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Performance and selectivity of floral attractant-baited traps targeted for cetoniin scarabs (Coleoptera: Scarabaeidae) in Central and Southern Europe
Crop Protection 29 (2010) 1177e1183
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Crop Protection journal homepage: www.elsevier.com/locate/cropro
Performance and selectivity of floral attractant-baited traps targeted for cetoniin scarabs (Coleoptera: Scarabaeidae) in Central and Southern Europe J. Vuts a, *, B. Baric b, J. Razov c, T.B. Toshova d, M. Subchev d, I. Sredkov e, R. Tabilio f, F. Di Franco g, M. Tóth a a
Plant Protection Institute, HAS, Herman O. u. 15, H-1022 Budapest, Hungary University of Zagreb, Faculty of Agriculture, Department of Agricultural Zoology, Svetosimunska 25, HR-10000 Zagreb, Croatia c University of Zadar, Department of Mediterranean Agriculture and Aquaculture, Mihovila Pavlinovica bb., HR-23000 Zadar, Croatia d Zoology Institute, Bulgarian Academy of Sciences, blvd. Tzar Osvoboditel 1, BG-1000 Sofia, Bulgaria e Institute of Agronomy, Sofijskko shose, BG-2500 Kyustendil, Bulgaria f Centro di Ricerca per la Frutticoltura di Roma, Via di Fioranello 52, I-00040 Ciampino Airport (RM), Italy g CRA e Centro di Ricerca per l’Agrumicoltura e le Colture Meridionali, Corso Savoia 190, I-95024 Acireale (Catania), Italy b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 January 2010 Received in revised form 12 May 2010 Accepted 13 May 2010
Trapping tests were performed concurrently in several countries of Central and Southern Europe throughout the spring and summer of 2008, to study the selectivity and performance of floral attractantbaited traps developed for catching Epicometis (Tropinota) hirta Poda (CA-baited traps), Cetonia a. aurata L./Potosia (Protaetia) cuprea Fabr. (ME-baited traps) or Oxythyrea funesta Poda (PH-baited traps) (Coleoptera: Scarabaeidae, Cetoniinae). Amongst the species caught, E. hirta showed strongest attraction to the CA-baited and ME-baited traps. O. funesta was mostly caught by PH-baited traps. In capturing C. a. aurata and P. cuprea, the ME-baited trap appeared to be the most efficient. At two sites in Italy, a related scarab, Tropinota squalida Scop. (Coleoptera: Scarabaeidae, Cetoniinae), was attracted in similar numbers to both CA-baited and ME-baited traps. For the scarab Valgus hemipterus L. (Coleoptera: Scarabaeidae, Valginae), ME-baited traps proved to be the most attractive. Of the scarabs coming to the CA-baited trap, E. hirta was the most abundant, except at the two Italian sites where large percentages were shown to be T. squalida. The most abundant species in the catch by the PH-baited trap was O. funesta, although at some sites, C. a. aurata and E. hirta were captured in sizeable numbers. ME-baited traps caught mostly C. a. aurata at sites with large C. a. aurata populations, whereas at sites with low populations, good numbers of E. hirta or T. squalida were caught. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Cetoniins Mass trapping Control strategies Scarab pests Monitoring
1. Introduction Many species in the subfamily Cetoniinae (Coleoptera: Scarabaeidae) are of agricultural importance. The adult beetles cause damage by feeding on the reproductive parts of fruit trees and ornamental plants, and also on ripening fruit later in the season (Hurpin, 1962). Control of these species is difficult, since most insecticides cannot be applied during flowering without affecting honeybees and other beneficial insects, or before harvest because of health hazards. Mass trapping of adult beetles can be an alternative control method, provided that an efficient trapping system is available. In Europe, the most important cetoniin pest is Epicometis (Tropinota) hirta Poda (Hurpin, 1962; Homonnay and HomonnaynéCsehi, 1990; Mircheva et al., 2004). A binary chemical attractant * Corresponding author. Tel.: þ36 1 391 8647; fax: þ36 1 391 8655. E-mail address: [email protected] (J. Vuts). 0261-2194/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2010.05.007
comprising (E)-cinnamyl alcohol and (E)-anethol has been optimized previously and proved to be attractive to adult E. hirta beetles (Tóth et al., 2003, 2004). Application of this binary chemical attractant, together with a light blue colour in funnel traps, resulted in significantly higher catches than in traps containing either the chemical or the visual cue alone (Schmera et al., 2004). The first attempts at mass trapping trials in strawberry plantations and apple orchards against E. hirta using attractant-baited light blue traps were reported by Sivcev et al. (2006) and Tóth et al. (2005). Reports of significant damage by Cetonia a. aurata L. and Potosia (Protaetia) cuprea Fabr. in Hungary have increased in frequency during recent years (Voigt et al., 2005). This indicates that the significance of these pest species is growing. A ternary chemical attractant comprising 3-methyl eugenol, 1-phenylethanol and (E)anethol was optimized previously and proved to be attractive to adults of C. a. aurata and P. cuprea (Tóth et al., 2005). C. a. aurata and P. cuprea were attracted in higher numbers to a light blue, rather than to other colours tested in the presence of their floral attractant
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(Tóth et al., 2005). Light blue traps baited with the ternary attractant are in use today in Central Europe for monitoring and mass trapping of C. a. aurata and P. cuprea (Voigt et al., 2005; Tóth et al., 2006; Razov et al., 2008). More recently, the addition of ()-lavandulol to the known ternary bait increased catches of C. a. aurata and P. cuprea significantly, providing a more efficient attractant for these scarabs (Vuts et al., 2010). The cetoniin scarab Oxythyrea funesta Poda can also cause occasional damage in orchards (Hurpin, 1962; Tóth et al., 2005). A fluorescent yellow trap exploiting the strong attractancy of O. funesta to this colour (Tóth et al., 2005), and baited with the binary lure of ()-lavandulol and 2-phenylethanol, has been developed for monitoring and mass trapping of this scarab (Vuts et al., 2008). The objective of the present research was to study the performance and selectivity in catching cetoniin scarabs of traps developed for E. hirta, Cetonia/Potosia or O. funesta, respectively, throughout the spring and summer in 2008. Parallel tests were conducted in several Central and Southern European countries. 2. Material and methods 2.1. Baits To prepare the bait dispensers, a 1 cm piece of dental roll (CelluronÒ, Paul Hartmann AG, Heidenheim, Germany) was placed into a tight polythene bag made of 0.02 mm linear polyethylene foil (ca. 1.5 1.5 cm). The dispenser was attached to a plastic strip (8 1 cm) for easy handling when assembling the traps. For making up the baits, compounds were administered onto the dental roll and the polythene bag was heat-sealed. Previous experience showed that bait activity was not reduced after several weeks of field exposure, so we decided that it was safe to renew the lures at 2e3-week-intervals (Tóth et al., unpublished data). Details of treatments set up in the tests are shown in Table 1. Dispensers were wrapped singly in pieces of alufoil and were stored at 30 C before use. Synthetic compounds were obtained from SigmaeAldrich Kft. (Budapest, Hungary). All compounds were >95% pure as stated by the supplier.
