Mating Disruption of Striped Rice Stem Borer: Importance of Early Deployment of Dispensers and Impact on Airborne Pheromone Concentration

Aitor Gavara, Sandra Vacas, Jaime Primo, Vicente Navarro-Llopis

Letter

Mating Disruption of Striped Rice Stem Borer: Importance of Early Deployment of Dispensers and Impact on Airborne Pheromone Concentration

Aitor Gavara, Sandra Vacas, Jaime Primo, Vicente Navarro-Llopis

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Mating disruption (MD) is an effective environmentally- friendly control method against the striped rice stem borer (RSB),(Lepidoptera: Crambidae). In this study, the current MD dispensers release the pheromone exponentially, with higher initial release rates that decrease throughout the time. To adjust the timing of dispensers’ deployment and evaluate the importance of controlling the early first or the second male flight, field trials were carried out to test the efficacy of two strategies: the early dispenser deployment prior to the first male flight (May) and the late deployment prior to the second flight (June). The early dispenser deployment was more effective in reducing plant damage inflicted by RSB when assessed at harvest. However, neither of these strategies was able to inhibit the male catches of the third flight due to the dispensers’ depletion. Attending to the airborne pheromone concentrations obtained, around 1.60 ng/m3were capable to inhibitmale flight effectively.

RSB is one of the most serious rice pests in Asia, southern Europe and northern Africa (Chen et al, 2011). It is a polyphagous pest that can develop three generations annually under Mediterranean climate conditions (Vacas et al, 2016). Damage and losses are produced when plant stems are bored by RSB larvae, leading to the death of the top of the plant producing ‘white heads’ with unfilled grains (Chen and Klein, 2012). Conventional chemical control against this pest is restricted or banned in many areas since paddy fields are placed in environmentally protected areas, such as the whole rice- growing area of the Valencian Region, Spain. In these cases, MD withsex pheromone is an effective alternative to insecticides (Alfaro et al, 2009; Vacas et al, 2016). This study demonstrated that controlling the first emerging moths was crucial for efficacy and deploying MD dispensers prior to the first RSB male flight was more effective in reducing plant damage.

Bioselibatepheromone dispensers (Suterra LLC, Oregon, USA) are employed by all rice producers, in a collective strategy promoted by the regional government, to fight this pest by MD in the area of Valencia (16000 hm2). These are extrusion devices based on a cellulose-matrix, where the pheromone (250 mg) is impregnated in a mixture of ()-11-hexadecenal, ()-13-octadecenal and ()-9-hexadecenal (10:1:1) (Tatsuki et al, 1983). They are installed on stakes, 0.6 m above the ground, evenly distributed at a density of 31 dispensers/hm2on a 18 m × 18 m grid. Even though these dispensers provide good efficacy, our main goals were to evaluate their lifespan and how the date of their deployment affects the efficacy of MD. The release profile of the dispensers and the airborne pheromone concentrations present in the treated fields were simultaneously studied to establish the best deployment date to optimize their emission and to ensure better protection against this pest.

Three experimental replicates (blocks) were conducted in different paddy fields (Bomba cultivar) in the Valencian Region (Spain): a 17-hm2field located in Sueca (València) and two 90-hm2fields both located in Pego (Alicante). Each block included two plots to install two different MD strategies: (1) early dispenser deployment on 24 May 2019, prior to the first male flight and before the seeding, and (2) late dispenser deployment on 18 June 2019, prior to the second flight, after plant-emerging. No untreated plots were included in this study due to the collective strategy of MD followed in these areas. MD treatment efficacy was checked according to population monitoring (male captures in each plot) andcrop damage assessments (the number of infested plants inside 1-m2plots randomly selected). Both parameters were recorded at the center of each plot to avoid pheromone drift and edge effects.

The low male captures recorded in the three blocks (Fig. 1-A) are comparable to those reported in past studies carried out in the same area (Alfaro et al, 2009;Vacas et al, 2016), which is a consequence of the prolonged use of MD. Whilst male flights were not detected in the plots that received early dispenser deployment (May) until the third flight (90 days after their deployment when ears are ripening), the late deployment (June) strategy was not effective for the complete inhibition of the second flight catches (coinciding with ear-development). The third male flight was detected at the end of the growing season although no significant differences were observed between treatments (2= 0.05,= 1,21,= 0.82).

Fig. 1. Results of different deployment strategies (Early and Late): Male flights, dispensers’ emission rates and airborne pheromone quantifications.

