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Keywords:

  • (Z)-7-tetradecen-2-one;
  • Anomala orientalis ;
  • blueberries;
  • mating disruption;
  • pheromone;
  • turfgrass

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The oriental beetle, Anomala orientalis (Waterhouse) (Col., Scarabaeidae), is the most important root-feeding pest of blueberries and turfgrass in New Jersey, USA. Previous studies showed that mating disruption is a feasible option for oriental beetle management; however, assessing its efficiency can be challenging, and little is known on its long-term effects. Accordingly, we conducted studies to investigate low-dose pheromone lures equivalent to oriental beetle females (i.e. female mimics) as easy-to-use indicators of mating disruption success, determine the distance at which oriental beetle males respond to female-mimic lures and assess the long-term (3-year) effects of mating disruption on oriental beetle populations in entire blueberry fields. Our studies showed that rubber septa baited with 0.3 μg of the oriental beetle sex pheromone (Z)-7-tetradecen-2-one attract similar numbers of males as compared with virgin females and can thus be used as a female mimic. The range of attraction of this lure was found to be also similar to virgin females and <30 m. In blueberries, mating disruption provided 87% inhibition of oriental beetle populations (trap shutdown) over a 3-year period. Oriental beetle male captures in disrupted fields were threefold higher along the field edges than in the field interiors, indicating movement of males from nearby areas into the pheromone-treated fields. In addition, mating disruption reduced male attraction to female-mimic lures by 93% in all 3 years and reduced the number of larvae in sentinel potted plants in 1 of 2 years. These results show for the first time that mating disruption provides consistent long-term field-wide control of oriental beetle populations and that female-mimic pheromone lures can be used as a new tool to assess oriental beetle mating disruption success.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Highbush blueberries, Vaccinium corymbosum L., are a major component of the southern New Jersey (USA) agricultural economy where this crop is grown on 3000 ha with a total annual production of approx. 19.5 million kg, valued at US $ 80.8 million (USDA NASS 2013). The oriental beetle, Anomala orientalis (Waterhouse) (Col., Scarabaeidae), is the most abundant white grub pest in blueberry farms in New Jersey (Polavarapu 1996) and is considered by farmers as one of the most important insect pests of blueberries in the state (Rodriguez-Saona et al. 2009). In New Jersey, oriental beetle adults start to emerge in early June, reaching peak flight in mid- to late June (C. Rodriguez-Saona, personal observation). Females lay eggs in the soil at the base of bushes. The larvae go through three instars, with most larvae reaching the third instar by mid-September. Larvae remain in the soil during winter, resume feeding the following spring and enter the pre-pupal stage in late May. The root-feeding damage caused by larvae can result in complete destruction of the root system and the death of host plants, especially when larval populations are high (C. Rodriguez-Saona and D. Polk, personal observation). Infested bushes show reduced vigour and fewer berries. This insect is also considered a major pest of turfgrass and ornamentals (Vittum et al. 1999).

Limited options are currently available to control oriental beetle populations in blueberries. Although the neonicotinoid imidacloprid is the only insecticide registered in blueberries for larval control, there are several concerns associated with its use including limited efficacy against late-instar larvae (Koppenhöfer and Fuzy 2008) and its potential to disrupt pollination and biological control (e.g. Decourtye et al. 2003; Rogers and Potter 2003). Having a single control method for oriental beetle control also raises considerable resistance management issues. Because blueberries are grown in an ecologically sensitive region of New Jersey, known as the Pinelands or Pine Barrens that is characterized by porous acidic soils and a high water table, it is doubtful that other soil-applied insecticides will be registered. Chemical control methods do not target the adult stage because adults cause no economic damage to blueberries, their emergence period is long and occurs during harvest and they are difficult to target with insecticide sprays due to their cryptic behaviour (Facundo et al. 1999).