Table 2 Details of field tests. HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary. Experiment
Locality
Biotop
Period
1
Bascica (HR)
March 26eAugust 19, 2008
2 3
Prkos (HR) Zagreb (HR)
4 5 6 7 8
Kyustendil (BG) Sofia (BG) Rome (I) Acireale (I) Telki (HU)
Edge of a mixed orchard mixed orchard Edge of a mixed orchard Mixed orchard Mixed orchard Mixed orchard Mixed orchard Bushy edge of an oak forest
March 26eAugust 19, 2008 April 9eAugust 20, 2008 March 28eAugust 9, 2008 March 25eJuly 29, 2008 April 1eAugust 4, 2008 March 4eJuly 1, 2008 April 3eAugust 29, 2008
2.3. Field tests Experiments were conducted concurrently in several countries in Europe in 2008. Traps were set up in a randomized complete block design (number of blocks: 4, number of traps/site: 12). The distance between traps was 10e15 m, with a minimum distance of 25 m between blocks. Traps were set up in sunny places with no shade of trees or buildings, attached to poles at a 30e40 cm height above the ground. Traps were inspected twice weekly. Captured insects were removed, their species identified and numbers recorded. Details of each experiment are presented in Table 2. 2.4. Statistics Catches were transformed using (x þ 0.5)1/2 as suggested by Roelofs and Cardé (1977) for similar experiments and were analyzed by ANOVA. Treatment means were separated by the GameseHowell post hoc test (Jaccard et al., 1984). All statistical procedures were conducted using the software packages StatViewÒ v4.01 and SuperANOVAÒ v1.11 (Abacus Concepts Inc., Berkeley, CA). 3. Results
2.2. Traps In the tests, CSALOMONÒ VARb3 modified funnel traps (produced by Plant Prot. Inst., HAS, Budapest, Hungary) were used, which proved to be excellent for the capture of related scarabs (i.e. Imrei et al., 2001; Schmera et al., 2004). Photos of VARb3 traps can be viewed at www.julia-nki.hu/traps. The upper funnels of VARb3 traps developed for catching E. hirta or Cetonia/Potosia were light blue, while fluorescent yellow was used for traps developed for catching O. funesta. For the reflectance spectra of these colours, see Schmera et al. (2004). Later on in the text, the trap for the capture of E. hirta will be referred to as CA-baited trap due to the unique (E)cinnamyl alcohol content of its bait. Similarly, the trap for capturing Cetonia/Potosia will be referred to as ME-baited trap due to the 3-methyl eugenol content of its bait, and the trap developed for O. funesta will be referred to as PH-baited trap because of 2-phenylethanol.
3.1. E. hirta Except in Acireale Italy (I), where no E. hirta catches were observed, the PH-baited trap caught fewer beetles than CA-baited or ME-baited traps; at all sites except Zagreb Croatia (HR), the differences were significant (Fig. 1). There were no statistical differences observed between the catches of CA-baited or MEbaited traps. 3.2. O. funesta Catches of O. funesta were highest in PH-baited traps (Fig. 1). ME-baited traps were generally more attractive to O. funesta than CA-baited traps; at Bascica HR and Telki Hungary (HU), the differences were significant.
Table 1 Details of treatments tested. Treatment
A B C
Trap
ME-baited PH-baited CA-baited
Bait composition (mg)
Trap colour
(E)-Anethol
3-Methyl eugenol
1-Phenylethanol
(E)-Cinnamyl alcohol
()-Lavandulol
2-Phenylethanol
100 e 200
100 e e
100 e e
e e 200
100 200 e
e 200 e
Blue Fluorescent yellow Blue
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3.3. C. a. aurata
3.4. P. cuprea
In all sites where C. a. aurata was found, ME-baited traps were the most effective in attracting C. a. aurata, followed by PH-baited or CA-baited traps (Fig. 1).
This species was only captured in Prkos HR and Telki HU, where ME-baited traps attracted more P. cuprea beetles than the other two traps (Fig. 1).
Fig. 1. Mean catches of scarabs at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary) in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp. Columns with the same letter within one diagram are not significantly different at P ¼ 5% by ANOVA, GameseHowell. Total catches of less than 15 beetles in an experiment were categorized as ‘Very low numbers caught’ and are not shown in the figure.
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3.5. Other scarabs Tropinota squalida Scop. was observed only at Rome I and Acireale I, where it was attracted to CA-baited and ME-baited traps in similar numbers (Fig. 1). Valgus hemipterus L. (Coleoptera: Scarabaeidae, Valginae) was caught in high numbers only at Bascica HR and mostly in ME-baited traps (Fig. 1). Only low numbers were found in CA-baited or PHbaited traps. 3.6. Selectivity of the traps 3.6.1. ME-baited traps C. a. aurata was the most abundant cetoniin species collected at the two sites with the largest C. a. aurata populations (Zagreb HR and Telki HU) (70% and 76%, resp.) (Fig. 2). At sites with low C. a. aurata populations, good numbers of E. hirta were caught (ranging
from 90% to 31%). At Acireale I, T. squalida was the most abundant species caught in ME-baited traps (97%). At Rome I and Sofia Bulgaria (BG), C. a. aurata was absent. P. cuprea was caught in larger numbers at Telki HU (8%), while at other sites, it was recorded only in low numbers ranging from 12% to 0.4% of total catch. P. cuprea was absent at Kyustendil (BG), Sofia BG, Rome I and Acireale I. 3.6.2. PH-baited traps At 4 sites, O. funesta was caught in percentages ranging from 87% to 35% (Fig. 2). At Telki HU, C. a. aurata and at Prkos HR, E. hirta were caught in sizable numbers. At Kyustedil BG, very low (6%), and at Acireale I, no O. funesta catches were observed in PH-baited traps. 3.6.3. CA-baited traps Except for the two sites in Italy, E. hirta comprised 100% to 54% of the total captures in these traps (Fig. 2). At Rome I, 57% of the total catch was the closely related T. squalida. At Acireale I, only
Fig. 2. Percentage distribution of total catches of scarabs in the whole experimental period in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp., at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary). Numbers above each column show total number of scarabs caught.
