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Assessment of lure and kill and mass-trapping methods against the olive fly, Bactrocera oleae (Rossi), in desert-like environments in the Eastern Mediterranean
Crop Protection 57 (2014) 63e70
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Assessment of lure and kill and mass-trapping methods against the olive fly, Bactrocera oleae (Rossi), in desert-like environments in the Eastern Mediterranean S. Yasin a, P. Rempoulakis b, E. Nemny-Lavy b, A. Levi-Zada b, M. Tsukada c, N.T. Papadopoulos d, D. Nestel b, * a
Agro, Nippon International Cooperation for Community Development (NICCOD), Zababdeh Office, Palestine Department of Entomology, Institute of Plant Protection, ARO, Volcani Center, P.O. Box 6, Beit Dagan 50250, Israel Insect Ecology Laboratory, Faculty of Bioresources, Mie University, Tsu 514-8507, Japan d Laboratory of Entomology and Agricultural Zoology, University of Thessaly, Fytokou St., 38446 N. Ionia, Volos, Greece b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 September 2013 Received in revised form 3 December 2013 Accepted 14 December 2013
Management of the olive fly using environmentally friendly methods includes strategies based on lure and kill and/or mass-trapping. Despite a wealth of studies related to the efficacy of different lure and kill and mass-trapping systems in several olive producing areas, there are few known regarding the performance of such systems in low input olive farms of the desert-like areas of the Middle East. The present study reports on the control of the olive fly using both lure and kill and mass-trapping devices in lowinput farms in the region of Tubas, Palestine, between 2010 and 2012. The effect of environmental factors, such as elevation, on general patterns of olive fly infestation and the lure and kill system’s performance was also studied. Our final goal included the development of a general strategy to produce organic olive oil using alternative olive fly control methods. Initially we used a commercially available lure and kill device, the Eco-TrapÒ. The Eco-Trap performed relatively well during the three years of study, significantly reducing olive fly damage levels. Eco-Trap effectiveness was more evident at elevation above 400 m, where damage in the region of Tubas was more intense than at lower elevations. In a subsequent trial we tested a low-cost mass-trapping device. This device demonstrated similar levels of protection to the one seen with the Eco-Trap. Results showed that lure and kill and mass-trapping tactics can be effectively applied in the region of Tubas, and that accessible devices can be adopted to reduce control costs. The results also showed differential levels of damage throughout the region, which were related to elevation above sea level. The possibility of applying a regional management concept throughout the area by a centralized organization, such as a farmer’s union based on mass-trapping systems seems feasible and is discussed. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Olive fly Mass-trapping Regional control
1. Introduction Lure and kill and mass-trapping techniques have become widespread alternative methodologies for managing pests, especially Lepidoptera and Diptera (fruit flies) pests (El-Sayed et al., 2006, 2009). Throughout the last two decades, devices, feeding stations, traps, and other technologies have been developed, tested and marketed (e.g., Armsworth et al., 2008; Cohen and Yuval, 2000; Economopoulos, 1977; Economopoulos et al., 1986; Broumas and
* Corresponding author. Dept. of Entomology, Inst. of Plant Protection, ARO, Volcani Ctr., P.O. Box 6, Beit Dagan 50250, Israel. Tel.: þ972 39683690. E-mail address: [email protected] (D. Nestel). 0261-2194/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cropro.2013.12.020
Haniotakis, 1986; Piñero et al., 2009; Prokopy et al., 2000). All these techniques are based on the principle of attracting efficiently the pest insects (preferably females) to the devices, where they are removed from the rest of the population, either by retaining them in the device (e.g., mass-trapping), or by exposing them to toxic substances (e.g., lure and kill) (Cunningham, 1989; Economopoulos, 1989 and references therein). The general idea behind these methods is that a large proportion of the pest population will be removed from the agroecosystem, thus effectively reducing crop damage. In many cases the efficacy of such systems has not been completely proven, or the ability to replicate results has been difficult, probably due to the large variability between regions, orchards, and agroecosystems where these devices have been tested (Nestel et al., 2004). In addition, effective implementation of lure
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and kill and mass-trapping may become too costly and nonaffordable for growers (Moraal et al., 1993.). In spite of this, and aiming at reducing massive pesticide utilization, the concepts of lure and kill and mass-trapping have continued developing, and existing and new techniques are being continually tested. The olive fly is a monophagous pest of olives (Oleae europea, L.). Eggs are laid on susceptible olives, and hatched larvae feed on the mesocarp, pupating after 3 instars inside the fruit (summer generations) or in the soil (autumn and winter generations) (Tzanakakis, 2003). The fact that the pest is monophagous on olives strongly stimulated the development of lure and kill and masstrapping strategies for this pest. With no control, olive fly can inflict an almost total loss of both the production of olive oil and table olives (Michelakis and Neuenschwander, 1983) and reduce dramatically the quality of any remaining crop. From 1970’s to 90’s a group of Greek and others scientists explored and characterized the sex pheromone composition of the olive fly (Haniotakis, 1979; Baker et al., 1980), and tested the attraction of olive fly to visual stimuli (color, shape, size) as well as to olfactory cues coming from food, such as ammonia releasing compounds and pheromone baits (Economopoulos, 1979; Haniotakis and Skyrianos, 1981; Mazomenos and Haniotakis, 1981, 1985). Throughout this process, several lure and kill and mass-trapping devices were developed (Mazomenos et al., 1983) and some of them were marketed. Some of these commercial devises have been tested in several locations throughout the geographic distribution of the pests, especially along the coasts of the Mediterranean Sea (e.g., Bueno, 1986; Hepdurgun et al., 2009). In recent years, we tested the Eco-TrapÒ (Vioryl S.A., Greece) in Israel with relatively good results (Nestel et al., 2002, 2004). The Eco-Trap (Broumas et al., 2002) is based on the attraction of both sexes of the olive fly to the odor of ammonia, simulating food sources and attraction of males to the sex pheromone. The color of the Eco-Trap surface is green in order to avoid the lure and kill of beneficial insects (Neunschwander, 1982; Bagnoli, 2000). Eco-Traps are impregnated with deltamethrin and a phagostimulant, which stimulates landing-flies to lick the surface and get poisoned by the pesticide. The main problems with the Eco-Trap encountered in Israel during those early studies were related to (1) a shorter effective activity of the Eco-Trap under the hot and dry conditions of the area, thus requiring to increase the number of traps per landarea by adding a second round of traps in mid-summer and (2) the need of regional management (e.g., mapping and differential intervention throughout the control area) to effectively deal with hot-spots and spatial differences in damage, endangering control efforts throughout the region (Nestel et al., 2004). Since then, several local devices have been developed and entered the market. We recently launched a study in Palestine to assess the possibility of using the concepts of lure and kill and mass-trapping to control damage inflicted by the olive fly. The general idea was to utilize a commercial device investigating the feasibility of the concept, and to evaluate how local environmental conditions may affect the efficacy of this method. The study was performed in the region of Tubas, which is located in the Eastern slopes of the Palestinian mountains. Olive production in this area is organized and managed by farmers’ organizations producing organic olive oil for export. The Eastern slopes extend from the highland of Nablus, to the Jordan River valley, and their altitude ranges from approximately 700 m above sea level (asl) to 200 m below sea level. Olives can be found throughout the region, but the main production areas in this region extend from 100 to 700 m asl. The region is mainly planted with the local variety ‘Nabali-Baladi’, with a relatively low planting density (150e200 trees per hectare). No olive fly control is performed in this region, but damaged fruit is manually removed at harvest time. Trees are rain-fed, and plots are scattered
throughout the landscape with gaps of uncultivated land between them. The area is considered as semi-desert, with environmental conditions (temperature and precipitation) differing throughout the slope. During the 3 years of the study we assessed the ability of Eco-Traps to control fly damage at a single elevation (400 m asl), then we investigated the effect of elevation on the ability of the device to control pest damage, and finally we compared a local trapping device (in which flies are attracted to yellow color and ammonium, simulating protein food) with the ability of the EcoTrap to attract and control fly damage. 2. Materials and methods 2.1. Olive-fly population and temperature patterns in Tubas In order to monitor the adult olive fly population trends in the area of Tubas, we followed the population in a representative untreated plot in the area. Monitoring was conducted by trapping flies with yellow sticky traps (RimiÒ, Israel) (YST). YST are flat yellow polyethylene hard-plates (20 14 cm), coated with glue that withholds landing insects (see inset in Fig 7). In the representative orchard, we established five YST in fixed sampling stations that were established from the beginning of the study. Sampling stations were exposed in the center of 200 m2 blocks. Traps were suspended in the center of the canopy at a height of 1.5 m. Gentle pruning of the canopy was conducted in the winter. Sampling stations were serviced every two weeks throughout the study: the YST were exchanged and the trapped olive flies were counted. Monitoring was initiated in January 2010 and continued throughout the entire period of the study. We extrapolated the monthly average temperature patterns expected in the olive tree canopy in the area of Tubas for the whole period of the study by using land surface temperature derived from Moderate Imagining Spectrometer satellite data (Blum et al., 2013). This system calculates the canopy temperature at 10:30 AM (time at which Terra polar orbiting NASA satellite serves this region) using satellite data and a function modeled with Fourier series and a vegetation index (consult Blum et al., 2013 for more information). Based on our experience, the temperature at 10:30 AM is a good representative of the maximal day temperature, which usually peaks 1e2 h later. 2.2. Evaluation of Eco-Trap ability to control olive flies damage at a single elevation: a 3 years’ experience We set this experiment in orchards around the town of Tubas, Palestine (32 210 N 35 210 E), which is located at approximately 400 m asl. In this area we selected 6 plots (1 ha each). Adjacent plots (separated by at least 100 m) were paired and one of them was treated with Eco-Trap devices while the second served as a reference (no treatments at all against olive fly or other pests), providing 3 replicates of Eco-Trap and 3 Reference plots. Eco-Trap density was set at two traps per tree (twice the manufacturer’s recommended density for Greece). Deployment of the first EcoTrap per tree in the first year was conducted on July 22, 2010. The second Eco-Trap was deployed in early October. In 2011, we used the same 6 plots deploying the first Eco-Trap treatment at the beginning of June and the second at the beginning of September. In 2012, we continued with the same setting, and that year Eco-Trap devices were deployed in the same plots at the end of June and in mid-August 2012. We decided not to interchange between treatment and Reference plots during the 3 years in order to maintain long-term effects, and diminish the effects of annual fluctuations.