An alternative to insecticides for pest control is the use of mating disruption (Cardé 2007; Rodriguez-Saona and Stelinski 2009). Previous studies demonstrated the feasibility of using microencapsulated sprayable formulations of (Z)-7-tetradecen-2-one, the major component of the oriental beetle's sex pheromone, for oriental beetle mating disruption in blueberries (Polavarapu et al. 2002) and turfgrass (Koppenhöfer et al. 2005). Polavarapu et al. (2002) found a 90% reduction in trap male captures in 1-ha plots treated with the pheromone compared with untreated plots. However, because the oriental beetle pheromone is a ketone, use of sprayable microencapsulated formulations is restricted in food crops (Weatherston and Minks 1995). On the contrary, retrievable hand-applied plastic dispensers are exempt from tolerance restrictions. Using 50–75 hand-applied plastic dispensers per ha containing (Z)-7-tetradecen-2-one at 1 g a.i./dispenser, Sciarappa et al. (2005) showed lower trap captures, reduced mating rates and fewer larvae in 1-ha blueberry plots treated with pheromone dispensers compared with untreated plots. Subsequent studies showed that a low rate of 0.05 g a.i./dispenser at 50 dispensers per ha (total pheromone = 2.5 g/ha) was sufficient to provide effective oriental beetle mating disruption in blueberries and was comparable in cost to an imidacloprid treatment (Rodriguez-Saona et al. 2009).

Retrievable hand-applied plastic dispensers (ChemTica Internacional S.A., Costa Rica) for oriental beetle mating disruption became registered in 2013. Now that this technology is available to blueberry farmers, it is most likely that they will treat entire fields instead of field sections. Accordingly, in this study, we scaled-up the area under mating disruption by treating entire blueberry fields with hand-applied plastic pheromone dispensers. In previous studies, virgin oriental beetle females were used to assess the success of mating disruption in blueberries (e.g. Sciarappa et al. 2005; Rodriguez-Saona et al. 2009, 2010) and turfgrass (e.g., Koppenhöfer et al. 2008). Because the process of collecting and rearing oriental beetles to obtain virgin females is labour-intensive and unlikely to be used by farmers, another of our objectives was to identify a ‘female mimic’, that is, a pheromone-dispensing device and dose that attracts male oriental beetles in similar numbers as virgin oriental beetle females.

Thus, this study's main goals were to develop an easy-to-use method to assess mating disruption for oriental beetle and prove the long-term efficacy of mating disruption in suppressing oriental beetle populations. Specifically, (i) we tested low-dose pheromone lures equivalent to oriental beetle females for use as indicators of mating disruption success – a study carried out in blueberries and turfgrass, (ii) we determined the distance at which oriental beetle males respond to these low-dose pheromone lures–a study carried out in turfgrass and (iii) we conducted a 3-year study to determine the long-term effects of mating disruption on oriental beetle populations – a study carried out in blueberries.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Female-mimic, low-dose pheromone lures

In 2009 and 2010, experiments were conducted to develop a method that would attract males at a rate comparable with virgin females. The new method should ideally replace the female with a lure because lures are easier to obtain and have more uniform pheromone release rates than females. These experiments were carried out in turfgrass and blueberry fields, because both are preferred hosts of oriental beetles and have contrasting architecture, using two different trapping devices (traps and cages) in combination with three different lures. Treatments were a newly emerged virgin oriental beetle female (placed in a metal mesh cage with some moist paper towel), red rubber septa loaded with 0.3, 1 or 3 μg of the oriental beetle pheromone ((Z)-7-tetradecen-2-one) and a control (for a total of five treatments). These lures contained pheromone amounts 10–1000 times lower than those used in previous studies (Sciarappa et al. 2005; Koppenhöfer et al. 2008; Rodriguez-Saona et al. 2009). In 2010, the 3-μg lure was eliminated because in 2009, as compared to females, it attracted higher number of males (see Results section). To obtain virgin females, larvae collected in May were reared to adults in the laboratory in individual plastic cups. The trapping devices were Japanese beetle traps (Trécé Inc., Adair, OK) and a cage as used by Koppenhöfer et al. (2008) and Rodriguez-Saona et al. (2009). Controls were traps and cages without female or lure. Cages consisted of a small cage made from aluminium screen (3 mm openings) and 10 cm in diameter and 10 cm in height. The small cage had six openings in the lateral walls with microcentrifuge tubes (1.5 ml) tightly fitted in the openings. The bottoms of the tubes had been cut off and the lids removed. The size and position of the tubes made entry of males easy but exit very unlikely (Koppenhöfer et al. 2008; Rodriguez-Saona et al. 2009). Thus, the top of the tubes (10 mm diameter) was flush with the outside surface of the cages, but the bottom end (7 mm diameter) extended 20 mm into the inside of the cages. A soil core was taken with a standard size golf hole cup cutter and placed into a plastic pot (10 cm diameter × 10 cm depth). The small cage was then positioned snugly into the pot. The top of the cage was closed with a plastic lid and the cage and lid secured with rubber bands around the bottom of the pot and the lid. The cage/pot arrangement was placed in the hole in the soil.