J. Vuts et al. / Crop Protection 29 (2010) 1177e1183
T. squalida was collected, suggesting that E. hirta was absent at that location. The second most abundant species in CA-baited traps was C. a. aurata, ranging from 40% to 6%, while O. funesta ranged from 23% to 2%. Only small numbers of P. cuprea (3e1% of total catch) and V. hemipterus (15e1%) were caught in CA-baited traps. The selectivity of the traps studied in the present project was influenced by the local occurrence of the target species and the relative abundance of the other cetoniins at any given site. Thus, even the most selective trap tested in this study, the PH-baited trap, caught cetoniins other than O. funesta in large percentages where O. funesta was evidently present in low populations, or was not present at all. Another factor to consider is that selectivity of a given trap calculated for the whole season may be significantly different from selectivity of the same trap during the main flight period of the
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target species (which may occur before or after flights of other related species coming to the trap). Thus, for example, the 54% E. hirta selectivity of the CA-baited trap at Telki HU (Fig. 2) becomes 94% if we consider only the main flight period (between April 7 and May 10 at this site) of E. hirta (Fig. 3) and, likewise, the 41% Cetonia/ Potosia selectivity of the ME-baited trap at Prkos HR becomes 99% if we consider only the main flight period (between June 27 and July 23 at this site) of C. a. aurata and P. cuprea (see also Fig. 3). 4. Discussion In the present experiments, equally large numbers of E. hirta were caught in CA-baited and ME-baited traps. Previously, we had no data on the performance of the ME-baited trap early in the spring, when E. hirta is flying (Tóth et al., 2005). The surprisingly
Fig. 3. Percentage distribution of total catches of scarabs in the main flight period of the target species in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp., at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary). Period shown for Cetonia/Potosia: Exp. 1: May 30eJun 9; Exp. 2: Jun 27eJul 23; Exp. 3: Jul 2eAug 6; Exp. 4: Apr 24eAug 9; Exp. 5: Apr 30eJul 29; Exp. 6: Jun 4eAug 4; Exp. 7: May 15eJul 1; Exp. 8: Jun 24eAug 4. For O. funesta: Exp. 1: May 30eJul 11; Exp. 2: Apr 21eJun 5; Exp. 3: Apr 30eJul 2; Exp. 4: Jun 2eAug 9; Exp. 5: May 26eJul 29; Exp. 6: Apr 14eAug 4; Exp. 7: Mar 4eJul 1; Exp. 8: May 10eJun 19. For E. hirta: Exp. 1: Mar 31eMay 30; Exp. 2: Mar 31eMay 19; Exp. 3: Apr 16eMay 14; Exp. 4: Mar 31eApr 29; Exp. 5: Apr 1eJun 12; Exp. 6: Apr 7eMay 27; Exp. 7: Mar 4eApr 7; Exp. 8: Apr 7eMay 10. Numbers above each column show total number of scarabs caught.
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good performance of the ME-baited traps can be explained partly by the presence of (E)-anethol (which is a component in baits for both E. hirta and Cetonia/Potosia), but a possible synergism for E. hirta among the other components of the Cetonia/Potosia bait cannot be excluded and should be investigated further. Another factor could be related to the blue colour of both traps, as E. hirta is strongly attracted to objects in blue (Schmera et al., 2004; Tóth et al., 2005). Based on the results in the present study, for practical applications, the ME-baited traps could be used as “multi-species traps” in Europe for catching E. hirta, C. a. aurata and P. cuprea. This could be advantageous in situations where control of both E. hirta and Cetonia/Potosia is required, (i.e. on farms with orchard cultures with ripening fruit from spring to mid-summer). However, when only E. hirta needs to be controlled, the original bait targeted for this species may be more economical, since it contains only two components as opposed to four in the Cetonia/Potosia bait. Catches of E. hirta showed a tendency to be somewhat lower in PH-baited traps, with significant difference at two sites (Prkos HR, Telki HU: this experiment caught the largest total number of E. hirta). The performance of the PH-baited trap in catching E. hirta could be explained by the relatively high sensitivity of E. hirta to the visual stimulus of fluorescent yellow (Tóth et al., 2005), but the possible attractive activity of constituents in the O. funesta bait on E. hirta cannot be excluded and should be studied in more detail in the future. Catches of O. funesta were largest in PH-baited traps in the present study, supporting an earlier report (Vuts et al., 2008). The CA-baited traps caught negligible numbers from O. funesta. The somewhat higher activity of the ME-baited traps could be attributed to the presence of (þ)-lavandulol in both the O. funesta and the Cetonia/Potosia baits. For practical applications, if the damage is caused predominantly by O. funesta and the mass trapping of this species is targeted, for reliable results, the application of the PH-baited trap can be recommended. C. a. aurata and P. cuprea showed the strongest attraction to MEbaited traps, although at some sites the PH-baited traps also caught sizeable numbers. This could be explained by the presence of (þ)-lavandulol in both baits. The colour sensitivity of C. a. aurata and P. cuprea is not as overwhelming as in E. hirta or O. funesta (Tóth et al., 2005), so the different colour of the traps may have had only a minor influence. The lowest numbers of C. a. aurata and P. cuprea were generally found in CA-baited traps. For practical applications, the ME-baited traps appeared to work well in several regions in the present study and can be recommended for general use in Europe. T. squalida is a Mediterranean pest scarab with similar morphology, life habits, behavior and the damage it causes to the closely related E. hirta, which is abundant in more temperate Europe (Hurpin, 1962). In the present study, it was recorded in the traps in Sicily (Acireale I), where this was the only scarab captured, and near Rome I. T. squalida was caught in larger numbers by both CA-baited and ME-baited traps, which closely resembled responses of E. hirta. From this point of view, results from our site near Rome I are of particular interest, since both T. squalida and E. hirta were present and showed very similar responses. The good catch of T. squalida in the CA-baited traps is not surprising, since attraction of the same compounds as in the E. hirta bait [(E)-anethol plus (E)-cinnamyl alcohol] has already been reported for T. squalida (Ortu et al., 2001, 2003). Successful capture of T. squalida in the ME-baited traps could partly be explained by the presence of (E)-anethol, however, the effect of trap colour cannot be excluded. The colour sensitivity of T. squalida has not been studied in detail, but white objects have been
