biologique et intégrée (PBI) en cultures de fleurs coupées sous serres, situations et applications en France. Phytoma. La défense des végétaux 529: 14-17.
Survey of thrips species in horticultural greenhouses in Southern France J. Pizzol, D. Nammour, S. Voisin, M. Ziegler, N. Desneux, C. Poncet INRA±UR 880 URIH 400, route des Chappes, BP 16 06 903 Sophia-Antipolis France
P. Reynaud Anses Laboratoire de la Santé des Végétaux, 7, rue Jean Dixméras, 49044 Angers cedex 01, France
Key words: Thrips, sampling, greenhouse, rose, gerbera Abstract Thrips are widespread pests in ornamental greenhouses in France. The survey of thrips populations in greenhouses on rose and gerbera crops in two sites in Southern France, at the I NRA Research Center (Sophia-Antipolis, France) and at the CREAT Experimental Center (Nice, France), were performed from 2006 to 2009. During that period, more than 6000 thrips were collected using direct sampling on a weekly basis. Nine genera and nineteen different species were identified. Frankliniella occidentalis (Pergande) and Thrips tabaci Lindeman [Thysanoptera: Thripidae], respectively 81.5% and 16.5% , were the most abundant. Two new species were observed; one in France i.e. the Scirtothrips inermis Priesner and one in Europe i.e. the Thrips hawaiiensis (M organ). Two predators belonging to the Aeolothrips [Thysanoptera: Aeolothrips] genera were also present, the Aeolothrips tenuicornis Bagnall and the A. ericae Bagnall as well as one to the Scolothrips: Scolothrips longicornis Priesner genus.
I NTRODUCTI ON
Thrips are widespread crop pests and approximately 5500 species are currently known in the world, belonging to over 750 genera; 1% are considered harmful. In France, there are approximately 350 species of Thysanoptera, of which twenty have real agronomic impact (Reynaud, 1998). These insects are particularly invasive. Long-distance transport of plants and crops have made it easier for them to be introduced and to spread. It is very difficult to keep them at bay in many greenhouse vegetables e.g. cucumbers, peppers, etc. (Ridray and Lacordaire, 2007) or on ornamental crops e.g. anthurium, roses, etc. (LhosteDrouineau, 2005; Brun et al., 2004). On roses, they cause significant direct damage affecting esthetic appearance and production (Morse et al., 2006; Poncet et al., 2010) and this usually prompts the use of pesticides to prevent yield losses. However, it is well known that there are problems connected to extensive use of insecticides: resistant strains can appear in pests (Humeres and Morse, 2006) and chemicals can have negative effects on human health and nontarget organisms (Desneux et al., 2006a, 2006b; Desneux et al., 2007; Weisenberger, 1993). In France, the rose is the main marketed plant species and much of the flower production is done in greenhouses. In 2001, in Europe, French roses rank 3rd behind the Netherlands and Italy in terms of acreage: 300 hectares. The Var produces 38%, making the French Riviera the principal producing region (Emery et al., 2005). In 1999, rose
crops also represented 14% of the area of cut flowers that used Integrated Pest Management (IPM) (Mary et al., 2000). Keeping thrips species below economic thresholds is difficult to implement. Therefore, it is necessary to develop a strategy for efficient, optimal protection against thrips on ornamental plants and on rose crops in particular. In this study, we surveyed and identified the thrips species present on two greenhouse crops in France.
