult females of each thrips species were released and the number of adult thrips caught was counted daily for a period of 1 week. For each thrips species this procedure was replicated five times. Comparisons in greenhouse
Fig. 1. Number of thrips trapped by flower model trap (FMT) and yellow sticky trap (YST) for 1 week at 28 °C in a growth chamber. See text for statistics.
Comparisons between the flower model trap and the yellow sticky trap were conducted in a commercial strawberry greenhouse at Songchun, Andong. The greenhouse (74 m × 7.5 m) was divided into 35 plots each measuring 1 m × 10 m, and from those, 20 plots were randomly chosen. One flower model trap and one sticky trap were placed at a distance of 1.2m apart facing each other in the center of the selected plot. The comparison tests were conducted twice from 30 April to 3 May and from 10 May to 13 May in 2007. Both the flower model traps and the yellow sticky traps were collected after 3 days and brought to the laboratory for the identification of the adult thrips caught. The adult thrips caught in the sticky surface were extracted by using xylene and ethylene glycol and identified under a stereomicroscope according to Mound and Kibby (1998).
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
Statistical analyses Numbers of thrips caught on the flower model trap and the yellow sticky trap were compared between F. occidentalis and F. intonsa using an extension of the Kruskal–Wallis ranks test proposed by Scheirer (1976). Data from the strawberry greenhouse were analyzed with a paired t-test. Results Choice tests The flower model trap attracted 2.6 and 3.2 times more adult thrips compared to the yellow sticky trap for F. occidentalis and F. intonsa, respectively (H = 12.360, d.f. = 1, 19, P = 0.0004; Fig. 1). Daily mean numbers of F. occidentalis caught were 4.3 in the flower model trap and 1.6 in the yellow sticky trap while those of F. intonsa were 2.2 and 0.7, respectively. Significant difference in attractiveness between the two species was also found (H = 4.321, d.f. = 1, 19, P = 0.0376), although no interaction between the trap kinds and thrips species was found (H = 0.006, d.f. = 1, 19, P = 0.9397). No-choice tests No-choice tests also showed higher numbers of adult thrips on the flower model trap compared to the yellow sticky trap (H = 13.720, d.f. = 1, 19, P = 0.0002), even though we found no differences between the two thrips species in the number of adult thrips attracted to traps (H = 3.571, d.f. = 1, 19, P = 0.0588) and no interaction between trap type and thrips species (H = 0.006, d.f. = 1, 19, P = 0.9397) (Fig. 1). The flower model trap attracted 1.7 and 1.8 times more adult thrips compared to the yellow sticky trap for F. occidentalis and F. intonsa, respectively. Daily mean numbers of F. occidentalis caught were 5.4 in the flower model trap and 3.2 in the yellow sticky trap while those of F. intonsa were 4.0 and 2.3, respectively. Comparisons in greenhouse In the first trial when the thrips population was low in the greenhouse, the flower model trap caught more adult thrips than the yellow sticky trap (F. occidentalis t =3.149, d.f. = 9, P = 0.0053; F. intonsa t = 2.800, d.f. = 19, P = 0.0114; Other unidentified thrips t = 6.097, d.f. = 19, P b 0.0001; Fig. 2A). The total number of adult F. occidentalis and F. intonsa caught by the flower model trap was about 2.1 and 4.1 times higher than that caught by the yellow sticky trap, respectively. The proportion of female F. occidentalis and F. intonsa caught was 0.40 and 0.42 on the flower model trap and 0.29 and 0.25 on the yellow sticky trap, respectively. In the second trial the flower model trapped adult F. occidentalis and F. intonsa 4.1 and 5.4 times more compared to the yellow sticky trap (F. occidentalis t =6.548, d.f. = 19, P b 0.0001; F. intonsa t = 12.22, d.f. =19, P b 0.0001; Other unidentified thrips t =4.232, d.f. = 19, P = 0.0005; Fig. 2B). The proportion of female F. occidentalis and F. intonsa was 0.75 and 0.64 on the flower model trap and 0.72 and 0.61 on the yellow sticky trap, respectively. The highest numbers of adult thrips were found in F. occidentalis in both trials. Although about 42% of the thrips in the first trial and 21% in the second trial were not identified, only 2% of the unidentified thrips appeared to be different from either F. occidentalis or F. intonsa. Thrips classified as unidentified were those that could not be extracted without damaging the body parts.