reported to attract the species (Ortu et al., 2001). E. hirta responds almost equally well to both white or blue (Tóth et al., 2005), and current results suggest that the blue colour can also be a significant cue for T. squalida. Tests to investigate this phenomenon are under way and will be published in detail elsewhere. For practical applications, both the CA-baited and ME-baited traps can be recommended for use when the capture of T. squalida is necessary. The scarab V. hemipterus, which is mostly known as a visitor of flowers (Hurpin, 1962), can damage Prunus L., Malus Mill. (Buresh and Lazarov, 1956), Rosa damascena Mill. (Nikolova, 1968), Castanea sativa Mill. (Ovcharov et al., 2007) and Tulipa L. (Horváth et al., 2007). This species was caught in low numbers at most sites, but at Bascica HR, significantly more beetles were caught in ME-baited traps than in the other two treatments. (E)-Cinnamyl alcohol has previously been reported to attract V. hemipterus (Tóth et al., 2003). This compound was present only in the E. hirta bait in the present study. If the practical need to capture V. hemipterus arises in the future, more detailed studies are necessary on the activity of constituents of the Cetonia/Potosia bait vs. (E)-cinnamyl alcohol and their combinations. Further research will optimize attractive chemical and visual cues for T. squalida, and develop “multi-species” traps with a wider species-range, possibly targeting O. funesta and other pest cetoniins. Acknowledgement This work was partially supported by grant DO02-244/2008 of the Bulgarian National Scientific Fund, by OTKA grant K 81494 of HAS and by the grant of KUKBOGMV OM-00063/2008 JÁP. References Buresh, I., Lazarov, A., 1956. Vrednite nasekomi za selskoto i gorskoto stopanstvo v Balgariya. Balgarska Akademiya na naukite, Sofiya. 289 str. (in Bulgarian). Homonnay, F., Homonnayné-Csehi, É, 1990. Cserebogarak e Melolonthidae. In: Jermy, T., Balázs, K. (Eds.), A növényvédelmi állattan kézikönyve (Handbook of Plant Protection Zoology), vol. 3/A. Akadémiai Kiadó, Budapest, pp. 156e215 (in Hungarian). Horváth, Z., Kiss, T., Lévai, P., Vecseri, Cs., Vörös, G., 2007. A szabadföldi tulipán védelme. Növényvédelem 43, 71e86. Hurpin, B., 1962. Super-famille des Scarabaeoidea. In: Balachowsky, A.S. (Ed.), Entomologie appliquée á l’agriculture. Masson et Cie Éditeurs, Paris, pp. 24e204. Imrei, Z., Tóth, M., Tolasch, T., Francke, W., 2001. 1,4-Benzoquinone attracts males of Rhizotrogus vernus Germ. Z. Naturforsch. C 57, 177e181. Jaccard, J., Becker, M.A., Wood, G., 1984. Pairwise multiple comparison procedures: a review. Psychol. Bull. 96, 589e596. Mircheva, A., Subchev, M., Sredkov, I., Tóth, M., 2004. Seasonal flight of Epicometis hirta Poda (Coleoptera, Scarabaeidae) established by attractant traps. Annuaire de l’Université de Sofia “St. Kliment Ohridski” 96, 201e204. Nikolova, V., 1968. Entomotsenologichni i biologichni prouchvaniya v nasazhdeniya s maslodajna roza. II. Coleoptera. Izv. Zool. Inst. Muzej 26, 119e155 (in Bulgarian, with Russian abstract). Ortu, S., Lentini, A., Acciaro, M., 2001. Observations préliminaires sur les infestations de Tropinota squalida (Scopoli) dans les vignobles en Sardaigne. IOBC WPRS Bull. 24, 113e116. Ortu, S., Lentini, A., Pilo, C., Foxi, C., 2003. Observations on the efficacy of different traps in capturing Tropinota squalida (Scopoli). IOBC WPRS Bull. 26, 163e166. Ovcharov, D., Doychev, D., Dimitrova, P., 2007. Insects feeding on the sweet chestnut (Castanea sativa Mill.) in Bulgaria. In: Bratanova-Doncheva, S. (Ed.), Sustainable Management of Sweet Chestnut Ecosystems. CAST Bulletin Reports, Sofia, pp. 173e182. Razov, J., Baric, B., Tóth, M., 2008. Population dynamics and damage analysis of Cetonia aurata/Potosia cuprea in Croatian peach orchards. In: VII IOBC International Conference of Integrated Fruit Production, Avignon, France, 27e30 October, 2008. Roelofs, W.L., Cardé, R.T., 1977. Responses of Lepidoptera to synthetic sex pheromone chemicals and their analogues. Annu. Rev. Entomol. 22, 377e405. Schmera, D., Tóth, M., Subchev, M., Sredkov, I., Szarukán, I., Jermy, T., Szentesi, Á, 2004. Importance of visual and chemical cues in the development of an attractant trap for Epicometis (Tropinota) hirta Poda (Coleoptera: Scarabaeidae). Crop Prot. 23, 939e944.
J. Vuts et al. / Crop Protection 29 (2010) 1177e1183 Sivcev, I., Tóth, M., Tomasev, I., 2006. Application of attractants in control of the sugar-beet weevil and the blossom feeder scarab (Bothynoderes punctiventris, Epicometis hirta). Poljoprivedni Kalendar 2006, 138e140 (in Serbian). Tóth, M., Klein, M.G., Imrei, Z., 2003. Field screening for attractants of scarab pests in Hungary (Coleoptera: Scarabaeidae). Acta Phytopath. Entomol. Hung. 38, 323e331. Tóth, M., Schmera, D., Imrei, Z., 2004. Optimization of a chemical attractant for Epicometis (Tropinota) hirta Poda. Z. Naturforsch. C 59, 288e292. Tóth, M., Imrei, Z., Szarukán, I., Voigt, E., Schmera, D., Vuts, J., Harmincz, K., Subchev, M., 2005. Gyümölcs- ill. virágkárokat okozó cserebogárfélék kémiai kommunikációja: egy évtized kutatási eredményei. Növényvédelem 41, 581e588 (in Hungarian, with English abstract).