M ATERI ALS AND M ETHODS
We collected the thrips inside rose greenhouses at the INRA-URIH site in SophiaAntipolis (site 1) and at the CREAT site in La Baronne (site 2), both sites are located in Southern France. Site 1 Span n° 1: In 2006, 2007 and 2008, samples were taken from the following rose varieties: Sonia, Milva, Suela, Magnum as well as from other rose varieties, all potted plants and crop conduced using an IPM program. PIC greenhouse spans 2-3-4: The samples were taken in 2006, 2007, 2008 and 2009, on greenhouse roses planted in rockwool and using IPM in the PIC greenhouse (spans 2, 3 and 4); these spans were not separated. Each span has five double rows of roses and three cultivars on each row (cv. Magnum, cv. Milva, cv. Suela). Three varieties of roses were planted on May 6, 2003, gathered on May 14, 2008, and a single variety, Dark Milva was then planted. Other greenhouses: In 2006, 2007, 2008 and 2009 samplings were taken from roses planted in rockwool and cultivated using IPM. The Aubade variety was planted on April 28, 2006, in 12 small 1m x 2m compartments and on May 15, 2008, in three compartments approximately 40m2 (6.2m x 6.2m). In two 250 m2 greenhouse compartments, the rose cultivar ³Akito Sweet´ was planted in coconut fibre, on June 28th, 2006. In all these greenhouses, the roof-vent was equipped with nets. Site 2 On roses: The study was carried out in 2006 at the CREAT Experimental Center (Centre GH5HFKHUFKHV(FRQRPLTXHVHWG¶$FWLRQV7HFKQLTXHs) in La Baronne (Nice). Two 130 m2 greenhouses (13m x 10m) were used, without insect nets over the openings. Each contained three varieties of roses: Aubade, Miss Paris and Sayonara, with two double rows of each variety. The roses were grown in either perlite or coconut fibre. On gerbera: The study was also carried out at the CREAT Experimental Center in La Baronne (Nice) in 2007 and 2008. Two 50 m2 greenhouses oriented east-west were used, without insect nets over the openings. Each contained two gerbera varieties, the yellow Dino and the red Alcatraz. Sampling In all sites and all greenhouses, thrips were collected. Rose or gerbera flowers were lightly tapped three times onto a white sheet of paper on a rigid support. If any thrips were detected on the paper, the rose was tapped again for as long as thrips continued to drop onto the paper (Pizzol et al., 2006 and 2010). Then, using a brush, adults were collected to be identified. Identifying larvae is difficult (Mound and Kibly, 1998) so the samples were only adults and they were deposited inside Eppendorf tubes, containing 2
ml of wetting solution in 10% alcohol. This solution was adapted to allow identification at a further date of the thrips without breaking their key body parts (Reynaud et al., 2008). Thrips identification: The conditioned samples were identified in the French National Laboratory of Plant Protection in Angers. Thrips were observed first using a stereomicroscope (LEICA MZ12 magnified 8 to 100 times) Then they were placed in lactic acid to be examined under an optical microscope (LEICA DMLB2 magnified 50 to 630). When required, preparations between slide and coverslip were done in Canada balsam. The identification key of Zur-Strassen (2003) (Reynaud et al., 2008) was used for species indentification.
RESULTS I - Thrips survey on site 1 (Sophia-Antipolis, France) - Species present inside the PI C greenhouse - span 1 Five thrips species were recorded in the greenhouse: Frankliniella occidentalis, Thrips tabaci, F. intonsa Trybom, T. flavus Schrank and Scirtothrips inermis Priesner among the 71 samples and over 638 specimens collected on roses. Many F. occidentalis and T. tabaci were present, and represented respectively 84% and 14% of thrips recorded from 2006 to 2008 (Fig. 1). Occasionally, F. intonsa, T. flavus and S. inermis were found but they represented only 2.35% of the total number of thrips (Fig. 1 and Table 1). - Species present inside PI C greenhouse - spans 2-3-4 Seven thrips species were identified within the greenhouse: F. occidentalis, T. tabaci, T. hawaiiensis Morgan, T. major Uzel, T. minutissimus Linnaeus, T. flavus and S. inermis; these were found among the 316 samples and over 2,706 specimens collected from all roses. Frankliniella occidentalis and T. tabaci were the most dominant collected species with respectively 80% and 19% thrips recorded from 2006 to 2009 (Fig. 2). T. hawaiiensis, T. major, T. minutissimus, T. flavus and S. inermis were only occasionally found (Fig. 2 and Table 1). - Species present inside other greenhouses Nine species were identified in the other group of URIH greenhouses, from the 193 samples and 1,542 thrips. The following thrips species were found: Aeolothrips tenuicornis Bagnall, F. occidentalis, Odontothrips dorycnii Priesner, Pezothrips kellyanus Bagnall, S. inermis, Scolothrips longicornis Priesner, T. flavus, T. major and T. tabaci. Frankliniella occidentalis represented 85% of the total number of thrips, T. tabaci 12% and the 7 other species represented 3% (Fig. 3 and Table 1). I I - Thrips survey on site 2 (La Baronne, France) Eight thrips species were identified: A. ericae Bagnall, A. tenuicornis, Ceratothrips ericae Haliday, F. occidentalis, Tenothrips discolor Karny, T. flavus, T. major and T. tabaci on the 145 samples collected and on 1,127 thrips samples collected i.e. 276 samples on roses and 851 samples on gerbera.