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2.2.1. Olive fruit infestation rates Olive fly damage was assessed by randomly collecting 100 olives per plot from all sections of the canopy in trees located in the center of the plot. Olives were inspected visually and those with signs of olive fly infestation were dissected. The numbers of olives with “active damage” (i.e., with hatched eggs and larval activity and tunneling of the mesocarp), “sterile or cold stings” (i.e., visual sting markings with the presence of un-hatched eggs), or no damage, were recorded. The contribution of sterile stings to the total damage (i.e., active damage and sterile stings) was around 10%. In 2010 we sampled fruit on two occasions: in July 25 (at the time of EcoTrap deployment), and in September 25 (at the start of harvest period). In 2011 we increased the sampling of fruit to 5 collections: June 1 (deployment of Eco-Traps), July 1, August 1, September 1 and October 1 (at the start of the harvesting period). In 2012 fruit sampling was conducted in mid-August, mid-September, earlyOctober and mid-October (at the start of harvest period). Statistical inference on the effect of treatment on damage was performed for 2010 with a non-parametric ANOVA (Kruskale Wallis) applied independently on the two sampling dates (Statgraphics, 2000). For 2011 and 2012, differences between EcoTrap treated and Reference plots were inferred with General Linear Models (GLM), with treatment and sampling dates as source of variation (Statgraphics, 2000). 2.2.2. Field duration of Eco-Trap In order to evaluate the durability of the Eco-Trap under the hot summer conditions of the Tubas area, three Eco-Traps were collected from the plots (one per plot) and shipped to the manufacturer in Greece (Vioryl S.A.) for residual chemical analysis and characterization. Eco-Traps were only analyzed on two occasions during 2010: In August 26 (35 days after deployment) and on October 4 (74 days after deployment). Chemical analysis quantified the remaining levels of pheromone (1,7-dioxaspiro [5,5]undecane) and deltamethrin in the Eco-Trap device. Differences in content of the two chemicals between dates were inferred with a nonparametric ANOVA (KruskaleWallis) (Statgraphics, 2000). 2.3. Effect of elevation on the performance of Eco-Traps In order to assess the ability of the Eco-Trap to control the olive fly populations at different altitudes, we selected plots located at a gradient of elevations (ranging from 150 to 550 m asl) across the Eastern slopes of Tubas. Plots treated with Eco-Traps (14 in total) were compared with Reference plots (18 plots) located at approximately the same elevation. This study was conducted during 2011. Damage was assessed by sampling fruit at two different dates: September 25, and at the start of the harvesting period on October 5. Assessment of damage was conducted following the methodology given above. Collected fruit was also weighted and correlated with damage level. Effect of Eco-Trap treatment on damage (during the two sampling dates) was inferred from an ANCOVA (Sokal and Rohlf, 1981), with elevation and average fruit weight as covariates. 2.4. Color and ammonia as attractants of control devices In order to find a more affordable system to control the olive fly we tested the YST combined with 10 gr of ammonia bicarbonate powder (Sigma Aldrich) packed on a slow releasing polyethylene sleeve (60 mm width 0.03 mm thickness, Poly-Sac, Gedera, Israel) sealed on both sides. The bags were adhered to a top corner of the YST before field exposure (see inset in Fig. 7). This device is similar to the one tested, with variable results, by Economopoulos et al. (1986) in Greece.
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Fly capture in YST þ ammonium bicarbonate, in YST alone, and in plastic McPhail traps (Yellow bottomed with transparent top; Shabtieli A.C., Givat Ein, Israel) loaded with an aqueous solution of 3% ammonium bicarbonate was assessed both in Israel and Palestine. This test was conducted in Timrat (32 690 N 35 240 E), Israel, between August and December 2011 and Tubas between June 2011 and November 2012 (in Tubas the comparison did not included the McPhail trap). In Timrat, the experiment was set in two different plots (approximately one hectare each). Five blocks were selected per plot. Each block consisted of three adjacent olive trees. The three tested traps were then suspended from the trees, serviced after one week and refreshed with clean or new traps. Each week, traps were rotated within the block. The whole experiment in Timrat continued for fifteen consecutive weeks. In Tubas, the comparison between YST þ ammonium bicarbonate and YST alone was conducted in a single plot with five blocks consisting of two adjacent trees. In contrast to Timrat, traps were serviced and refreshed every two weeks. In both cases, differences in the numbers of trapped flies between trap-types were analyzed using GLM (Statgraphics, 2000). In Timrat, blocks were treated as subjects while in Tubas, sampling stations were treated as subjects. The effectiveness of the YST þ ammonium to control olive fly damage was evaluated in Tubas during 2012 using nine plots. Three plots served as reference (no treatment), three plots were treated with Eco-Traps and three plots were treated with YST þ ammonium bicarbonate. The three different treatments were set in adjacent plots, as blocks. Plots were separated by a distance of at least 100 m. Differences in damage level between treatments were inferred using GLM (Statgraphics, 2000).
3. Results 3.1. Olive fly population and temperature trends The temperature patterns at 10:30 AM in the region of Tubas throughout the whole study are shown in Fig. 1. In general, temperature patterns during the three years are similar: average of 15 C in winter and up to 35 C in the middle of the summer (August). Main differences between the three years can be observed in the extension of the heat during the summer time. In 2010, average temperatures above 30 C extended from early June to early November, one month longer than in 2011 and 2012 which was observed between early June and early October. Fig. 1 also shows the male and female population trends during the three years of the study in the area of Tubas. In general, peaks of flight during the three years were at the same period of the year: a first peak in March, a second peak in JuneeJuly and a third one in the autumn (usually starting in October). During the hot summer (AugusteSeptember), trapping was very low. In 2010, trapping during the summer was unusually low, extending from mid-July until mid-November. This pattern contrasted with the subsequent years in which trapping levels during the summer were relatively low, but not absent or almost nil like in 2010 (Fig. 1). This unusual low trapping activity during the summer of 2010 seems to be related to the particularly hot summer and fall that affected the whole region of the Mediterranean. The level of the three main peaks of the year differed between the three years of the study. The lowest trapping levels were recorded during 2010; levels in 2011 and 2012 were similar. Male olive flies were trapped in larger numbers, in several cases up to several folds more than females during the peak periods. The yellow color of the YST probably favored the trapping of males over females, a result previously reported by Economopoulos (1977).
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Fig. 1. Average monthly olive tree canopy temperature in Tubas extrapolated from MODIS (surface land temperature) data derived from NASA Terra satellite at 10:30 AM (time of satellite service over the area) and from a model constructed with Fourier series and vegetation index (see Blum et al., 2013) (line), and male and female olive fly population trends between 2010 and 2012 in a Reference plot (i.e., non-treated) in the area of Tubas, Palestine (bars; black for males, gray for females). The plot was located at approximately 400 m above sea level.
3.2. Olive fly damage under an Eco-Trap control regime In 2010, fruit infestation levels in July 25, at the time of Eco-Trap establishment for this year, were similar in the Eco-Trap treated plots and Reference plots (H ¼ 0.5, P > 0.05), and were around 15% (Fig. 2). In contrast at the start of harvest period, in September, damage levels in general declined from those in July, and were significantly lower in the Eco-Trap treated plots (ca. 2%) than in the Reference plots (ca. 5%) (H ¼ 4.4, P < 0.05) (Fig. 2). In 2011, no fruit infestation was detected at the beginning of June (Fig. 2). Damage slightly increased in July, to an average of approximately 2%. Damage levels in October, at the harvest period, significantly increased from July to an approximate average of 9% in the Eco-Trap treated plots (F ¼ 3.1; d.f. 4, 20; P < 0.05) (Fig. 2). The average damage levels were higher in the Eco-Trap treated plots, although not significantly different (F ¼ 3.0; d.f. 1, 20; P > 0.05) than in the Reference plots. No significant interaction between treatment and sampling date was detected (F ¼ 0.7; d.f. 4, 20; P > 0.05).
Fig. 2. Olive fly damage level in Eco-Trap protected plots and Reference plots in the region of Tubas, Palestine, during the olive growing seasons of 2010e2012.