173
morphology, although the different reflectance pattern between the two traps might also affect it (Mainali and Lim, 2008). Visual location of plants by herbivores, parasitoids or predators has received no more than marginal or scattered attention (Prokopy and Owens, 1983). Terry (1997) reviewed the studies that describe the recognition of flower morphology by the thrips Thrips palmi Karny in Dendrobium orchids (Hata et al., 1991) and F. occidentalis in chrysanthemum (Broadbent and Allen, 1995; de Jager et al., 1995). Response to shape by thrips was studied by Moreno et al. (1984) who found that Scirtothrips citri Moulton prefer triangular, elliptical, and rectangular shapes over circular and square ones. Perception of visual cues has been also found in other insects such as hawkmoths (Raguso and Willis, 2002) and bees (Galizia et al., 2004). Flowers serve as mating sites for male and female F. occidentalis (Kirk, 1985; Terry, 1997; Kiers et al., 2000), and their pollen and nectar have nutritional value for female reproduction (Kirk, 1984; de Jager et al., 1993; Gerin et al., 1999; Wäckers et al., 2007). Hence, within-plant abundance of the flower thrips has been reported to be highest in flowers (Reitz, 2002; Hansen et al., 2003; Buitenhuis and Shipp, 2006). Approaches of plant visual attraction that could be used for pest management have been proposed. Prokopy (1975) developed an apple sphere model mimicking ripe apple to attract sexually mature apple maggots, Rhagoletis pomonella Walsh. Katsoyannos and Papadopoulos (2004) also evaluated sticky coated yellow spheres to attract the Mediterranean fruit fly, Ceratitis capitata Wiedemann. Management of insect pest using plant visual attractants like the apple spheres and the flower model in this study could be analogous to the process by which plant olfactory attractants are identified and employed (Prokopy and Owens, 1983). The retail price for the two traps was calculated to be 12.56 and 45.51 US dollars for 100 yellow sticky traps and flower model traps, respectively (exchange rate: 1,040 Korean won = 1 US dollar). Although the flower model trap costs 3.6 times more than yellow sticky trap, it attracts 4.1 times more of F. occidentalis and 5.4 times more of F. intonsa than the yellow sticky trap in the strawberry greenhouse, thus can save labor costs by reducing the number of traps needed to be installed. However, at a high thrips density, deploying many expensive traps would not be economically feasible for mass trapping. The flower model traps can be effectively used when thrips density is low by attracting or intercepting the thrips similar to the use of a real flowering crop used as trap crop, hence reduce initial infestation in the main crop (Buitenhuis and Shipp, 2006). Considering the fact that the strawberry plants in the greenhouse evaluation were all in the flowering stage, the attractiveness of the flower model trap would be higher when the main crop was not in flowering stage. Furthermore, the effectiveness of the flower model trap can be enhanced by the addition of attractive chemicals such as anisaldehyde or aggregation pheromone (Lewis, 1997; Terry, 1997; Hamilton et al., 2005). The flower model trap can also attract other pests such as whiteflies (Mainali and Lim, 2008), tephritid flies, and lepidopterans that preferentially orient toward flowering crops. However, a potential adverse effect of trapping beneficial arthropods such as bees and predatory bugs and mites should be considered before employing the flower model trap as a component of integrated thrips management. Acknowledgment This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2007-331F00010).
Discussion References The flower model trap attracted significantly more F. occidentalis and F. intonsa than regular yellow sticky trap in both laboratory and greenhouse tests. The flower model's attractiveness to these thrips can be explained by tempting visual cues of the trap, i.e., the flower
Blumthal, M.R., Cloyd, R.A., Spomer, L.A., Warnock, D.F., 2005. Flower color preferences of western flower thrips. HortTechnology 15, 846–853. Broadbent, B.A., Allen, W.R., 1995. Interactions within the western flower thrips/tomato spotted wilt virus/host plant complex on virus epidemiology. In: Parker, B.L.,
174
B.P. Mainali, U.T. Lim / Journal of Asia-Pacific Entomology 11 (2008) 171–174