- Species found on roses: On the rose crop, F. occidentalis represented 53% of the samples, T. tabaci 43% and 5% for these other species (A. ericae, A. tenuicornis, C. ericae, T. flavus and T. major) (Fig. 4 and Table 1). - Species found on gerbera: On gerbera, F. occidentalis represented 84.84% of the samples, T. tabaci, 14 %, and 1% for these other species (A. tenuicornis, T.discolor and T. major) (Fig. 4 and Table 1).
DI SCUSSI ON
Nine genera and fourteen different species on rose crops or gerbera were identified in Southern France. Two dominant species were observed: F. occidentalis Pergande and T. tabaci Lindeman [Thysanoptera: Thripidae] with respectively 81% and 17% of individuals collected respectively. On the Sophia-Antipolis site, two distinct infestation periods occurred in the greenhouse, one in spring and one in autumn (Pizzol J. unpublished data). Overall, in the various sites, about 80% of thrips found were F. occidentalis, except at the La Baronne site in 2006 where F. occidentalis was present only on 53% of thrips on roses sampled. The second most abundant species was T. tabaci on all sites and cultures with a maximum of 43% on roses in 2006 at the La Baronne site. This difference in proportion of each species between the two sites can be explained by different environmental conditions, with trees and diverse crops near the greenhouses at La Baronne. On the Sophia-Antipolis site, where a majority of rose crops were grown in greenhouses and F. occidentalis was predominant, compared to T. tabaci (as described on roses in Brazil by Carvalho, 2005). Frankliniella occidentalis was reported to stay inside greenhouses in the United States for 12 to 15 generations per year (OEPP / EPPO, 1989). It is likely that greenhouse conditions allow this species to survive and grow in favorable climate conditions for most of the year. However, between 1995 and 1996 in Germany, Sauer (1997) indicated and reported on the same crop that T. tabaci was predominant but it decreased to respectively 56.2% and 44.5% during the course of the study. According to that author, T tabaci is in competition with F. occidentalis when both are present on the same crop at the same time. On the Sophia-Antipolis site, the decrease of T. tabaci in the greenhouses can also be explained by the competition between F. occidentalis and T. tabaci. In addition, F. occidentalis lays on average 135 eggs at 25°C during its life (Robb, 1989) while at the same temperature T. tabaci can lay 70 to 100 eggs (26 to 48% less). Therefore in these conditions (competition) F. occidentalis population increase faster than those of T. tabaci. Regarding species diversity, apart from F. occidentalis and T. tabaci, twelve other thrips species were identified on the rose crops. Three species: A. ericae, A.tenuicornis, S. longicornis are predators of other insects, e.g. of thrips and of mites (depending on the Aeolothrips stage for the latter pest), whereas S. longicornis is a consumer of mite eggs. Nine species are phytophagous i.e. C. ericae, F. intonsa, O. dorycnii, P. kellyanus, T. hawaiiensis, T. major, T. minutissimus, T. flavus, Scirtothrips inermis; among these, three of them the C. ericae, O. dorycnii, P. kellyanus are quite oligophagous or monophagous and the others are polyphagous species. In Russia, from 2006 to 2008, fourteen species were also identified on ornamental crops the most common of which was F. occidentalis (Klishima, 2009). Another species was found on the gerbera T. discolor, also a polyphagous phytophagous species. Among all these other species recorded and identified, two species are new, one in France, the S. inermis and one in Europe, the T. hawaiiensis.
CONCLUSI ON
Among the 14 species recorded in the rose greenhouses in Southern France, two species are predominant: Frankliniella occidentalis Pergande and Thrips tabaci Lindeman [Thysanoptera: Thripidae]. Greater effort should be directed towards the biological control of these two species in rose crops. For other species, monitoring is required, especially for the new potentially invasive recorded species that could ultimately become widespread pests, as is currently the case for F. occidentalis which was introduced in France in 1986 (Bournier and Bournier, 1987). This is particularly important because invasive species represent a major threat to crops (Ragsdale et al., 2011).