Average damage levels in 2012 were approximately 3% in Julye August in both Eco-Trap and Reference plots (Fig. 2). Damage levels significantly increased to 13% in the Reference plots by mid-October (F ¼ 19.3; d.f. 3,40; P < 0.01), beginning of the harvest period. Average damage in Eco-Trap treated plots were significantly lower during the whole growing season of 2012 than those found in the Reference plots (F ¼ 40.0; d.f. 1, 40; P < 0.01). No interaction was found between treatment and date (F ¼ 2.5; d.f. 3, 40; P > 0.05). Average concentrations of the two principal chemical components in the Eco-Trap devices exposed for 35 and 74 days during 2010 in Tubas olive orchard conditions is shown in Fig. 3. Concentration of pheromone and deltamethrin significantly differed between the two dates (for both: H ¼ 3.9, P < 0.05). While pheromone concentration was still above the active level after 74 days of field exposure, deltamethrin, the killing agent on the surface of the EcoTrap, was below the minimal required concentration (Ragoussis,
Fig. 3. Average olive fly pheromone and deltamethrin concentration in Eco-Trap devices exposed for 35 and 74 days to the environmental conditions prevailing in Tubas, Palestine, olive orchards during the summer (JulyeOctober) of 2010. Horizontal lines show the known minimal level of the chemical required for the device to be effective in attracting and killing olive flies.
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Vioryl S.A., personal communication). This result suggests that the Eco-Trap device is effective for approximately 2 months in the area of Tubas, which is shorter than the time required to protect fruit from olive fly damage in this area. 3.3. Effect of elevation on Eco-Trap ability to control olive fly damage The relationship between elevation above sea level, average damage and plot treatment, for October 5, 2011 (at the start of the harvest period), is shown in Fig. 4. Fruit infestation level was significantly smaller at lower than at higher elevations (F ¼ 31.2; d.f. 1, 62; P < 0.01). Fruit infestation significantly differed between EcoTrap treated and Reference plots (F ¼ 4.5; d.f. 1, 62; P < 0.05). Differences in damage level were more pronounced at higher elevations than at lower elevations (Fig. 4). Below 400 m asl, average damage was 5.1 2.9% in the Reference plots and 4.8 3.2% in the Eco-Trap plots, while above 400 m asl, damage in the Reference plots doubled (12.2 7.7%) as compared with the average damage found in Eco-Trap plots (6.2 3.2%). Fruit weight significantly affected the level of damage (F ¼ 34.9; d.f. 1, 62; P < 0.01). Heavier fruits were more susceptible to become damaged (Fig. 5). Degree of damage of heavy fruit was lower in Eco-Trap plots than in Reference plots (Fig. 5). The sampling date significantly affected the general level of damage (F ¼ 5.8; d.f. 1, 62; P < 0.05). No interaction was found between plot type (Eco-Trap or Reference) and sampling date (F ¼ 0.2; d.f. 1, 62; P > 0.05). 3.4. Performance of yellow sticky traps combined with ammonium bicarbonate The ability of the yellow sticky traps (YST) loaded with ammonium bicarbonate to trap flies, as compared with YST with no other attractant and McPhail traps with a solution of 3% ammonium bicarbonate, is shown in Fig. 6. The comparison of the 3 trap types was conducted in Timrat, Israel, during 2011 (Fig. 6A), and the comparison, in Tubas, Palestine was only between YST with and without ammonium bicarbonate (Fig. 6B). The YST þ ammonium bicarbonate trapped significantly more olive flies in the two locations than any of the other two trap types (Ftimrat ¼ 44.4; d.f. 2, 351; P < 0.01; FTubas ¼ 15.6; d.f. 1272; P < 0.01) (Fig. 6). In Timrat (Fig. 6A) olive fly catches significantly differed between sampling dates (F ¼ 34.5; d.f. 13, 351; P < 0.01); trapping
Fig. 5. Average olive fly damage as a function of fruit weight at the onset of 2011 harvest period in Eco-Trap protected plots and in Reference plots in the region of Tubas, Palestine.
was highest in OctobereNovember. During this period of high catches, the YST þ ammonium bicarbonate caught almost 3 times more flies than the YST without attractant or the McPhail trap with ammonium solution (Fig. 6A). No significant differences were found between YST and McPhail trapping levels in Timrat. There was a significant interaction in Timrat between catches in the different trap types and date (F ¼ 5.6; d.f. 26, 351; P < 0.01). This interaction is probably the result of the catching-patterns observed in the YST and the McPhail traps (Fig. 6A). In Tubas, the level of catches also differed throughout the whole sampling period (F ¼ 12.1; d.f. 34, 272; P < 0.01) (Fig. 6B). In Tubas there was also a significant interaction between trap-type catches and sampling date (F ¼ 3.0; d.f. 34, 272; P < 0.01). The results of the experiment conducted in Tubas in which the ability of the YST þ ammonium bicarbonate to control damage by olive fly was compared with that of the Eco-Trap is shown in Fig. 7. Level of damage in Reference plots significantly differed from the damage observed in Eco-Trap and YST þ ammonium bicarbonate plots (F ¼ 21.4; d.f. 2, 22; P < 0.01). No significant differences were observed between YST þ ammonium bicarbonate plots and EcoTrap plots. Average level of damage in Reference plots at the onset of harvest was four-fold larger than the one found in the YST þ ammonium bicarbonate and the Eco-Trap plots. Damage significantly increased throughout the growing season (F ¼ 5.8; d.f. 3, 22; P < 0.01), but no interaction was detected between sampling date and treatment (F ¼ 2.2; d.f. 6, 22; P > 0.05). 4. Discussion
Fig. 4. Average olive fly damage levels at the onset of 2011 harvest period in the region of Tubas, Palestine, in plots located at different elevations above sea level, and treated with Eco-Traps or without any treatment to control olive fly fruit injury.
Control of the olive fly with lure and kill and/or mass-trapping has been attempted in the past with variable levels of success. In mainland Greece, Eco-Trap devices were shown to effectively control olive fly populations and damage (Broumas et al., 2002; Ragoussis, 2002, 2005). Other studies have also claimed successful olive fly control with a variety of devices (e.g., Haniotakis and Skyrianos, 1981; Jones et al., 1983; Haniotakis et al., 1986, 1991; Ricciolini et al., 2000; Petacchi et al., 2003). In the present study, our results suggest an effective control of the olive fly using both the lure and kill and mass-trapping approach in the region of Tubas. The level of control varied with year and location of plots along an elevation gradient. In 2010, damage was significantly lower in EcoTrap plots than in control. The general economic effect of control for this year, however, was minimal since general damage in the area
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Fig. 6. Trapping trends of male and female olive flies (shown as total) on yellow-sticky trap devices (YST) loaded with ammonium bicarbonate, and without ammonium, and in McPhail traps activated with an aqueous solution of 3% ammonium bicarbonate in Timrat (Israel) during 2011 (A), and in Tubas, Palestine, during 2011 and 2012 (B). In Tubas, only yellow sticky traps with and without ammonium bicarbonate were compared.
was relatively low. In 2011 we were unable to show any significant effective control at 400 m. This being probably due to the fact that the Eco-Traps were redeployed after three months, and not after two months as recommended from the results of 2010 (see Fig. 3). However, control and damage were shown to be highly linked to elevation. The Eco-Trap showed some effectiveness in controlling the fly at elevations above 400 m, as compared with the Reference plots at this height. The efficiency of the Eco-Traps at higher elevations remained for a longer period of time due to lower temperatures. In addition the general damage level in 2011 in the region was relatively low. The effectiveness of lure and kill and mass-trapping as a control strategy was in fact more evident during 2012. In the two set of experiments running that year, lure and kill and mass-trapping devices (Eco-Trap and YST þ ammonium bicarbonate) showed a significant ability to control damage inflicted by the olive fly, reducing infestation by more than 50%.
Fig. 7. Olive fly damage level in Eco-Trap protected plots, yellow-sticky traps (YST) loaded with ammonium bicarbonate protected plots and Reference plots in the region of Tubas, Palestine, during the olive growing season of 2012. The inset shows a picture of the RimiÒ yellow sticky-trap loaded with ammonium bicarbonate.