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Tóth, M., Voigt, E., Imrei, Z., Szarukán, I., Schmera, D., Vuts, J., Harmincz, K., Subchev, M., Sivcev, I., 2006. Semiochemical-baited traps for scarab pests damaging fruits and blossoms. In: 58th International Symposium on Crop Protection, Gent, Belgium, 23 May, 2006. Voigt, E., Tóth, M., Imrei, Z., Vuts, J., Szöllös, L., Szarukán, I., 2005. A zöld cserebogár és az aranyos rózsabogár növekvö kártétele és a környezetkímélö védekezés lehetöségei. Agrofórum 16, 63e64 (in Hungarian). Vuts, J., Imrei, Z., Tóth, M., 2008. Development of an attractant-baited trap for Oxythyrea funesta Poda (Scarabaeidae, Cetoniinae). Z. Naturforsch. C 63, 761e768. Vuts, J., Imrei, Z., Tóth, M., 2010. New co-attractants synergizing attraction of Cetonia aurata aurata and Potosia cuprea to the known floral attractant. J. Appl. Entomol. 134, 9e15.
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Performance and selectivity of floral attractant-baited traps targeted for cetoniin scarabs (Coleoptera: Scarabaeidae) in Central and Southern Europe J. Vuts a, *, B. Baric b, J. Razov c, T.B. Toshova d, M. Subchev d, I. Sredkov e, R. Tabilio f, F. Di Franco g, M. Tóth a a
Plant Protection Institute, HAS, Herman O. u. 15, H-1022 Budapest, Hungary University of Zagreb, Faculty of Agriculture, Department of Agricultural Zoology, Svetosimunska 25, HR-10000 Zagreb, Croatia c University of Zadar, Department of Mediterranean Agriculture and Aquaculture, Mihovila Pavlinovica bb., HR-23000 Zadar, Croatia d Zoology Institute, Bulgarian Academy of Sciences, blvd. Tzar Osvoboditel 1, BG-1000 Sofia, Bulgaria e Institute of Agronomy, Sofijskko shose, BG-2500 Kyustendil, Bulgaria f Centro di Ricerca per la Frutticoltura di Roma, Via di Fioranello 52, I-00040 Ciampino Airport (RM), Italy g CRA e Centro di Ricerca per l’Agrumicoltura e le Colture Meridionali, Corso Savoia 190, I-95024 Acireale (Catania), Italy b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 January 2010 Received in revised form 12 May 2010 Accepted 13 May 2010
Trapping tests were performed concurrently in several countries of Central and Southern Europe throughout the spring and summer of 2008, to study the selectivity and performance of floral attractantbaited traps developed for catching Epicometis (Tropinota) hirta Poda (CA-baited traps), Cetonia a. aurata L./Potosia (Protaetia) cuprea Fabr. (ME-baited traps) or Oxythyrea funesta Poda (PH-baited traps) (Coleoptera: Scarabaeidae, Cetoniinae). Amongst the species caught, E. hirta showed strongest attraction to the CA-baited and ME-baited traps. O. funesta was mostly caught by PH-baited traps. In capturing C. a. aurata and P. cuprea, the ME-baited trap appeared to be the most efficient. At two sites in Italy, a related scarab, Tropinota squalida Scop. (Coleoptera: Scarabaeidae, Cetoniinae), was attracted in similar numbers to both CA-baited and ME-baited traps. For the scarab Valgus hemipterus L. (Coleoptera: Scarabaeidae, Valginae), ME-baited traps proved to be the most attractive. Of the scarabs coming to the CA-baited trap, E. hirta was the most abundant, except at the two Italian sites where large percentages were shown to be T. squalida. The most abundant species in the catch by the PH-baited trap was O. funesta, although at some sites, C. a. aurata and E. hirta were captured in sizeable numbers. ME-baited traps caught mostly C. a. aurata at sites with large C. a. aurata populations, whereas at sites with low populations, good numbers of E. hirta or T. squalida were caught. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Cetoniins Mass trapping Control strategies Scarab pests Monitoring
1. Introduction Many species in the subfamily Cetoniinae (Coleoptera: Scarabaeidae) are of agricultural importance. The adult beetles cause damage by feeding on the reproductive parts of fruit trees and ornamental plants, and also on ripening fruit later in the season (Hurpin, 1962). Control of these species is difficult, since most insecticides cannot be applied during flowering without affecting honeybees and other beneficial insects, or before harvest because of health hazards. Mass trapping of adult beetles can be an alternative control method, provided that an efficient trapping system is available. In Europe, the most important cetoniin pest is Epicometis (Tropinota) hirta Poda (Hurpin, 1962; Homonnay and HomonnaynéCsehi, 1990; Mircheva et al., 2004). A binary chemical attractant * Corresponding author. Tel.: þ36 1 391 8647; fax: þ36 1 391 8655. E-mail address: [email protected] (J. Vuts). 0261-2194/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2010.05.007
comprising (E)-cinnamyl alcohol and (E)-anethol has been optimized previously and proved to be attractive to adult E. hirta beetles (Tóth et al., 2003, 2004). Application of this binary chemical attractant, together with a light blue colour in funnel traps, resulted in significantly higher catches than in traps containing either the chemical or the visual cue alone (Schmera et al., 2004). The first attempts at mass trapping trials in strawberry plantations and apple orchards against E. hirta using attractant-baited light blue traps were reported by Sivcev et al. (2006) and Tóth et al. (2005). Reports of significant damage by Cetonia a. aurata L. and Potosia (Protaetia) cuprea Fabr. in Hungary have increased in frequency during recent years (Voigt et al., 2005). This indicates that the significance of these pest species is growing. A ternary chemical attractant comprising 3-methyl eugenol, 1-phenylethanol and (E)anethol was optimized previously and proved to be attractive to adults of C. a. aurata and P. cuprea (Tóth et al., 2005). C. a. aurata and P. cuprea were attracted in higher numbers to a light blue, rather than to other colours tested in the presence of their floral attractant
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(Tóth et al., 2005). Light blue traps baited with the ternary attractant are in use today in Central Europe for monitoring and mass trapping of C. a. aurata and P. cuprea (Voigt et al., 2005; Tóth et al., 2006; Razov et al., 2008). More recently, the addition of ()-lavandulol to the known ternary bait increased catches of C. a. aurata and P. cuprea significantly, providing a more efficient attractant for these scarabs (Vuts et al., 2010). The cetoniin scarab Oxythyrea funesta Poda can also cause occasional damage in orchards (Hurpin, 1962; Tóth et al., 2005). A fluorescent yellow trap exploiting the strong attractancy of O. funesta to this colour (Tóth et al., 2005), and baited with the binary lure of ()-lavandulol and 2-phenylethanol, has been developed for monitoring and mass trapping of this scarab (Vuts et al., 2008). The objective of the present research was to study the performance and selectivity in catching cetoniin scarabs of traps developed for E. hirta, Cetonia/Potosia or O. funesta, respectively, throughout the spring and summer in 2008. Parallel tests were conducted in several Central and Southern European countries. 2. Material and methods 2.1. Baits To prepare the bait dispensers, a 1 cm piece of dental roll (CelluronÒ, Paul Hartmann AG, Heidenheim, Germany) was placed into a tight polythene bag made of 0.02 mm linear polyethylene foil (ca. 1.5 1.5 cm). The dispenser was attached to a plastic strip (8 1 cm) for easy handling when assembling the traps. For making up the baits, compounds were administered onto the dental roll and the polythene bag was heat-sealed. Previous experience showed that bait activity was not reduced after several weeks of field exposure, so we decided that it was safe to renew the lures at 2e3-week-intervals (Tóth et al., unpublished data). Details of treatments set up in the tests are shown in Table 1. Dispensers were wrapped singly in pieces of alufoil and were stored at 30 C before use. Synthetic compounds were obtained from SigmaeAldrich Kft. (Budapest, Hungary). All compounds were >95% pure as stated by the supplier.