Acknowledgments
We thank J.M. Rabasse for helpful comments on the manuscript, J. Bazzano, J.M. Drapier, C. Metay, C. Wdziekonski and L. Cambournac for their technical assistance. This work was funded by the PACA REGION Projects (N° 2005 -20372 and N° 2006 13517. Literature Cited Bournier, J.P. and Bournier, $ /¶LQWURGXFWLRQ HQ )UDQFH G¶XQ QRXYHDX UDYDJHXU Frankliniella occidentalis. Phytoma. Défense des cultures 388: 14-17. Brun, R., Bertaux, F., Métay, C., Blanc, M.L., Wdziekonski, C. and Nuée, S. 2004. Stratégie de protection intégrée globale sur rosier de serre. PHM ± Revue horticole 461: 23-27. Carvalho, A.R., Bueno, V.H.P. and Diniz, A.J.F. 2005. Thrips (Thysanoptera) in protected rose crops in Brazil. Integrated Control in Protected Crops, Temperate Climate IOBC/WPRS Bulletin 28 (1): 39-42. Desneux, N., Denoyelle, R. and Kaiser, L. 2006. A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65: 1697-1706. Desneux, N., Ramirez-Romero, R. and Kaiser, L. 2006. Multi step bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environmental Toxicology and Chemistry, 25: 2675-2682. Desneux, N., Decourtye, A., and Delpuech, J.M. 2007. The sublethal effects of pesticides on beneficial arthropods. Ann. Rev. Entomol. 52: 81-106. Emery, C. and Shwartzman, M. 2005. Le marché de la rose. ONIFLHOR: p10. Humeres, E. and Morse, J.C. 2006. Resistance of avocado thrips (Thysanoptera: Thripidae) to sabadilla, a botanically derived bait. Pest Manage. Sci. 62: 886-889. Klishina, I. S. 2009. Thrips in the greenhouses of north-west Russia. Zashchita i Karantin 12:16-17. Lhoste ± Drouineau, $3URWHFWLRQ%LRORJLTXHLQWpJUpHGHO¶$QWKXULXP&DPSDJQH 2004 ± 2005. Atouts fleurs, 58: 51- 56. Mary, L., Blum, J., Queraud, T., Marrec, C. and Maisonneuve, J.C. 2000. La protection biologique et intégrée (PBI) en cultures de fleurs coupées sous serres, situations et applications en France. Phytoma. La défense des végétaux 529: 14-17. Morse, J.G. and Hoddle, M.S. 2006. Invasion Biology of Thrips. Ann. Rev. Entomol. 51: 67- 89. Mound, L.A. and Kibby, G. 1998. Thysanoptera : an identification guide. 2nd Ed, CABInt, Wallingford, p 70.
OEPP/EPPO. 1989. Fiche informative sur les organismes de quarantaine- Frankliniella occidentalis. Bulletin OEPP/EPPO 19. 177: 725 ± 731. Pizzol, J., Poncet, C., Hector, S. and ZiHJOHU 0 0LVH HQ SODFH G¶XQH SURWHFWLRQ biologique intégrée préventive contre les ravageurs des cultures de rosiers sous serre dans le sud de la France. IOBC/WPRS Bulletin 29: 31-36. Pizzol, J., Nammour, D., Hervouet, P., Bout, A., Desneux, N. and Mailleret, L. (2010). Comparison of two methods of monitoring thrips populations in a greenhouse rose crop. Journal of Pest Science 83 (2):191-196. Poncet, C., Lemesle, V., Mailleret, L., Bout, A., Boll, R. and Vaglio, J. 2010. Spatiotemporal analysis of plant pests in a greenhouse using a Bayesian approach. Agricultural and Forest Entomology 12: 325-332. Ragsdale, D.W., Landis D.A, Brodeur J, Heimpel G.E, Desneux N. 2011. Ecology and management of the soybean aphid in North America. Annu. Rev. Entomol. 