In a previous study (conducted between 1999 and 2001) in which Eco-Trap devices were investigated as a tool for lure and kill control of the olive fly in Israel, we already observed that the EcoTrap can effectively control damage of highly sensitive varieties in the region (Nestel et al., 2002, 2004). In the 1999e2001 study, damage levels were kept below 7% in very sensitive olive-fly varieties while control plots reached up to 50% of infestation (Nestel et al., 2002). This previous result encouraged us to select this device to explore the possibility of applying lure and kill as a strategy to control olive fly damage in Tubas. During the 1999e2001 study, however, two main difficulties were already pointed out: the need for a higher density of devices than the recommended by the producer (Ragoussis, 2005), and the need to approach control with a lure and kill strategy from a regional perspective (Nestel et al., 2004). The reason to double the density of devices during this early experiment was linked to the observation that the duration of the effective activity of the Eco-Trap in the summer of Israel was shorter than that reported by the manufacturer for Greece conditions (Ragoussis, 2005), requiring an addition of a second round of Eco-Traps after 2 months of field exposure (Nestel et al., 2002). In the present study, we also found a similar effective field-life span of the Eco-Trap at the conditions of Tubas (Fig. 3). Thus, although we knew that control with the Eco-Trap was not economically viable before starting the project, the aim of using this device in the current study was to explore the application of the lure and kill concept in Tubas with a known effective tool. The results of this study were very encouraging, suggesting that this approach is viable, and leading us to look for a more economical alternative control system for the region of Tubas, and other areas of Palestine. From the results of 2011 and 2012, it seems that the YST þ ammonium bicarbonate may fulfill this aim. This device showed both a stronger attractiveness of the olive fly than nonammonium bicarbonate baited YST and baited McPhail trap (Fig. 6), and an ability of control comparable to the Eco-Trap (Fig. 7). The more accessible cost of the YST is based on the fact that odorattraction is only sustained by ammonium bicarbonate and not by pheromone, and the possibility of cleaning and recycling the YST plastic for several field applications. Thus, although labor-intensive,
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the application of the mass-trapping strategy based on YST þ ammonium bicarbonate dispensers may be appropriate for places where labor is available in excess and where capitalintensive systems are not accessible. Before implementation, however, the YST þ ammonium bicarbonate device should be tested at more environmental conditions of Palestine and throughout more years, and simple systems of recycling should be developed and tested. Lower olive fly populations during 2010, and during the summer months, and reduced damage in areas below 400 m asl, is probably linked to the effect of temperatures on olive fly survival, activity and reproductive effort. Above 29 C olive fly has been reported to halt flying and reproductive activity (Avidov, 1954). Above 30 C, olive fly eggs, larvae and adult start to die and temperatures above 35 C may be highly detrimental to the population (Tsiropoulos, 1972; Tzanakakis, 2003 and references therein). Moreover, olive fly trapping patterns have been shown to be affected by elevation and seasons of the year, and linked to the environmental temperature regimes affected by elevation and season (Kounatidis et al., 2008). During the summer months, temperatures in many areas of Israel and Palestine usually are above 30 C (Blum et al., 2013). High temperatures can frequently exceed 35 C, and stay for prolonged periods of time. The temperature in Tubas throughout summers is high, above 30 C (Fig. 1), being several degrees warmer the more we descend in elevation above sea level (unpublished data). Thus, both, summer and lower elevations are expected to affect olive fly population and damage. This was in fact the observed patterns in Tubas during the three years (Figs. 2 and 4). In this sense, 2010 was of special interest. During 2010 population levels were low, as expressed by low trapping levels (Fig. 1), and damage at Tubas was relatively minor (around 5% without protection). During 2010, average temperatures during the summer months were slightly higher than the ones observed during 2011 and 2012 (Engelhard, 2012). Of more importance than the slightly higher temperatures registered during 2010, however, was the fact that the hot summer extended for an extra month, until earlyNovember (Fig. 1), leading to a delay in the appearance of the fall peak in olive fly trapping throughout the entire region (Engelhard, 2012). This delayed emergence of the fall population, and the fact that harvest was initiated early in October, explain the low olive fly damage in the experiment, and the low damage reported by farmers throughout the entire region. As mentioned earlier, our previous study (1999e2001) suggested that the implementation of lure and kill and mass-trapping as a control strategy should be undertaken at a regional level (Nestel et al., 2002). This was our initial aim in Tubas, and the exploration of damage and Eco-Trap efficacy at different elevation pointed towards this direction. Our observations regarding the effect of elevation and control during 2011, support this idea and approach. The differential level of damage observed with elevation can be managed differentially if the entire region is integrated into a cooperative enterprise. The fact that at lower elevations damage is in general much lower than at higher elevations, suggest that low elevation orchards could be managed with less lure and kill and/or mass-trapping control efforts, directing resources and management efforts to the high elevation orchards. At the completion of the project, this approach was suggested to the farmers’ organization, and we expect that its adoption, together with the incorporation of a less expensive device, will lead the whole community to produce good quality organic olive oil suitable for export. Acknowledgments To the farmers and olive producers of Tubas for their willingness to provide us with access to their orchards. To Mayumi Yoshida for
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her professional, and humane, management approach throughout the project and to her invaluable collaboration, and to all members of NICCOD for their help and enthusiastic participation. Also to Miriam Kishinevsky for technical assistance and to Dr. N. Ragoussis (Vioryl, S.A.) for his support in analyzing Eco-Traps. To Dr. Ezra Dunkelblum for his suggestions and language improvements. We appreciate the input of three anonymous reviewers that helped improve an early draft of the manuscript. The project was financed by the Ministry of Foreign Affairs of Japan through Nippon International Cooperation for Community Development (NICCOD), project no 131-1631.
References Armsworth, C.G., Rogers, C.D., Barton, L.E.E., Soares, C., Poppy, G.M., 2008. Uptake of adhesive powders from lure stations by Mediterranean fruit fly (Dipt., Tephritidae). J. Appl. Entomol. 132, 45e53. Avidov, Z., 1954. Further investigations on the ecology of the olive fly (Dacus oleae, Gmel.) in Israel. Ktavim 4, 39e50. Bagnoli, B., 2000. Indagini sull’ impatto di dispositivi per la cattura massale di adulti di Bactrocera oleae sull’ entomofauna utile dell’ oliveto. In: Proceedings “Metodi alternativi di lotta alla mosca delle olive”, Firenze, Italy; 24 Mars 2000 (in Italian). Baker, R., Herbert, R., Howse, P.E., Jones, O.T., Franke, W., Reith, W., 1980. Identification and synthesis of the major sex pheromone of the olive fly (Dacus oleae). Journal of the Chemical Society. Chem. Commun. 1, 52e53. Blum, M., Lensky, I.M., Nestel, D., 2013. Estimation of olive grove canopy temperatures from MODIS thermal imagery is more accurate than interpolation from meteorological stations. Agric. For. Meteorol. 176, 90e93. Broumas, T., Haniotakis, G., Sept. 1986. Further studies on the control of the olive fruit fly by mass trapping. In: Proc. II International Symposium on Fruit Flies, Crete, pp. 561e565, 1987. Broumas, T., Haniotakis, G., Liaropoulos, C., Tomazou, T., Ragoussis, N., 2002. The efficacy of an improved form of the mass-trapping method, for the control of the olive fruit fly, Bactrocera oleae (Gmelin) (Dipt., Tephritidae): pilot-scale feasibility studies. J. Appl. Entomol. 126, 217e223. Bueno, A.M., 1986. The use of sex pheromone for monitoring and control of olive fruit fly. In: Proceedings of the Second International Symposium on Fruit Flies of Economic Importance, Crete, Greece, pp. 483e492. Cohen, H., Yuval, B., 2000. Perimeter trapping strategy to reduce Mediterranean fruit fly (Diptera: Tephritidae) damage on different host species in Israel. J. Econ. Entomol. 93, 721e725. Cunningham, R.T., 1989. Population detection. In: Robinson, A.S., Hooper, G. (Eds.), World Crop Pests, Fruit flies, their biology, natural enemies and control, vol. 3B. Elsevier Science Publishers B. V., Amsterdam, pp. 169e173, 447 pp. Economopoulos, A.P., 1977. Controlling Dacus oleae by fluorescent yellow traps. Entomol. Exp. Appl. 22, 183e190. Economopoulos, A.P., 1979. Attraction of Dacus oleae (Gmelin) (Diptera, Tephritidae) to odor and color traps. Zeitsch. fur Angewandte Entomol. 88, 90e97. Economopoulos, A.P., 1989. Use of traps based on color and/or shape. In: Robinson, A.S., Hooper, G. (Eds.), World Crop Pests, Fruit flies, their biology, natural enemies and control, vol. 3B. Elsevier Science Publishers B. V., Amsterdam, pp. 315e327, 447 pp. Economopoulos, A.P., Raptis, A., Stavropoulou-Delivoria, A., Papadopoulos, A., 1986. Control of Dacus oleae by yellow sticky traps combined with ammonium acetate slow-release dispensers. Entomol. Exp. Appl. 41, 11e16. El-Sayed, A.M., Suckling, D.M., Wearing, C.H., Byers, J.A., 2006. Potential of masstrapping for long-term pest management and eradication of invasive species. J. Econ. Entomol 99, 1550e1564. El-Sayed, A.M., Suckling, D.M., Byers, J.A., Jang, E.B., Wearing, C.H., 2009. Potential for “lure and kill” in long-terms pest management and eradication of invasive species. J. Econ Entomol. 102, 815e835. Engelhard, I., 2012. Olive Fly Bactrocera oleae Population Trends in Israel as Affected by Geo-climatic Location. M.Sc. thesis submitted to the Faculty of Agriculture, Food and Environment. Hebrew University of Jerusalem, Rehovot, Israel, p. 40. Haniotakis, G.E., 1979. Potential practical uses of the olive fruit fly sex attractant pheromones. In: Proc. Int. Symp. I.O.B.C./W.P.R.S. “Integrated Control in Agriculture and Forestry” Vienna. 8e12 Oct, pp. 471e476. Haniotakis, G.E., Skyrianos, G., 1981. Attraction of the olive fruit fly to pheromone, McPhail and color traps. J. Econ. Entomol. 74, 58e60. Haniotakis, G., Kozyrakis, M., Bonatsos, C., 1986. Control of the olive fruit fly Dacus oleae Gmel. (Diptera: Tephritidae) by mass trapping: pilot scale feasibility study. J. Appl. Entomol. 101, 343e352. Haniotakis, G., Kozyrakis, M., Fitsakis, T., Antonidaki, A., 1991. An effective mass trapping method for the control of Dacus oleae (Diptera: Tephritidae). J. Econ. Entomol. 84 (2), 564e569. Hepdurgun, B., Turanli, T., Zumreoglu, A., 2009. Control of the olive fruit fly, Bactrocera oleae, (Diptera: Tephritidae) through mass trapping and mass releases of the parasitoid Psyttalia concolor (Hymenoptera: Braconidae) reared on irradiated Mediterranean fruit fly. Biocont. Sci. Technol. 19, 211e224.