Table 2 Details of field tests. HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary. Experiment
Locality
Biotop
Period
1
Bascica (HR)
March 26eAugust 19, 2008
2 3
Prkos (HR) Zagreb (HR)
4 5 6 7 8
Kyustendil (BG) Sofia (BG) Rome (I) Acireale (I) Telki (HU)
Edge of a mixed orchard mixed orchard Edge of a mixed orchard Mixed orchard Mixed orchard Mixed orchard Mixed orchard Bushy edge of an oak forest
March 26eAugust 19, 2008 April 9eAugust 20, 2008 March 28eAugust 9, 2008 March 25eJuly 29, 2008 April 1eAugust 4, 2008 March 4eJuly 1, 2008 April 3eAugust 29, 2008
2.3. Field tests Experiments were conducted concurrently in several countries in Europe in 2008. Traps were set up in a randomized complete block design (number of blocks: 4, number of traps/site: 12). The distance between traps was 10e15 m, with a minimum distance of 25 m between blocks. Traps were set up in sunny places with no shade of trees or buildings, attached to poles at a 30e40 cm height above the ground. Traps were inspected twice weekly. Captured insects were removed, their species identified and numbers recorded. Details of each experiment are presented in Table 2. 2.4. Statistics Catches were transformed using (x þ 0.5)1/2 as suggested by Roelofs and Cardé (1977) for similar experiments and were analyzed by ANOVA. Treatment means were separated by the GameseHowell post hoc test (Jaccard et al., 1984). All statistical procedures were conducted using the software packages StatViewÒ v4.01 and SuperANOVAÒ v1.11 (Abacus Concepts Inc., Berkeley, CA). 3. Results
2.2. Traps In the tests, CSALOMONÒ VARb3 modified funnel traps (produced by Plant Prot. Inst., HAS, Budapest, Hungary) were used, which proved to be excellent for the capture of related scarabs (i.e. Imrei et al., 2001; Schmera et al., 2004). Photos of VARb3 traps can be viewed at www.julia-nki.hu/traps. The upper funnels of VARb3 traps developed for catching E. hirta or Cetonia/Potosia were light blue, while fluorescent yellow was used for traps developed for catching O. funesta. For the reflectance spectra of these colours, see Schmera et al. (2004). Later on in the text, the trap for the capture of E. hirta will be referred to as CA-baited trap due to the unique (E)cinnamyl alcohol content of its bait. Similarly, the trap for capturing Cetonia/Potosia will be referred to as ME-baited trap due to the 3-methyl eugenol content of its bait, and the trap developed for O. funesta will be referred to as PH-baited trap because of 2-phenylethanol.
3.1. E. hirta Except in Acireale Italy (I), where no E. hirta catches were observed, the PH-baited trap caught fewer beetles than CA-baited or ME-baited traps; at all sites except Zagreb Croatia (HR), the differences were significant (Fig. 1). There were no statistical differences observed between the catches of CA-baited or MEbaited traps. 3.2. O. funesta Catches of O. funesta were highest in PH-baited traps (Fig. 1). ME-baited traps were generally more attractive to O. funesta than CA-baited traps; at Bascica HR and Telki Hungary (HU), the differences were significant.
Table 1 Details of treatments tested. Treatment
A B C
Trap
ME-baited PH-baited CA-baited
Bait composition (mg)
Trap colour
(E)-Anethol
3-Methyl eugenol
1-Phenylethanol
(E)-Cinnamyl alcohol
()-Lavandulol
2-Phenylethanol
100 e 200
100 e e
100 e e
e e 200
100 200 e
e 200 e
Blue Fluorescent yellow Blue
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3.3. C. a. aurata
3.4. P. cuprea
In all sites where C. a. aurata was found, ME-baited traps were the most effective in attracting C. a. aurata, followed by PH-baited or CA-baited traps (Fig. 1).
This species was only captured in Prkos HR and Telki HU, where ME-baited traps attracted more P. cuprea beetles than the other two traps (Fig. 1).
Fig. 1. Mean catches of scarabs at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary) in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp. Columns with the same letter within one diagram are not significantly different at P ¼ 5% by ANOVA, GameseHowell. Total catches of less than 15 beetles in an experiment were categorized as ‘Very low numbers caught’ and are not shown in the figure.