A, No. of male captures per trap per day (CTD) throughout the crop season with different mating disruption treatments. Early deployment of pheromone dispensers was conducted in May of 2019 and late deployment in June of 2019. Values are Mean ± SE (= 4). B, Residual pheromone content of bioselibatedispensers installed in May and June vs. the time of field exposure. C, Absolute airborne pheromone concentrations in the rice field treated with passive dispensers Bioselibateinstalled at 24 May, 2019. Air samples were collected monthly from June to September during the crop cycle. Bars labelled with different lowercase letters are significantly different by one-way analysis of variance followed by the Fisher’s LSD test (< 0.05). Values are Mean ± SE (= 4).

Damage level after the 2nd flight (Table 1) was low and similar to that reported in other experiments carried out in the same area, where damaged plants did not exceed 1.50 infested plants per m2(Alfaro et al, 2009) or 1% of damaged plants (Vacas et al, 2016). The level of plant attack was significantly lower in all the plots where dispensers were deployed early in the season. These early-treated plots suffered 27.0%–61.5% less damage than the strategy of late dispenser installation. Attending to the assessment carried out at post-harvest, the presence of RSB was high with both MD treatments as the third generation was allowed to build up. However, the damage in the early-treated plot remained significantly lower than that in the late-treated ones.

In parallel with the MD experiments, additional MD dispensers were aged in nearby areas of Sueca from the date of their deployment (24 May or 18 June 2019) until the harvest, to obtain their pheromone release profiles. Four dispensers were taken from the field each month to analyze their residual pheromone content by gas chromatography. Results showed that the residual pheromone content of the field aged dispensers fitted exponential models (Fig.1-B), with higher initial release rates and lower ones at the end of their lifespan. Early-deployed dispensers (May) emitted 50% of their pheromone load during the first month of field exposure, whilst the dispensers installed in June (late deployment) released 60% of their content in the same time interval. Higher temperatures could explain the higher emission performed by the dispensers installed in June (21 oC from May 24 to June 24 vs. 25 oC from June 18 to July 18). This fact caused that the residual pheromone content of these dispensers in the third month from their installation matched with the pheromone content of the May dispensers in their fourth month of ageing (around 80% of the pheromone released). The late deployment caused higher emissions in the same period of time and all the dispensers reached the end of their lifespan practically at the same time. In this way, the mean pheromone released by the dispensers, regardless the deployment date, was the same [60 mg/(d·hm2)]. Lower release rates at the end of their lifespan meant reduced emission during the second and the third male flights.

Table 1. Number of infested plants per square meter and percentage of attacked plants (%) obtained with each treatment in the damage assessment carried out after the second male flight and at post-harvest.

Assessments were performed after the second male flight in three blocks.For post-harvest, assessment was carried out only in Sueca by checking the non-burnt stubble. The statistical analyses showed significant differences between treatments (GLMM with likelihood ratio tests and Tukey’s HSD tests for post hoc pairwise comparisons,< 0.05). Values are Mean ± SE.

Airborne pheromone concentrations were also quantified. Air samples from paddy fields were monthly collected in Sueca coinciding with different plant growth phenological stages. Three samples were taken in June, coinciding with the setting up of the dispensers and the seeding, four samples in July (tillering formation), four in August (flowering) and the last three at the beginning of September (end of ripening). Air was sampled with a high-volume air sampler (CAV-A/Mb, MCV, Barcelona, Spain) provided with an adsorbent 30 g/L polyurethane foam (PUF) (MCV, Barcelona, Spain), at 15 m3/h for 24 h. Sampling and pheromone quantification were based on airborne pheromone quantifications in vineyards done by Gavara et al (2020). The profile of airborne pheromone concentrations present in the field followed the same trend observed in the release profile of the dispensers installed in May, with the emission rate and the airborne concentration decreasing significantly throughout the crop cycle (= 23.82;= 13,3;< 0.001) (Fig.1-C). The most significant reduction of the airborne pheromone occurred after the first month, from 1.60 to 0.74ng/m3at the beginning of June and July, respectively (< 0.001). After the second month, the quantified concentration decreased but not significantly, reaching 0.41 ng/m3(= 0.057). At the end of the season, the mean concentration decreased up to 0.24 ng/m3, differing significantly from the initial sampling periods (= 0.013). These results match with the dispensers’ release profiles, with higher emission at the beginning of the growing season [147.66 to 60.44 mg/(d·hm2) from June to July] and lower rates at the end of their lifespan [23.83 and 9.93 mg/(d·hm2)].