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Jones, O.T., Lisk, J.C., Longhurst, C., House, P.E., 1983. Development of a monitoring trap for the olive fly, Dacus oleae (Gmelin) (Diptera: Tephritide), using a component of its sex pheromone as lure. Bull. Entomol. Res. 73, 97e106. Kounatidis, I., Papadopoulos, N.T., Mavragani-Tsipidou, P., Cohen, Y., Tertivanidis, K., Nomikou, M., Nestel, D., 2008. Effect of elevation on spatio-temporal patterns of olive fly (Bactrocera oleae) populations in Northern Greece. J. Appl. Entomol. 132, 722e733. Mazomenos, B.E., Haniotakis, G.E., 1981. A multi component female sex pheromone of Dacus oleae Gmel. Isolation and bioassay. J. Chem. Ecol. 7, 437e443. Mazomenos, B.E., Haniotakis, G.E., 1985. Male olive fruit fly attraction to synthetic sex pheromone components in laboratory and field tests. J. Chem. Ecol. 11, 397e 405. Mazomenos, B.E., Haniotakis, G.E., Ioannou, A., Spanakis, I., Kozirakis, A., 1983. Field evaluation of the olive fruit fly pheromone traps with various dispensers and concentrations. In: Cavalloro, R. (Ed.), Fruit Flies of Economic Importance, Proc. of the CEC/IOBC, Intern. Sympos. Athens Greece, 16e19 Nov. 1982, pp. 506e512. Michelakis, S.E., Neuenschwander, P., 1983. Estimates of the crop losses caused by Dacus oleae (Gmel.) (Diptera, Tephritidae) in Crete, Greece. In: Cava1loro, R. (Ed.), Fruit Flies of Economic Importance, in Proceedings of the CEC/IOBC, International Symposium, p. 642. November 16_19 1982; Athens, Greece. Moraal, L.G., van der Kraan, C., van der Voet, H., 1993. Studies on the efficacy of the sex attractant of Paranthrene tabaniformis Rott. (Lep., Sesiidae). J. Appl. Entomol. 116, 364e370. Nestel, D., Carvalho, J., Zaidan, S., Ben-Yehuda, S., Nemny-Lavy, E., 2002. Three years of trials on mass-trapping of the olive fly (Bactrocera oleae) in Israel. Alon Hanotea 56, 460e469 (in Hebrew).
Nestel, D., Carvalho, J., Nemny-Lavy, E., 2004. The spatial dimension in the ecology of insect pests and its relevance to pest management. In: Horowitz, A.R., Ishaaya, I. (Eds.), Insect Pests Management. Springer-Verlag, Berlin, Germany, pp. 45e63. Neunschwander, P., 1982. Beneficial insects caught by yellow traps used in mass trapping of the olive fly, Dacus oleae. Entomol. Exp. Appl. 32, 286e296. Petacchi, R., Rizzi, I., Guidotti, D., 2003. The “lure and kill” technique in Bactrocera oleae (Gmel.) control: effectiveness indices and suitability of the technique in area-wide experimental trials. J. Pest Manag. 49 (4), 305e311. Piñero, J.C., Mau, R.F., McQuate, G.T., Vargas, R., 2009. Novel bait stations for attractand-kill of pestiferous fruit flies. Entomol. Exp. Appl. 133, 208e216. Prokopy, R.J., Wright, S.E., Black, J.L., Hu, X.P., McGuire, M.R., 2000. Attracticidal spheres for controlling apple maggot flies: commercial-orchard trials. Entomol. Exp. Appl. 97, 293e299. Ragoussis, N., 2002. Eco-Trap: efficient tool for the control of the olive fruit FLY Bactrocera oleae in the Mediterranean area. IOBC/Wprs Bull. 25 (9), 195e202. Ragoussis, N., 2005. Contribution to the biological olive agriculture. Efficient control of the olive fruit fly by the ECO-TRAPÒ. IOBC/Wprs Bull. 28 (9), 29e35. Ricciolini, M., Bottazzi, P., Nizzi Grifi, F., Silvestri, E., Toma, M., 2000. Le esperienze di cattura massale in Toscana. In: Proceedings “Metodi alternativi di lotta alla mosca delle olive” Firenze, Italy; 24 Mars 2000. Sokal, R.R., Rohlf, F.J., 1981. Biometry. WH Freeman and Co., NY, USA. Statgraphics, 2000. Statgraphics 5 Plus Manual. Manugistics Inc, Rockville, MD, USA. Tsiropoulos, G.J., 1972. Storage temperatures of eggs and pupae of the olive fruit fly. J. Econ. Entomol. 65 (1), 100e102. Tzanakakis, M.E., 2003. Seasonal development and dormancy of insects and mites feeding on olive: a review. Neth. J. Zool. 52, 87e224.
Contents lists available at ScienceDirect
Crop Protection journal homepage: www.elsevier.com/locate/cropro
Assessment of lure and kill and mass-trapping methods against the olive fly, Bactrocera oleae (Rossi), in desert-like environments in the Eastern Mediterranean S. Yasin a, P. Rempoulakis b, E. Nemny-Lavy b, A. Levi-Zada b, M. Tsukada c, N.T. Papadopoulos d, D. Nestel b, * a
Agro, Nippon International Cooperation for Community Development (NICCOD), Zababdeh Office, Palestine Department of Entomology, Institute of Plant Protection, ARO, Volcani Center, P.O. Box 6, Beit Dagan 50250, Israel Insect Ecology Laboratory, Faculty of Bioresources, Mie University, Tsu 514-8507, Japan d Laboratory of Entomology and Agricultural Zoology, University of Thessaly, Fytokou St., 38446 N. Ionia, Volos, Greece b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 September 2013 Received in revised form 3 December 2013 Accepted 14 December 2013
Management of the olive fly using environmentally friendly methods includes strategies based on lure and kill and/or mass-trapping. Despite a wealth of studies related to the efficacy of different lure and kill and mass-trapping systems in several olive producing areas, there are few known regarding the performance of such systems in low input olive farms of the desert-like areas of the Middle East. The present study reports on the control of the olive fly using both lure and kill and mass-trapping devices in lowinput farms in the region of Tubas, Palestine, between 2010 and 2012. The effect of environmental factors, such as elevation, on general patterns of olive fly infestation and the lure and kill system’s performance was also studied. Our final goal included the development of a general strategy to produce organic olive oil using alternative olive fly control methods. Initially we used a commercially available lure and kill device, the Eco-TrapÒ. The Eco-Trap performed relatively well during the three years of study, significantly reducing olive fly damage levels. Eco-Trap effectiveness was more evident at elevation above 400 m, where damage in the region of Tubas was more intense than at lower elevations. In a subsequent trial we tested a low-cost mass-trapping device. This device demonstrated similar levels of protection to the one seen with the Eco-Trap. Results showed that lure and kill and mass-trapping tactics can be effectively applied in the region of Tubas, and that accessible devices can be adopted to reduce control costs. The results also showed differential levels of damage throughout the region, which were related to elevation above sea level. The possibility of applying a regional management concept throughout the area by a centralized organization, such as a farmer’s union based on mass-trapping systems seems feasible and is discussed. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Olive fly Mass-trapping Regional control
1. Introduction Lure and kill and mass-trapping techniques have become widespread alternative methodologies for managing pests, especially Lepidoptera and Diptera (fruit flies) pests (El-Sayed et al., 2006, 2009). Throughout the last two decades, devices, feeding stations, traps, and other technologies have been developed, tested and marketed (e.g., Armsworth et al., 2008; Cohen and Yuval, 2000; Economopoulos, 1977; Economopoulos et al., 1986; Broumas and
* Corresponding author. Dept. of Entomology, Inst. of Plant Protection, ARO, Volcani Ctr., P.O. Box 6, Beit Dagan 50250, Israel. Tel.: þ972 39683690. E-mail address: [email protected] (D. Nestel). 0261-2194/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cropro.2013.12.020
Haniotakis, 1986; Piñero et al., 2009; Prokopy et al., 2000). All these techniques are based on the principle of attracting efficiently the pest insects (preferably females) to the devices, where they are removed from the rest of the population, either by retaining them in the device (e.g., mass-trapping), or by exposing them to toxic substances (e.g., lure and kill) (Cunningham, 1989; Economopoulos, 1989 and references therein). The general idea behind these methods is that a large proportion of the pest population will be removed from the agroecosystem, thus effectively reducing crop damage. In many cases the efficacy of such systems has not been completely proven, or the ability to replicate results has been difficult, probably due to the large variability between regions, orchards, and agroecosystems where these devices have been tested (Nestel et al., 2004). In addition, effective implementation of lure
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and kill and mass-trapping may become too costly and nonaffordable for growers (Moraal et al., 1993.). In spite of this, and aiming at reducing massive pesticide utilization, the concepts of lure and kill and mass-trapping have continued developing, and existing and new techniques are being continually tested. The olive fly is a monophagous pest of olives (Oleae europea, L.). Eggs are laid on susceptible olives, and hatched larvae feed on the mesocarp, pupating after 3 instars inside the fruit (summer generations) or in the soil (autumn and winter generations) (Tzanakakis, 2003). The fact that the pest is monophagous on olives strongly stimulated the development of lure and kill and masstrapping strategies for this pest. With no control, olive fly can inflict an almost total loss of both the production of olive oil and table olives (Michelakis and Neuenschwander, 1983) and reduce dramatically the quality of any remaining crop. From 1970’s to 90’s a group of Greek and others scientists explored and characterized the sex pheromone composition of the olive fly (Haniotakis, 1979; Baker et al., 1980), and tested the attraction of olive fly to visual stimuli (color, shape, size) as well as to olfactory cues coming from food, such as ammonia releasing compounds and pheromone baits (Economopoulos, 1979; Haniotakis and Skyrianos, 1981; Mazomenos and Haniotakis, 1981, 1985). Throughout this process, several lure and kill and mass-trapping devices were developed (Mazomenos et al., 1983) and