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3.5. Other scarabs Tropinota squalida Scop. was observed only at Rome I and Acireale I, where it was attracted to CA-baited and ME-baited traps in similar numbers (Fig. 1). Valgus hemipterus L. (Coleoptera: Scarabaeidae, Valginae) was caught in high numbers only at Bascica HR and mostly in ME-baited traps (Fig. 1). Only low numbers were found in CA-baited or PHbaited traps. 3.6. Selectivity of the traps 3.6.1. ME-baited traps C. a. aurata was the most abundant cetoniin species collected at the two sites with the largest C. a. aurata populations (Zagreb HR and Telki HU) (70% and 76%, resp.) (Fig. 2). At sites with low C. a. aurata populations, good numbers of E. hirta were caught (ranging
from 90% to 31%). At Acireale I, T. squalida was the most abundant species caught in ME-baited traps (97%). At Rome I and Sofia Bulgaria (BG), C. a. aurata was absent. P. cuprea was caught in larger numbers at Telki HU (8%), while at other sites, it was recorded only in low numbers ranging from 12% to 0.4% of total catch. P. cuprea was absent at Kyustendil (BG), Sofia BG, Rome I and Acireale I. 3.6.2. PH-baited traps At 4 sites, O. funesta was caught in percentages ranging from 87% to 35% (Fig. 2). At Telki HU, C. a. aurata and at Prkos HR, E. hirta were caught in sizable numbers. At Kyustedil BG, very low (6%), and at Acireale I, no O. funesta catches were observed in PH-baited traps. 3.6.3. CA-baited traps Except for the two sites in Italy, E. hirta comprised 100% to 54% of the total captures in these traps (Fig. 2). At Rome I, 57% of the total catch was the closely related T. squalida. At Acireale I, only
Fig. 2. Percentage distribution of total catches of scarabs in the whole experimental period in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp., at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary). Numbers above each column show total number of scarabs caught.
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T. squalida was collected, suggesting that E. hirta was absent at that location. The second most abundant species in CA-baited traps was C. a. aurata, ranging from 40% to 6%, while O. funesta ranged from 23% to 2%. Only small numbers of P. cuprea (3e1% of total catch) and V. hemipterus (15e1%) were caught in CA-baited traps. The selectivity of the traps studied in the present project was influenced by the local occurrence of the target species and the relative abundance of the other cetoniins at any given site. Thus, even the most selective trap tested in this study, the PH-baited trap, caught cetoniins other than O. funesta in large percentages where O. funesta was evidently present in low populations, or was not present at all. Another factor to consider is that selectivity of a given trap calculated for the whole season may be significantly different from selectivity of the same trap during the main flight period of the
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target species (which may occur before or after flights of other related species coming to the trap). Thus, for example, the 54% E. hirta selectivity of the CA-baited trap at Telki HU (Fig. 2) becomes 94% if we consider only the main flight period (between April 7 and May 10 at this site) of E. hirta (Fig. 3) and, likewise, the 41% Cetonia/ Potosia selectivity of the ME-baited trap at Prkos HR becomes 99% if we consider only the main flight period (between June 27 and July 23 at this site) of C. a. aurata and P. cuprea (see also Fig. 3). 4. Discussion In the present experiments, equally large numbers of E. hirta were caught in CA-baited and ME-baited traps. Previously, we had no data on the performance of the ME-baited trap early in the spring, when E. hirta is flying (Tóth et al., 2005). The surprisingly
Fig. 3. Percentage distribution of total catches of scarabs in the main flight period of the target species in ME-baited (developed for catching Cetonia/Potosia), PH-baited (developed for catching O. funesta) and CA-baited (developed for catching E. hirta) traps, resp., at the experimental sites (HR: Croatia, BG: Bulgaria, I: Italy, HU: Hungary). Period shown for Cetonia/Potosia: Exp. 1: May 30eJun 9; Exp. 2: Jun 27eJul 23; Exp. 3: Jul 2eAug 6; Exp. 4: Apr 24eAug 9; Exp. 5: Apr 30eJul 29; Exp. 6: Jun 4eAug 4; Exp. 7: May 15eJul 1; Exp. 8: Jun 24eAug 4. For O. funesta: Exp. 1: May 30eJul 11; Exp. 2: Apr 21eJun 5; Exp. 3: Apr 30eJul 2; Exp. 4: Jun 2eAug 9; Exp. 5: May 26eJul 29; Exp. 6: Apr 14eAug 4; Exp. 7: Mar 4eJul 1; Exp. 8: May 10eJun 19. For E. hirta: Exp. 1: Mar 31eMay 30; Exp. 2: Mar 31eMay 19; Exp. 3: Apr 16eMay 14; Exp. 4: Mar 31eApr 29; Exp. 5: Apr 1eJun 12; Exp. 6: Apr 7eMay 27; Exp. 7: Mar 4eApr 7; Exp. 8: Apr 7eMay 10. Numbers above each column show total number of scarabs caught.
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good performance of the ME-baited traps can be explained partly by the presence of (E)-anethol (which is a component in baits for both E. hirta and Cetonia/Potosia), but a possible synergism for E. hirta among the other components of the Cetonia/Potosia bait cannot be excluded and should be investigated further. Another factor could be related to the blue colour of both traps, as E. hirta is strongly attracted to objects in blue (Schmera et al., 2004; Tóth et al., 2005). Based on the results in the present study, for practical applications, the ME-baited traps could be used as “multi-species traps” in Europe for catching E. hirta, C. a. aurata and P. cuprea. This could be advantageous in situations where control of both E. hirta and Cetonia/Potosia is required, (i.e. on farms with orchard cultures with ripening fruit from spring to mid-summer). However, when only E. hirta needs to be controlled, the original bait targeted for this species may be more economical, since it contains only two components as opposed to four in the Cetonia/Potosia bait. Catches of E. hirta showed a tendency to be somewhat lower in PH-baited traps, with significant difference at two sites (Prkos HR, Telki HU: this experiment caught the largest total number of E. hirta). The performance of the PH-baited trap in catching E. hirta could be explained by the relatively high sensitivity of E. hirta to the visual stimulus of fluorescent yellow (Tóth et al., 2005), but the possible attractive activity of constituents in the O. funesta bait on E. hirta cannot be excluded and should be studied in more detail in the future. Catches of O. funesta were largest in PH-baited traps in the present study, supporting an earlier report (Vuts et al., 2008). The CA-baited