Skinner, M., Lewis, T. (Eds.), Thrips Biology and Management. Plenum, New York, pp. 185–196. Buitenhuis, R., Shipp, J.L., 2006. Factors influencing the use of trap plants for the control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse potted chrysanthemum. Environ. Entomol. 35, 1411–1416. Cook, S.M., Khan, Z.R., Pickett, J.A., 2007. The use of push–pull strategies in integrated pest management. Annu. Rev. Entomol. 52, 375–400. de Jager, C.M., Butôt, R.P.T., de Jong, T.J., Klinkhamer, P.G.L., van der Meijeden, E., 1993. Population growth and survival of western flower thrips Frankliniella occidentalis (Thysanoptera, Thripidae) on different chrysanthemum cultivars. J. Appl. Entomol. 115, 519–525. de Jager, C.M., Butot, R.P.T., Klinkhamer, P.G.L., de Jong, T.J., Wolff, K., van der Meijden, E., 1995. Genetic variation in chrysanthemum for resistance to Frankliniella occidentalis. Entomol. Exp. Appl. 77, 277–287. Galizia, C.G., Kunze, J., Gumbert, A., Borg-Karlson, A., Sachse, S., Markl, C., Menzel, R., 2004. Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system. Behav. Ecol. 16, 159–168. Gerin, C., Hance, T.H., van Impe, G., 1999. Impact of flowers on the demography of western flower thrips Frankliniella occidentalis (Thysan., Thripidae). J. Appl. Entomol. 123, 569–574. Hamilton, J.G.C., Hall, D.R., Kirk, W.D.J., 2005. Identification of a male-produced aggregation pheromone in the western flower thrips Frankliniella occidentalis. J. Chem. Ecol. 31, 1369–1379. Hansen, E.A., Funderburk, J.E., Reitz, S.R., Ramachandran, S., Eger, J.E., McAuslane, H., 2003. Within-plant distribution of Frankliniella species (Thysanoptera: Thripidae) and Orius insidiosus (Heteroptera: Anthocoridae) in field pepper. Environ. Entomol. 35, 1035–1044. Hata, T.Y., Hara, A.H., Hansen, J.D., 1991. Feeding preference of melon thrips on orchids in Hawaii. HortScience 26, 1294–1295. Herron, G.A., James, T.M., 2005. Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Aust. J. Entomol. 44, 299–303. Jacobson, R.J., 1997. Integrated pest management in glasshouses. In: Lewis, T. (Ed.), Thrips as Crop Pests. CAB International, Wallingford, United Kingdom, pp. 639–666. Katsoyannos, B.I., Papadopoulos, N.T., 2004. Evaluation of synthetic female attractants against Ceratitis capitata (Diptera: Tephritidae) in sticky coated spheres and Mcphail type traps. J. Econ. Entomol. 97, 21–26. Kiers, E., De Kogal, W.J., Balkema-Boomstra, A., Mollema, C., 2000. Flower visitation and oviposition behaviour of Frankliniella occidentalis (Thysanoptera: Thripidae) on cucumber plants. J. Appl. Entomol. 124, 27–32. Kirk, W.D.J., 1984. Pollen-feeding in thrips (Insecta: Thysanoptera). J. Zool. 204, 107–117. Kirk, W.D.J., 1985. Aggregation and mating of thrips in flowers of Calystegia sepium. Ecol. Entomol. 10, 433–440.
Lee, G.S., Lee, J.H., Kang, S.H., Woo, K.S., 2001. Thrips species (Thysanoptera: Thripidae) in winter season and their vernal activities on Jeju island, Korea. J. Asia-Pacific Entomol. 4, 115–122. Lewis, T., 1997. Pest thrips in perspective. In: Lewis, T. (Ed.), Thrips as crop pests. CAB International, Wallingford, United Kingdom, pp. pp. 1–4. Mainali, B.P., Lim, U.T., 2008. Use of flower model trap to reduce the infestation of greenhouse whitefly on tomato. J. Asia-Pacific Entomol. 11, 65–68. Matsuura, S., Hoshino, S., Koga, H., 2006. Verbena as a trap crop to suppress thripstransmitted tomato spotted wilt virus in chrysanthemums. J. Gen. Plant Pathol. 72, 180–185. Mound, L.A., Kibby, G., 1998. Thysanoptera: An Identification Guide, 2nd. CAB International, Wallingford, United Kingdom. Moreno, D.S., Gregory, W.A., Tanigoshi, L.K., 1984. Flight response of Aphytis melinus (Humenoptera: Aphelinidae) and Scirtothrips citri (Thysanoptera: Thripidae) to trap color, size, and shape. Environ. Entomol. 13, 935–940. Nagata, T., Peters, D., 2001. An anatomical perspective of tospovirus transmission. In: Harris, K.F., Smith, O.P., Duffus, J.E. (Eds.), Virus–Insect–Plant Interactions. Academic Press, San Diego, CA., pp. 51–67. Pearsall, I.A., 2000. Flower preference behaviour of western flower thrips in the Similkameen Valley, British Columbia, Canada. Entomol. Exp. Appl. 95, 303–313. Prokopy, R.J., 1975. Apple maggot control by sticky red spheres. J. Econ. Entomol. 68, 197–198. Prokopy, R.J., Owens, E.D., 1983. Visual detection of plants by herbivorous insects. Annu. Rev. Entomol. 28, 337–364. Reitz, S.R., 2002. Seasonal and within plant distribution of Frankliniella thrips (Thysanoptera: Thripidae) in north Florida tomatoes. Fla. Entomol. 85, 431–439. Raguso, R.A., Willis, M.A., 2002. Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Maduca sexta. Anim. Behav. 64, 685–695. Scheirer, C.J., 1976. The analysis of ranked data derived from completely randomized factorial designs. Biometrics 32, 429–434. Shelton, A.M., Badenes-Perez, F.R., 2006. Concepts and applications of trap cropping in pest management. Annu. Rev. Entomol. 51, 285–308. Terry, I., 1997. Host selection communication and reproductive behavior. In: Lewis, T. (Ed.), Thrips as Crop Pests. CAB International, Wallingford, United Kingdom, pp. 65–118. Vernon, R.S., Gillespie, D.R., 1990. Spectral responsiveness of Frankliniella occidentalis (Thysanoptera: Thripidae) determined by trap catches in greenhouses. Environ. Entomol. 19, 1229–1241. Wäckers, F.L., Romeis, J., Van Rijn, P., 2007. Nectar and pollen feeding by insect herbivores and implications for multitrophic interaction. Annu. Rev. Entomol. 52, 301–323. Yudin, L.S., Tabashnik, B.E., Cho, J.J., Mitchell, W.C., 1988. Colonization of weeds and lettuce by thrips (Thysanoptera: Thripidae). Environ. Entomol. 17, 522–526.