some of them were marketed. Some of these commercial devises have been tested in several locations throughout the geographic distribution of the pests, especially along the coasts of the Mediterranean Sea (e.g., Bueno, 1986; Hepdurgun et al., 2009). In recent years, we tested the Eco-TrapÒ (Vioryl S.A., Greece) in Israel with relatively good results (Nestel et al., 2002, 2004). The Eco-Trap (Broumas et al., 2002) is based on the attraction of both sexes of the olive fly to the odor of ammonia, simulating food sources and attraction of males to the sex pheromone. The color of the Eco-Trap surface is green in order to avoid the lure and kill of beneficial insects (Neunschwander, 1982; Bagnoli, 2000). Eco-Traps are impregnated with deltamethrin and a phagostimulant, which stimulates landing-flies to lick the surface and get poisoned by the pesticide. The main problems with the Eco-Trap encountered in Israel during those early studies were related to (1) a shorter effective activity of the Eco-Trap under the hot and dry conditions of the area, thus requiring to increase the number of traps per landarea by adding a second round of traps in mid-summer and (2) the need of regional management (e.g., mapping and differential intervention throughout the control area) to effectively deal with hot-spots and spatial differences in damage, endangering control efforts throughout the region (Nestel et al., 2004). Since then, several local devices have been developed and entered the market. We recently launched a study in Palestine to assess the possibility of using the concepts of lure and kill and mass-trapping to control damage inflicted by the olive fly. The general idea was to utilize a commercial device investigating the feasibility of the concept, and to evaluate how local environmental conditions may affect the efficacy of this method. The study was performed in the region of Tubas, which is located in the Eastern slopes of the Palestinian mountains. Olive production in this area is organized and managed by farmers’ organizations producing organic olive oil for export. The Eastern slopes extend from the highland of Nablus, to the Jordan River valley, and their altitude ranges from approximately 700 m above sea level (asl) to 200 m below sea level. Olives can be found throughout the region, but the main production areas in this region extend from 100 to 700 m asl. The region is mainly planted with the local variety ‘Nabali-Baladi’, with a relatively low planting density (150e200 trees per hectare). No olive fly control is performed in this region, but damaged fruit is manually removed at harvest time. Trees are rain-fed, and plots are scattered
throughout the landscape with gaps of uncultivated land between them. The area is considered as semi-desert, with environmental conditions (temperature and precipitation) differing throughout the slope. During the 3 years of the study we assessed the ability of Eco-Traps to control fly damage at a single elevation (400 m asl), then we investigated the effect of elevation on the ability of the device to control pest damage, and finally we compared a local trapping device (in which flies are attracted to yellow color and ammonium, simulating protein food) with the ability of the EcoTrap to attract and control fly damage. 2. Materials and methods 2.1. Olive-fly population and temperature patterns in Tubas In order to monitor the adult olive fly population trends in the area of Tubas, we followed the population in a representative untreated plot in the area. Monitoring was conducted by trapping flies with yellow sticky traps (RimiÒ, Israel) (YST). YST are flat yellow polyethylene hard-plates (20 14 cm), coated with glue that withholds landing insects (see inset in Fig 7). In the representative orchard, we established five YST in fixed sampling stations that were established from the beginning of the study. Sampling stations were exposed in the center of 200 m2 blocks. Traps were suspended in the center of the canopy at a height of 1.5 m. Gentle pruning of the canopy was conducted in the winter. Sampling stations were serviced every two weeks throughout the study: the YST were exchanged and the trapped olive flies were counted. Monitoring was initiated in January 2010 and continued throughout the entire period of the study. We extrapolated the monthly average temperature patterns expected in the olive tree canopy in the area of Tubas for the whole period of the study by using land surface temperature derived from Moderate Imagining Spectrometer satellite data (Blum et al., 2013). This system calculates the canopy temperature at 10:30 AM (time at which Terra polar orbiting NASA satellite serves this region) using satellite data and a function modeled with Fourier series and a vegetation index (consult Blum et al., 2013 for more information). Based on our experience, the temperature at 10:30 AM is a good representative of the maximal day temperature, which usually peaks 1e2 h later. 2.2. Evaluation of Eco-Trap ability to control olive flies damage at a single elevation: a 3 years’ experience We set this experiment in orchards around the town of Tubas, Palestine (32 210 N 35 210 E), which is located at approximately 400 m asl. In this area we selected 6 plots (1 ha each). Adjacent plots (separated by at least 100 m) were paired and one of them was treated with Eco-Trap devices while the second served as a reference (no treatments at all against olive fly or other pests), providing 3 replicates of Eco-Trap and 3 Reference plots. Eco-Trap density was set at two traps per tree (twice the manufacturer’s recommended density for Greece). Deployment of the first EcoTrap per tree in the first year was conducted on July 22, 2010. The second Eco-Trap was deployed in early October. In 2011, we used the same 6 plots deploying the first Eco-Trap treatment at the beginning of June and the second at the beginning of September. In 2012, we continued with the same setting, and that year Eco-Trap devices were deployed in the same plots at the end of June and in mid-August 2012. We decided not to interchange between treatment and Reference plots during the 3 years in order to maintain long-term effects, and diminish the effects of annual fluctuations.
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2.2.1. Olive fruit infestation rates Olive fly damage was assessed by randomly collecting 100 olives per plot from all sections of the canopy in trees located in the center of the plot. Olives were inspected visually and those with signs of olive fly infestation were dissected. The numbers of olives with “active damage” (i.e., with hatched eggs and larval activity and tunneling of the mesocarp), “sterile or cold stings” (i.e., visual sting markings with the presence of un-hatched eggs), or no damage, were recorded. The contribution of sterile stings to the total damage (i.e., active damage and sterile stings) was around 10%. In 2010 we sampled fruit on two occasions: in July 25 (at the time of EcoTrap deployment), and in September 25 (at the start of harvest period). In 2011 we increased the sampling of fruit to 5 collections: June 1 (deployment of Eco-Traps), July 1, August 1, September 1 and October 1 (at the start of the harvesting period). In 2012 fruit sampling was conducted in mid-August, mid-September, earlyOctober and mid-October (at the start of harvest period). Statistical inference on the effect of treatment on damage was performed for 2010 with a non-parametric ANOVA (Kruskale Wallis) applied independently on the two sampling dates (Statgraphics, 2000). For 2011 and 2012, differences between EcoTrap treated and Reference plots were inferred with General Linear Models (GLM), with treatment and sampling dates as source of variation (Statgraphics, 2000). 2.2.2. Field duration of Eco-Trap In order to evaluate the durability of the Eco-Trap under the hot summer conditions of the Tubas area, three Eco-Traps were collected from the plots (one per plot) and shipped to the manufacturer in Greece (Vioryl S.A.) for residual chemical analysis and characterization. Eco-Traps were only analyzed on two occasions during 2010: In August 26 (35 days after deployment) and on October 4 (74 days after deployment). Chemical analysis quantified the remaining levels of pheromone (1,7-dioxaspiro [5,5]undecane) and deltamethrin in the Eco-Trap device. Differences in content of the two chemicals between dates were inferred with a nonparametric ANOVA (KruskaleWallis) (Statgraphics, 2000). 2.3. Effect of elevation on the performance of Eco-Traps In order to assess the ability of the Eco-Trap to control the olive fly populations at different altitudes, we selected plots located at a gradient of elevations (ranging from 150 to 550 m asl) across the Eastern slopes of Tubas. Plots treated with Eco-Traps (14 in total) were compared with Reference plots (18 plots) located at approximately the same elevation. This study was conducted during 2011. Damage was assessed by sampling fruit at two different dates: September 25, and at the start of the harvesting period on October 5. Assessment of damage was conducted following the methodology given above. Collected fruit was also weighted and correlated with damage level. Effect of Eco-Trap treatment on damage (during the two sampling dates) was inferred from an ANCOVA (Sokal and Rohlf, 1981), with elevation and average fruit weight as covariates. 2.4. Color and ammonia as attractants of control devices In order to find a more affordable system to control the olive fly we tested the YST combined with 10 gr of ammonia bicarbonate powder (Sigma Aldrich) packed on a slow releasing polyethylene sleeve (60 mm width 0.03 mm thickness, Poly-Sac, Gedera, Israel) sealed on both sides. The bags were adhered to a top corner of the YST before field exposure (see inset in Fig. 7). This device is similar to the one tested, with variable results, by Economopoulos et al. (1986) in Greece.