traps caught negligible numbers from O. funesta. The somewhat higher activity of the ME-baited traps could be attributed to the presence of (þ)-lavandulol in both the O. funesta and the Cetonia/Potosia baits. For practical applications, if the damage is caused predominantly by O. funesta and the mass trapping of this species is targeted, for reliable results, the application of the PH-baited trap can be recommended. C. a. aurata and P. cuprea showed the strongest attraction to MEbaited traps, although at some sites the PH-baited traps also caught sizeable numbers. This could be explained by the presence of (þ)-lavandulol in both baits. The colour sensitivity of C. a. aurata and P. cuprea is not as overwhelming as in E. hirta or O. funesta (Tóth et al., 2005), so the different colour of the traps may have had only a minor influence. The lowest numbers of C. a. aurata and P. cuprea were generally found in CA-baited traps. For practical applications, the ME-baited traps appeared to work well in several regions in the present study and can be recommended for general use in Europe. T. squalida is a Mediterranean pest scarab with similar morphology, life habits, behavior and the damage it causes to the closely related E. hirta, which is abundant in more temperate Europe (Hurpin, 1962). In the present study, it was recorded in the traps in Sicily (Acireale I), where this was the only scarab captured, and near Rome I. T. squalida was caught in larger numbers by both CA-baited and ME-baited traps, which closely resembled responses of E. hirta. From this point of view, results from our site near Rome I are of particular interest, since both T. squalida and E. hirta were present and showed very similar responses. The good catch of T. squalida in the CA-baited traps is not surprising, since attraction of the same compounds as in the E. hirta bait [(E)-anethol plus (E)-cinnamyl alcohol] has already been reported for T. squalida (Ortu et al., 2001, 2003). Successful capture of T. squalida in the ME-baited traps could partly be explained by the presence of (E)-anethol, however, the effect of trap colour cannot be excluded. The colour sensitivity of T. squalida has not been studied in detail, but white objects have been
reported to attract the species (Ortu et al., 2001). E. hirta responds almost equally well to both white or blue (Tóth et al., 2005), and current results suggest that the blue colour can also be a significant cue for T. squalida. Tests to investigate this phenomenon are under way and will be published in detail elsewhere. For practical applications, both the CA-baited and ME-baited traps can be recommended for use when the capture of T. squalida is necessary. The scarab V. hemipterus, which is mostly known as a visitor of flowers (Hurpin, 1962), can damage Prunus L., Malus Mill. (Buresh and Lazarov, 1956), Rosa damascena Mill. (Nikolova, 1968), Castanea sativa Mill. (Ovcharov et al., 2007) and Tulipa L. (Horváth et al., 2007). This species was caught in low numbers at most sites, but at Bascica HR, significantly more beetles were caught in ME-baited traps than in the other two treatments. (E)-Cinnamyl alcohol has previously been reported to attract V. hemipterus (Tóth et al., 2003). This compound was present only in the E. hirta bait in the present study. If the practical need to capture V. hemipterus arises in the future, more detailed studies are necessary on the activity of constituents of the Cetonia/Potosia bait vs. (E)-cinnamyl alcohol and their combinations. Further research will optimize attractive chemical and visual cues for T. squalida, and develop “multi-species” traps with a wider species-range, possibly targeting O. funesta and other pest cetoniins. Acknowledgement This work was partially supported by grant DO02-244/2008 of the Bulgarian National Scientific Fund, by OTKA grant K 81494 of HAS and by the grant of KUKBOGMV OM-00063/2008 JÁP. References Buresh, I., Lazarov, A., 1956. Vrednite nasekomi za selskoto i gorskoto stopanstvo v Balgariya. Balgarska Akademiya na naukite, Sofiya. 289 str. (in Bulgarian). Homonnay, F., Homonnayné-Csehi, É, 1990. Cserebogarak e Melolonthidae. In: Jermy, T., Balázs, K. (Eds.), A növényvédelmi állattan kézikönyve (Handbook of Plant Protection Zoology), vol. 3/A. Akadémiai Kiadó, Budapest, pp. 156e215 (in Hungarian). Horváth, Z., Kiss, T., Lévai, P., Vecseri, Cs., Vörös, G., 2007. A szabadföldi tulipán védelme. Növényvédelem 43, 71e86. Hurpin, B., 1962. Super-famille des Scarabaeoidea. In: Balachowsky, A.S. (Ed.), Entomologie appliquée á l’agriculture. Masson et Cie Éditeurs, Paris, pp. 24e204. Imrei, Z., Tóth, M., Tolasch, T., Francke, W., 2001. 1,4-Benzoquinone attracts males of Rhizotrogus vernus Germ. Z. Naturforsch. C 57, 177e181. Jaccard, J., Becker, M.A., Wood, G., 1984. Pairwise multiple comparison procedures: a review. Psychol. Bull. 96, 589e596. Mircheva, A., Subchev, M., Sredkov, I., Tóth, M., 2004. Seasonal flight of Epicometis hirta Poda (Coleoptera, Scarabaeidae) established by attractant traps. Annuaire de l’Université de Sofia “St. Kliment Ohridski” 96, 201e204. Nikolova, V., 1968. Entomotsenologichni i biologichni prouchvaniya v nasazhdeniya s maslodajna roza. II. Coleoptera. Izv. Zool. Inst. Muzej 26, 119e155 (in Bulgarian, with Russian abstract). Ortu, S., Lentini, A., Acciaro, M., 2001. Observations préliminaires sur les infestations de Tropinota squalida (Scopoli) dans les vignobles en Sardaigne. IOBC WPRS Bull. 24, 113e116. Ortu, S., Lentini, A., Pilo, C., Foxi, C., 2003. Observations on the efficacy of different traps in capturing Tropinota squalida (Scopoli). IOBC WPRS Bull. 26, 163e166. Ovcharov, D., Doychev, D., Dimitrova, P., 2007. Insects feeding on the sweet chestnut (Castanea sativa Mill.) in Bulgaria. In: Bratanova-Doncheva, S. (Ed.), Sustainable Management of Sweet Chestnut Ecosystems. CAST Bulletin Reports, Sofia, pp. 173e182. Razov, J., Baric, B., Tóth, M., 2008. Population dynamics and damage analysis of Cetonia aurata/Potosia cuprea in Croatian peach orchards. In: VII IOBC International Conference of Integrated Fruit Production, Avignon, France, 27e30 October, 2008. Roelofs, W.L., Cardé, R.T., 1977. Responses of Lepidoptera to synthetic sex pheromone chemicals and their analogues. Annu. Rev. Entomol. 22, 377e405. Schmera, D., Tóth, M., Subchev, M., Sredkov, I., Szarukán, I., Jermy, T., Szentesi, Á, 2004. Importance of visual and chemical cues in the development of an attractant trap for Epicometis (Tropinota) hirta Poda (Coleoptera: Scarabaeidae). Crop Prot. 23, 939e944.
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