56:375-399. Reynaud, P. 1998. Les Thysanoptères des cultures légumières et ornementales : 2 années G¶LQYHQWDLUH HW XQ LQYLWp VXUSULVH ,Q First transnational workshop on biological, integrated and rational control : status and perspectives with regard to regional and European experiences, Lille, France, 21-23 January 1998, 17-18. Reynaud, P., Balmes, V. and Pizzol, J. 2008. Thrips hawaiiensis (Morgan, 1913) (Thysanoptera: Thripidae), an Asian pest thrips now established in Europe. Bull.OEPP, 38: 155-160. Ridray, G. and Lacordaire, A.I. 2007. Simplification de la P.B.I du concombre sous serre avec Amblyseius swirskii. PHM ± Revue Horticole 489: 36-40. Robb, K.L. 1989. Analysis of Frankliniella occidentalis (Pergande) as a pest of floricultural crops on California greenhouses. Ph.D. dissertation, Univ.Calif.,Riverside, 135pp. Sauer, A. 1997. Populations dynamik von Thysanopteren und Befallsunterschiede bei Rosen im Gewachshaus. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 11: 337-340. Weisenburger, D.D. 1993. Human health - effects of agrichemicals use. Human Pathology 24: 571-576. zur-Strassen, R. 2003. Die terebranten Thysanoptera Europas und des Mittelmeergebietes. Die Tierwelt Deutschands 74: 1-277.
300
Number of thrips
250 200 150 100 50 0 2006
2007
2008
Year Other species
Fr ankliniella occidentalis
Thr ips tabaci
Figure 1: Thrips species in PIC rose greenhouse span 1 (in Sophia-Antipolis), Frankliniella occidentalis, Thrips tabaci and other species, in 2006, 2007 and 2008.
1200
Number of thrips
1000 800 600 400 200 0 2006
2007
2008
2009
Year Other species
Fr ankliniella occidentalis
Thr ips tabaci
Figure 2: Thrips species in PIC rose greenhouse spans 2-3-4 (in Sophia-Antipolis), Frankliniella occidentalis, Thrips tabaci and other species, in 2006, 2007, 2008 and 2009. 600
Number of thrips
500 400 300 200 100 0 2006
2007
2008
2009
Year Other species
Fr ankliniella occidentalis
Thr ips tabaci
)LJXUH 7KULSV VSHFLHV LQ 3,& URVH JUHHQKRXVH LQVLGH WKH ³RWKHU´ JUHHQKRXVHV in Sophia-Antipolis), Frankliniella occidentalis, Thrips tabaci and other species, in 2006, 2007, 2008 and 2009. 700
Number of thrips
600 500 400 300 200 100 0 2006 Rose
2006 Gerbera
2007 Gerbera
2008 Gerbera
Year Other species
Fr ankliniella occidentalis
Thr ips tabaci
Figure 4: Thrips species collected in La Baronne (Frankliniella occidentalis, Thrips tabaci and other species) in rose greenhouses in 2006, and thrips species (F. occidentalis, T. tabaci and other species) collected in gerbera greenhouses, in 2006, 2007 and 2008.
Entomophagous thrips Place
Plant
Rose Rose Rose Sophia Rose Antipolis Rose spans 2 3 4 Rose Rose Sophia Rose Antipolis Rose Old Rose greenhouses Rose La Baronne Rose Gerbera Gerbera Gerbera Sophia Antipolis span 1
Years Aeolothrips ericae
Aeolothrips tenuicornis
Scolothrips longicornis
Frankliniella intosa
Frankliniella occidentalis
2006 2007
1
2008 2006 2007 2008 2009 2006
1
2007 2008 2009 2006
1
1
2006 2007 2008
4
Phytophagous thrips Olygophagous/Monophagous
Phytophagous thrips - Polyphagous
19
194 179 160 439 653 891 183 263 416 440 197 145 87 582 53
Thrips hawaiiensis
1
Thrips major
Thrips minutissimus
3 3
3 9
8
Thrips flavus
2
Thrips Scirtothrips tabaci inermis
1 5 1
3 1 2
Table 1. List of thrips species collected on the different sites and the different greenhouses.
69 19 2 321 140 63 58 65 55 1 118 25 47 52
Tenothrips discolor
Ceratothrips ericae
Odontothrips dorycnii
Pezothrips kellyanus
13
1
1 3
7 1 1