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Fly capture in YST þ ammonium bicarbonate, in YST alone, and in plastic McPhail traps (Yellow bottomed with transparent top; Shabtieli A.C., Givat Ein, Israel) loaded with an aqueous solution of 3% ammonium bicarbonate was assessed both in Israel and Palestine. This test was conducted in Timrat (32 690 N 35 240 E), Israel, between August and December 2011 and Tubas between June 2011 and November 2012 (in Tubas the comparison did not included the McPhail trap). In Timrat, the experiment was set in two different plots (approximately one hectare each). Five blocks were selected per plot. Each block consisted of three adjacent olive trees. The three tested traps were then suspended from the trees, serviced after one week and refreshed with clean or new traps. Each week, traps were rotated within the block. The whole experiment in Timrat continued for fifteen consecutive weeks. In Tubas, the comparison between YST þ ammonium bicarbonate and YST alone was conducted in a single plot with five blocks consisting of two adjacent trees. In contrast to Timrat, traps were serviced and refreshed every two weeks. In both cases, differences in the numbers of trapped flies between trap-types were analyzed using GLM (Statgraphics, 2000). In Timrat, blocks were treated as subjects while in Tubas, sampling stations were treated as subjects. The effectiveness of the YST þ ammonium to control olive fly damage was evaluated in Tubas during 2012 using nine plots. Three plots served as reference (no treatment), three plots were treated with Eco-Traps and three plots were treated with YST þ ammonium bicarbonate. The three different treatments were set in adjacent plots, as blocks. Plots were separated by a distance of at least 100 m. Differences in damage level between treatments were inferred using GLM (Statgraphics, 2000).
3. Results 3.1. Olive fly population and temperature trends The temperature patterns at 10:30 AM in the region of Tubas throughout the whole study are shown in Fig. 1. In general, temperature patterns during the three years are similar: average of 15 C in winter and up to 35 C in the middle of the summer (August). Main differences between the three years can be observed in the extension of the heat during the summer time. In 2010, average temperatures above 30 C extended from early June to early November, one month longer than in 2011 and 2012 which was observed between early June and early October. Fig. 1 also shows the male and female population trends during the three years of the study in the area of Tubas. In general, peaks of flight during the three years were at the same period of the year: a first peak in March, a second peak in JuneeJuly and a third one in the autumn (usually starting in October). During the hot summer (AugusteSeptember), trapping was very low. In 2010, trapping during the summer was unusually low, extending from mid-July until mid-November. This pattern contrasted with the subsequent years in which trapping levels during the summer were relatively low, but not absent or almost nil like in 2010 (Fig. 1). This unusual low trapping activity during the summer of 2010 seems to be related to the particularly hot summer and fall that affected the whole region of the Mediterranean. The level of the three main peaks of the year differed between the three years of the study. The lowest trapping levels were recorded during 2010; levels in 2011 and 2012 were similar. Male olive flies were trapped in larger numbers, in several cases up to several folds more than females during the peak periods. The yellow color of the YST probably favored the trapping of males over females, a result previously reported by Economopoulos (1977).
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Fig. 1. Average monthly olive tree canopy temperature in Tubas extrapolated from MODIS (surface land temperature) data derived from NASA Terra satellite at 10:30 AM (time of satellite service over the area) and from a model constructed with Fourier series and vegetation index (see Blum et al., 2013) (line), and male and female olive fly population trends between 2010 and 2012 in a Reference plot (i.e., non-treated) in the area of Tubas, Palestine (bars; black for males, gray for females). The plot was located at approximately 400 m above sea level.
3.2. Olive fly damage under an Eco-Trap control regime In 2010, fruit infestation levels in July 25, at the time of Eco-Trap establishment for this year, were similar in the Eco-Trap treated plots and Reference plots (H ¼ 0.5, P > 0.05), and were around 15% (Fig. 2). In contrast at the start of harvest period, in September, damage levels in general declined from those in July, and were significantly lower in the Eco-Trap treated plots (ca. 2%) than in the Reference plots (ca. 5%) (H ¼ 4.4, P < 0.05) (Fig. 2). In 2011, no fruit infestation was detected at the beginning of June (Fig. 2). Damage slightly increased in July, to an average of approximately 2%. Damage levels in October, at the harvest period, significantly increased from July to an approximate average of 9% in the Eco-Trap treated plots (F ¼ 3.1; d.f. 4, 20; P < 0.05) (Fig. 2). The average damage levels were higher in the Eco-Trap treated plots, although not significantly different (F ¼ 3.0; d.f. 1, 20; P > 0.05) than in the Reference plots. No significant interaction between treatment and sampling date was detected (F ¼ 0.7; d.f. 4, 20; P > 0.05).
Fig. 2. Olive fly damage level in Eco-Trap protected plots and Reference plots in the region of Tubas, Palestine, during the olive growing seasons of 2010e2012.
Average damage levels in 2012 were approximately 3% in Julye August in both Eco-Trap and Reference plots (Fig. 2). Damage levels significantly increased to 13% in the Reference plots by mid-October (F ¼ 19.3; d.f. 3,40; P < 0.01), beginning of the harvest period. Average damage in Eco-Trap treated plots were significantly lower during the whole growing season of 2012 than those found in the Reference plots (F ¼ 40.0; d.f. 1, 40; P < 0.01). No interaction was found between treatment and date (F ¼ 2.5; d.f. 3, 40; P > 0.05). Average concentrations of the two principal chemical components in the Eco-Trap devices exposed for 35 and 74 days during 2010 in Tubas olive orchard conditions is shown in Fig. 3. Concentration of pheromone and deltamethrin significantly differed between the two dates (for both: H ¼ 3.9, P < 0.05). While pheromone concentration was still above the active level after 74 days of field exposure, deltamethrin, the killing agent on the surface of the EcoTrap, was below the minimal required concentration (Ragoussis,
Fig. 3. Average olive fly pheromone and deltamethrin concentration in Eco-Trap devices exposed for 35 and 74 days to the environmental conditions prevailing in Tubas, Palestine, olive orchards during the summer (JulyeOctober) of 2010. Horizontal lines show the known minimal level of the chemical required for the device to be effective in attracting and killing olive flies.
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Vioryl S.A., personal communication). This result suggests that the Eco-Trap device is effective for approximately 2 months in the area of Tubas, which is shorter than the time required to protect fruit from olive fly damage in this area. 3.3. Effect of elevation on Eco-Trap ability to control olive fly damage The relationship between elevation above sea level, average damage and plot treatment, for October 5, 2011 (at the start of the harvest period), is shown in Fig. 4. Fruit infestation level was significantly smaller at lower than at higher elevations (F ¼ 31.2; d.f. 1, 62; P < 0.01). Fruit infestation significantly differed between EcoTrap treated and Reference plots (F ¼ 4.5; d.f. 1, 62; P < 0.05). Differences in damage level were more pronounced at higher elevations than at lower elevations (Fig. 4). Below 400 m asl, average damage was 5.1 2.9% in the Reference plots and 4.8 3.2% in the Eco-Trap plots, while above 400 m asl, damage in the Reference plots doubled (12.2 7.7%) as compared with the average damage found in Eco-Trap plots (6.2 3.2%). Fruit weight significantly affected the level of damage (F ¼ 34.9; d.f. 1, 62; P < 0.01). Heavier fruits were more susceptible to become damaged (Fig. 5). Degree of damage of heavy fruit was lower in Eco-Trap plots than in Reference plots (Fig. 5). The sampling date significantly affected the general level of damage (F ¼ 5.8; d.f. 1, 62; P < 0.05). No interaction was found between plot type (Eco-Trap or Reference) and sampling date (F ¼ 0.2; d.f. 1, 62; P > 0.05). 3.4. Performance of yellow sticky traps combined with ammonium bicarbonate The ability of the yellow sticky traps (YST) loaded with ammonium bicarbonate to trap flies, as compared with YST with no other attractant and McPhail traps with a solution of 3% ammonium bicarbonate, is shown in Fig. 6. The comparison of the 3 trap types was conducted in Timrat, Israel, during 2011 (Fig. 6A), and the comparison, in Tubas, Palestine was only between YST with and without ammonium bicarbonate (Fig. 6B). The YST þ ammonium bicarbonate trapped significantly more olive flies in the two locations than any of the other two trap types (Ftimrat ¼ 44.4; d.f. 2, 351; P < 0.01; FTubas ¼ 15.6; d.f. 1272; P < 0.01) (Fig. 6). In Timrat (Fig. 6A) olive fly catches significantly differed between sampling dates (F ¼ 34.5; d.f. 13, 351; P < 0.01); trapping
Fig. 5. Average olive fly damage as a function of fruit weight at the onset of 2011 harvest period in Eco-Trap protected plots and in Reference plots in the region of Tubas, Palestine.
was highest in OctobereNovember. During this period of high catches, the YST þ ammonium bicarbonate caught almost 3 times more flies than the YST without attractant or the McPhail trap with ammonium solution (Fig. 6A). No significant differences were found between YST and McPhail trapping levels in Timrat. There was a significant interaction in Timrat between catches in the different trap types and date (F ¼ 5.6; d.f. 26, 351; P < 0.01). This interaction is probably the result of the catching-patterns observed in the YST and the McPhail traps (Fig. 6A). In Tubas, the level of catches also differed throughout the whole sampling period (F ¼ 12.1; d.f. 34, 272; P < 0.01) (Fig. 6B). In Tubas there was also a significant interaction between trap-type catches and sampling date (F ¼ 3.0; d.f. 34, 272; P < 0.01). The results of the experiment conducted in Tubas in which the ability of the YST þ ammonium bicarbonate to control damage by olive fly was compared with that of the Eco-Trap is shown in Fig. 7. Level of damage in Reference plots significantly differed from the damage observed in Eco-Trap and YST þ ammonium bicarbonate plots (F ¼ 21.4; d.f. 2, 22; P < 0.01). No significant differences were observed between YST þ ammonium bicarbonate plots and EcoTrap plots. Average level of damage in Reference plots at the onset of harvest was four-fold larger than the one found in the YST þ ammonium bicarbonate and the Eco-Trap plots. Damage significantly increased throughout the growing season (F ¼ 5.8; d.f. 3, 22; P < 0.01), but no interaction was detected between sampling date and treatment (F ¼ 2.2; d.f. 6, 22; P > 0.05). 4. Discussion
Fig. 4. Average olive fly damage levels at the onset of 2011 harvest period in the region of Tubas, Palestine, in plots located at different elevations above sea level, and treated with Eco-Traps or without any treatment to control olive fly fruit injury.