For turfgrass, Japanese beetle trap-based trapping devices were placed in the ground with only the funnel part above ground (Koppenhöfer et al. 2008). And to protect the small cage-based trapping device from damage by equipment and predators, a larger cage was placed over the small cage and secured to the ground with metal hooks. The larger cages consisted of strong iron screening (2.5 cm openings) about 30 cm in diameter and 15 cm in height. Ten (2009) and eight (2010) different trapping device–lure combinations (1 replicate) were placed in a 6.2 × 6.2 m grid pattern in a low maintenance turf area at the Rutgers Horticultural Farm II (North Brunswick, NJ). For blueberries, the Japanese beetle trap-based trapping devices were hung from metal poles so that the trap bottom touched the ground as described in Rodriguez-Saona et al. (2009). And the cage-based trapping devices did not have to be protected by larger cages because of the lower risk of damage. Eight to ten different trapping device–lure combinations (1 replicate) were placed at the edge of a blueberry field in a commercial farm (Hammonton, NJ) and at least 10 m from each other.

In both commodities, treatments were arranged in a randomized complete block design with 3–4 replicates in each of two experiment repetitions in each of 2 years. All sites contained natural oriental beetle populations. In 2009, the first experiment was conducted from the last week in June through the 1st week in July, while the second experiment was conducted from the 1st week in July through the 2nd week in July. Same periods were used in 2010 for both experiments. Treatments were set up around 16:00 hours of the first day of an experiment and terminated around 10:00 hours of the fourth day of the experiments (i.e. 66-h exposure). The traps/cages were recovered and the number of males found in each determined. For the cages, the soil portion in the pots was also carefully searched for males.

Range of attraction of female mimics

In 2009, the oriental beetle male range of attraction to different pheromone sources was investigated in mark, release, and recapture field studies. The range of attraction is defined as the distance at which oriental beetle males respond to the different pheromone sources. Experiments were conducted in turfgrass areas treated with the insecticide Merit® (imidacloprid; Bayer, Research Triangle Park, NC) in the preceding year to reduce any interference from the background natural oriental beetle population. Trécé Japanese beetle traps were placed in the ground with only the funnel part above ground. The traps were lured with newly emerged virgin oriental beetle females placed in a metal mesh cage with some moist paper towel or a red rubber septum loaded with 0.3, 1 or 3 μg of the oriental beetle sex pheromone. Colour-marked males were released 1.9, 3.81, 7.63, 15.25 and 30.5 m downwind (prevailing wind direction) from the traps (50–100 males per distance). Oriental beetle males (collected from Japanese beetle traps baited with (Z)-7-tetradecen-2-one overnight at the Rutgers Horticultural Farm II) were marked with different colours using Testors enamel paints (The Testor Corp., Rockford, IL) on the pronotum and/or left or right elytra according to experiment repetition, pheromone treatment and distance from source they were released from. Recapture rates were determined after 24 h. For each treatment, one replicate was tested on each of four separate days (3, 7, 9 and 15 July) with trap locations switched each time.

Long-term mating disruption

A 3-year (2010–2012) experiment was conducted to evaluate the efficacy of hand-applied plastic pheromone dispensers (ChemTica Internacional SA, Heredia, Costa Rica), deployed in entire commercial blueberry fields, for oriental beetle control. The study was carried out from the 1st week in June through the 2nd week in August–this time period covered the entire oriental beetle adults' emergence period in the field. Four blueberry fields (2–4 ha each) located in four different farms (Hammonton, NJ) were treated with 50 dispensers per ha. Each dispenser contained 0.05 g of (Z)-7-tetradecen-2-one (i.e. total of 2.5 g a.i./ha, max. of 10 g a.i./field). Four other fields of similar size within the same four farms were left untreated (controls). At least one side of all fields faced a wooded or grassy area, while the other sides faced other blueberry fields. The experiment was designed as randomized complete block with two treatments replicated in four different farms. Farms were used as blocks.