As depicted in Fig. 1, neither strategy was able to control the third male flight, which agrees with the depletion of the MD dispensers. This more abundant uncontrolled flight allowed population to build up, obtaining percentages of infested plants over 20% in the post-harvest assessment. This last damage assessment, despite not being useful to reduce yield losses since the rice is already harvested, highlight the importance of the traditional cultural practices conducted at the end of the crop cycle (burning or removing the straw rests and flooding the fields) to reduce the hibernating population on the perimeter marsh vegetation of the paddy fields, such as grasses, reeds and sedges. These individuals emerge later and migrate again toward the rice plants in the next season (Batalla, 1999). Accordingly, our results suggest that it is not essential to control the third male flight but an early deployment of the MD dispensers is recommended. An effective disruption of the first male flight is probably avoiding or delaying the mating of the first emerging moths that will colonize the young rice plants. By contrast, when dispensers are deployed after the first flight, the establishment of migrating gravid females in the rice fields and the development of the subsequent generation are then allowed.

The airborne pheromone concentrations obtained decreased in parallel with dispensers’ pheromone emission and never exceeded 1.60 ng/m3. Recent studies measuring airborne pheromone concentrations in vineyards obtained higher values, reaching in occasions more than 40 ng/m3(Gavara et al, 2020). These differences could be explained by factors related to the crop (type, height, foliage, etc), the environment or the kind of MD dispensers used. Vines are crops with a well-developed foliage that can act as pheromone reservoirs and reduce pheromone washing caused by wind (Karg and Sauer, 1997;Gavara et al, 2020). By contrast, rice is an herbaceous crop with limited foliage surface. The characteristic leaves of grasses, smaller and thinner layer of waxy surfaces, were described as a disadvantage for adsorbing pheromone (Karg and Sauer, 1997). In addition, their size and luxuriance does not prevent the crop area from pheromone-washing by strong wind exposition.

The pheromone dispensers employed againstin vineyards are hand-applied passive dispensers deployed at 500 dispensers/hm2that provide ca. 600 mg/(d·hm2). In contrast, the dispensers employed againstare also hand-applied but are installed at lower densities (31 dispensers/hm2) that provide ca. 60 mg/(d·hm2). Since the reported pheromone emission is around 10 times lower in paddy fields than in vineyards, it is consistent that the pheromone concentration measured in air is around 20 times lower in the paddy fields than in vineyards.

The decreasing quantity of airborne pheromone throughout the crop cycle, together with the decreasing emission rate of the dispensers, suggests that emissions above 70.19 mg/(d·hm2), producing 1.60 ng/m3of airborne pheromone, inhibitmale flight effectively. However, when airborne pheromone decreased under 0.45 ng/m3[with emission rates under 30 mg/(d·hm2)], male flight was not consistently disrupted, as captures were detected in the late-treated plots but not in the early-treated ones during the second flight. With these data, we cannot state whether the lack of male captures during the second flight in the early-deployment treatment was caused by the airborne pheromone concentration or by the fact that there was less moth migration into these fields and consequently lower populations installed after the first flight.

In conclusion, the late deployment of the MD dispensers after the first flight allowed the population to build up since the migration of mated females to the paddy fields was not avoided, suffering greater damage as set out in damage assessment results. Despite the unavailability of final yield loss data in our study, a 20-year data set showed that 1% of dead plants or white head panicles caused from 2.5% to 6.4% yield loss (Liu, 1990; Bandong and Litsinger, 2005). We hypothesized that this greater damage is probably due to a higher incidence of the mating of the first moths emerging from the neighbor vegetation, which were not affected by the late dispenser deployment. Accordingly, it would be interesting to study if early treatments applied to the adjacent vegetation of the paddies, such as installation of MD dispensers or spraying with liquid pheromone formulations (e.g. microencapsulated), before the seeding could be effective to reduce the offspring of the overwintering population. Moreover, it could be a convenient practice to reduce the initial populations rather than the early dispenser deployment inside the paddy fields which can be sometimes difficult to manage when seeding dates are not properly synchronized along the growing area.

Acknowledgements

This study was funded by Conselleria de Agricultura, Medio Ambiente, Cambio Climático y Desarrollo Rural (Generalitat Valenciana), Spain(Grant No. S8456000).Authors thank José Clérigues (Sueca) for providing experimental paddy fields and José Vicente Bolinches for his assistance in field experiments. We are also grateful to Ana Castellar for language editing.

SUPPLEMENTAL DATA

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Aitor Gavara (aigavi@etsiamn.upv.es); Sandra Vacas (sanvagon@ceqa.upv.es); Vicente Navarro-Llopis (vinallo@ceqa.upv.es)

22 December 2020;

14 May 2021

Copyright ? 2021, China National Rice Research Institute. Hosting by Elsevier B V

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Peer review under responsibility of China National Rice Research Institute

http://dx.doi.org/10.1016/j.rsci.2021.09.001