Control of the olive fly with lure and kill and/or mass-trapping has been attempted in the past with variable levels of success. In mainland Greece, Eco-Trap devices were shown to effectively control olive fly populations and damage (Broumas et al., 2002; Ragoussis, 2002, 2005). Other studies have also claimed successful olive fly control with a variety of devices (e.g., Haniotakis and Skyrianos, 1981; Jones et al., 1983; Haniotakis et al., 1986, 1991; Ricciolini et al., 2000; Petacchi et al., 2003). In the present study, our results suggest an effective control of the olive fly using both the lure and kill and mass-trapping approach in the region of Tubas. The level of control varied with year and location of plots along an elevation gradient. In 2010, damage was significantly lower in EcoTrap plots than in control. The general economic effect of control for this year, however, was minimal since general damage in the area
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Fig. 6. Trapping trends of male and female olive flies (shown as total) on yellow-sticky trap devices (YST) loaded with ammonium bicarbonate, and without ammonium, and in McPhail traps activated with an aqueous solution of 3% ammonium bicarbonate in Timrat (Israel) during 2011 (A), and in Tubas, Palestine, during 2011 and 2012 (B). In Tubas, only yellow sticky traps with and without ammonium bicarbonate were compared.
was relatively low. In 2011 we were unable to show any significant effective control at 400 m. This being probably due to the fact that the Eco-Traps were redeployed after three months, and not after two months as recommended from the results of 2010 (see Fig. 3). However, control and damage were shown to be highly linked to elevation. The Eco-Trap showed some effectiveness in controlling the fly at elevations above 400 m, as compared with the Reference plots at this height. The efficiency of the Eco-Traps at higher elevations remained for a longer period of time due to lower temperatures. In addition the general damage level in 2011 in the region was relatively low. The effectiveness of lure and kill and mass-trapping as a control strategy was in fact more evident during 2012. In the two set of experiments running that year, lure and kill and mass-trapping devices (Eco-Trap and YST þ ammonium bicarbonate) showed a significant ability to control damage inflicted by the olive fly, reducing infestation by more than 50%.
Fig. 7. Olive fly damage level in Eco-Trap protected plots, yellow-sticky traps (YST) loaded with ammonium bicarbonate protected plots and Reference plots in the region of Tubas, Palestine, during the olive growing season of 2012. The inset shows a picture of the RimiÒ yellow sticky-trap loaded with ammonium bicarbonate.
In a previous study (conducted between 1999 and 2001) in which Eco-Trap devices were investigated as a tool for lure and kill control of the olive fly in Israel, we already observed that the EcoTrap can effectively control damage of highly sensitive varieties in the region (Nestel et al., 2002, 2004). In the 1999e2001 study, damage levels were kept below 7% in very sensitive olive-fly varieties while control plots reached up to 50% of infestation (Nestel et al., 2002). This previous result encouraged us to select this device to explore the possibility of applying lure and kill as a strategy to control olive fly damage in Tubas. During the 1999e2001 study, however, two main difficulties were already pointed out: the need for a higher density of devices than the recommended by the producer (Ragoussis, 2005), and the need to approach control with a lure and kill strategy from a regional perspective (Nestel et al., 2004). The reason to double the density of devices during this early experiment was linked to the observation that the duration of the effective activity of the Eco-Trap in the summer of Israel was shorter than that reported by the manufacturer for Greece conditions (Ragoussis, 2005), requiring an addition of a second round of Eco-Traps after 2 months of field exposure (Nestel et al., 2002). In the present study, we also found a similar effective field-life span of the Eco-Trap at the conditions of Tubas (Fig. 3). Thus, although we knew that control with the Eco-Trap was not economically viable before starting the project, the aim of using this device in the current study was to explore the application of the lure and kill concept in Tubas with a known effective tool. The results of this study were very encouraging, suggesting that this approach is viable, and leading us to look for a more economical alternative control system for the region of Tubas, and other areas of Palestine. From the results of 2011 and 2012, it seems that the YST þ ammonium bicarbonate may fulfill this aim. This device showed both a stronger attractiveness of the olive fly than nonammonium bicarbonate baited YST and baited McPhail trap (Fig. 6), and an ability of control comparable to the Eco-Trap (Fig. 7). The more accessible cost of the YST is based on the fact that odorattraction is only sustained by ammonium bicarbonate and not by pheromone, and the possibility of cleaning and recycling the YST plastic for several field applications. Thus, although labor-intensive,
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the application of the mass-trapping strategy based on YST þ ammonium bicarbonate dispensers may be appropriate for places where labor is available in excess and where capitalintensive systems are not accessible. Before implementation, however, the YST þ ammonium bicarbonate device should be tested at more environmental conditions of Palestine and throughout more years, and simple systems of recycling should be developed and tested. Lower olive fly populations during 2010, and during the summer months, and reduced damage in areas below 400 m asl, is probably linked to the effect of temperatures on olive fly survival, activity and reproductive effort. Above 29 C olive fly has been reported to halt flying and reproductive activity (Avidov, 1954). Above 30 C, olive fly eggs, larvae and adult start to die and temperatures above 35 C may be highly detrimental to the population (Tsiropoulos, 1972; Tzanakakis, 2003 and references therein). Moreover, olive fly trapping patterns have been shown to be affected by elevation and seasons of the year, and linked to the environmental temperature regimes affected by elevation and season (Kounatidis et al., 2008). During the summer months, temperatures in many areas of Israel and Palestine usually are above 30 C (Blum et al., 2013). High temperatures can frequently exceed 35 C, and stay for prolonged periods of time. The temperature in Tubas throughout summers is high, above 30 C (Fig. 1), being several degrees warmer the more we descend in elevation above sea level (unpublished data). Thus, both, summer and lower elevations are expected to affect olive fly population and damage. This was in fact the observed patterns in Tubas during the three years (Figs. 2 and 4). In this sense, 2010 was of special interest. During 2010 population levels were low, as expressed by low trapping levels (Fig. 1), and damage at Tubas was relatively minor (around 5% without protection). During 2010, average temperatures during the summer months were slightly higher than the ones observed during 2011 and 2012 (Engelhard, 2012). Of more importance than the slightly higher temperatures registered during 2010, however, was the fact that the hot summer extended for an extra month, until earlyNovember (Fig. 1), leading to a delay in the appearance of the fall peak in olive fly trapping throughout the entire region (Engelhard, 2012). This delayed emergence of the fall population, and the fact that harvest was initiated early in October, explain the low olive fly damage in the experiment, and the low damage reported by farmers throughout the entire region. As mentioned earlier, our previous study (1999e2001) suggested that the implementation of lure and kill and mass-trapping as a control strategy should be undertaken at a regional level (Nestel et al., 2002). This was our initial aim in Tubas, and the exploration of damage and Eco-Trap efficacy at different elevation pointed towards this direction. Our observations regarding the effect of elevation and control during 2011, support this idea and approach. The differential level of damage observed with elevation can be managed differentially if the entire region is integrated into a cooperative enterprise. The fact that at lower elevations damage is in general much lower than at higher elevations, suggest that low elevation orchards could be managed with less lure and kill and/or mass-trapping control efforts, directing resources and management efforts to the high elevation orchards. At the completion of the project, this approach was suggested to the farmers’ organization, and we expect that its adoption, together with the incorporation of a less expensive device, will lead the whole community to produce good quality organic olive oil suitable for export. Acknowledgments To the farmers and olive producers of Tubas for their willingness to provide us with access to their orchards. To Mayumi Yoshida for
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her professional, and humane, management approach throughout the project and to her invaluable collaboration, and to all members of NICCOD for their help and enthusiastic participation. Also to Miriam Kishinevsky for technical assistance and to Dr. N. Ragoussis (Vioryl, S.A.) for his support in analyzing Eco-Traps. To Dr. Ezra Dunkelblum for his suggestions and language improvements. We appreciate the input of three anonymous reviewers that helped improve an early draft of the manuscript. The project was financed by the Ministry of Foreign Affairs of Japan through Nippon International Cooperation for Community Development (NICCOD), project no 131-1631.
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