Three methods were used to assess mating disruption: (i) Trap shutdown – In all 3 years, eight Japanese beetle traps (Trécé) baited with 300 μg of the oriental beetle sex pheromone (Sciarappa et al. 2005; Rodriguez-Saona et al. 2009) were placed in each of the blueberry fields and monitored weekly to determine male populations (trap shutdown). Traps were placed the same week the dispensers were placed in fields, that is 1st week in June. Lures in traps were replaced after 4 weeks (Sciarappa et al. 2005). To investigate any edge effects, five traps were placed along the field borders, while the other three traps were placed in the field's interior. Traps were placed at least 10 m apart. One interior trap was placed in the centre of the field (central row) and the other two interior traps were placed 6 rows away from it on opposite sides. (ii) Female-mimic lures–In all 3 years, the attraction of oriental beetle males to virgin females or female-mimic lures was evaluated in each field by placing Japanese beetle traps containing a newly emerged virgin female or a septum loaded with 1 or 0.3 μg of the oriental beetle pheromone or neither. Japanese beetle traps were used instead of small cages because traps are commercially available and thus more likely to be used by farmers. Also, traps and cages captured similar number of males in blueberries (see Results). These traps were placed in fields at least 10 m apart, in a single row three rows away from the central row, deployed twice over a 2-week period: at the end of June and in the 1st–2nd week of July, and for three nights and then retrieved to determine male presence. (iii) Larval infestation – In 2011–2012, number of larvae per field was assessed by placing a newly emerged virgin female in each of five pots containing a 2- to 3-yr-old blueberry plant (n = 40 virgin females). Pots were located in fields within a row, 3 rows away from the central row and on opposite side of traps containing female-mimic lures, and spaced at least 10 m from each other. Females were tethered to the plant using a fishing line carefully tied to the elytra as described in Rodriguez-Saona et al. (2009). Pots with tethered females were placed in the field at the end of June, that is at peak adult emergence. Females in traps and pots were not replaced because adult oriental beetles can live for about 2 weeks (A.M. Koppenhöfer, personal observation). Shortly after this period, enough for females to call for males, mate and lay eggs, pots were transported to a greenhouse, and the number of larvae in each pot was determined by destructive sampling in September, that is, when grubs had reached the 3rd instar.

Statistical analyses

For the female-mimic study, the effects of trapping device, lure, and experiment repetition (date), and interactions among any of these factors, on oriental beetle male captures were analysed using analysis of variance (anova) (Minitab 16; Minitab Inc., State College, PA). Data from turfgrass and blueberries for the two different years were analysed separately. For the mark-and-release study, the effects of pheromone source, distance males were released from the trap, and day of release, and interactions among these factors, on numbers of marked and unmarked (feral) male captures were analysed by anova. Regression equations were developed for each pheromone source by plotting on a semi-log scale the percentage of males recaptured (y-axis; log scale) on the distance they were released from the trap (x-axis; linear scale) (SigmaPlot 11; Systat Software, San Jose, CA). Zero percentage recovery was estimated based on these equations; due to the shape of the curves (log decline), for practical purposes, 0% recovery was assumed at <0.1% recovery. For the long-term mating disruption study, data on number of beetles in traps (trap shutdown), attraction of males to female-mimic lures and number of larvae per field were analysed separately using anova. For trap shutdown, the following independent variables and their interactions were tested: treatment (mating disruption vs. control), trap position (edge vs. interior), year and farm (block). For female-mimic lures, the following independent variables and their interactions were tested: treatment (mating disruption vs. control), lure type (female, female mimic and control), year and farm (block). For larval infestation, the following variables and their interactions were tested: treatment, year and farm. For all studies, when needed, data were natural log-transformed (x + 1) to meet normality requirements, and Tukey's tests were used for multiple pairwise comparisons among group means.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Female-mimic, low-dose pheromone lures – turfgrass

2009 experiment

In 2009, lures used were a virgin female and red rubber septa loaded with 0.3, 1 or 3 μg pheromone. anova showed that oriental beetle male capture was significantly affected by trapping device (F = 136.07; d.f. = 1, 43; P < 0.001), lure (F = 61.46; d.f. = 4, 43; P < 0.001) and experiment repetition (F = 27.62; d.f. = 1, 43; P < 0.001); there were no interactions among any of these factors (P > 0.05). Capture was between 10.8- and 28.5-fold higher in traps than cages for the different lure types (fig. 1a). And capture was higher with the 3-μg lures than the 1-μg lures, which was higher than with the 0.3-μg lures and with the virgin females, which were higher than without lures (controls) (fig. 1a).

image

Figure 1. Mean (±SE) numbers of oriental beetle males captured in cages or traps lured with a virgin female or a red rubber septum loaded with different sex pheromone amounts (0.3, 1.0 or 3.0 μg) or neither (Control). (a): Turfgrass, 2009; (b): Blueberries, 2009; (c): Turfgrass, 2010; (d): Blueberries, 2010. Columns with the same letter are not significantly different by Tukey's test (P > 0.05). 3.0-μg lures were not used in 2010 NA, not available). n = 6–8 replicates per year per commodity.

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2010 experiment

In 2010, lures used were a virgin female and red rubber septa loaded with 0.3 or 1 μg pheromone. anova showed that oriental beetle male capture was significantly affected by trapping device (F = 475.99; d.f. = 1, 36; P < 0.001), lure (F = 174.54; d.f. = 3, 36; P < 0.001) and experiment repetition (F = 8.12; d.f. = 1, 36; P < 0.01); there were no interactions among any of these factors (P > 0.05). Capture was between 25.2- and 41.2-fold higher in traps than cages for the different lure types (fig. 1c). And capture was higher with the 1-μg lures than the 0.3-μg lures, which was higher than with the virgin females, which were higher than without lures (controls) (fig. 1c).

Female-mimic, low-dose pheromone lures – blueberries

2009 experiment

anova showed that oriental beetle male capture was significantly affected by lure (F = 37.78; d.f. = 4, 40; P < 0.001) and experiment repetition (F = 6.4; d.f. = 1, 40; P = 0.015); there were no effects of trapping device or interactions among trapping device, lure and experiment repetition (P > 0.05). Capture was higher with the 3-μg lures than the 1-μg lures, and both were higher than with the 0.3-μg lures, virgin females and controls (fig. 1b).

2010 experiment

anova showed that oriental beetle male capture was significantly affected by trapping device (F = 5.68; d.f. = 1, 32; P = 0.023) and lure (F = 28.56; d.f. = 3, 32; P < 0.001); there were no effects of experiment repetition or interactions among trapping device, lure and experiment repetition (P > 0.05). Capture was ~1.7-fold higher in traps than cages for the different lure types (fig. 1d). And capture was higher with the 1-μg lures and 0.3-μg lures than with the virgin females, which was higher than the controls (fig. 1d).

Range of attraction of female mimics

anova showed that recapture was significantly affected by pheromone source (F = 14.63; d.f. = 3, 57; P < 0.001), distance males released from trap (F = 21.29; d.f. = 4, 57; P < 0.001) and day of release (F = 9.39; d.f. = 3, 57; P < 0.001); there were no interactions between any of these factors. Recapture rates were higher for the 3.0-μg septa and 1.0-μg septa than for the 0.3-μg septa and the virgin females and declined logarithmically with distance for all pheromone sources (fig. 2). Recapture rate was higher for males released at 1.9, 3.81 and 7.63 m than for males released at 15.25 and 30.5 m. Regression lines were almost identical for virgin females and the 0.3-μg septa. Based on the equations (fig. 2), 0% recovery (<0.1%) for virgin female and 0.3-, 1- and 3-μg septa was predicted at 32.0, 23.1, 45.1 and 122.6 m, respectively.

image

Figure 2. Percentage recovery within 24 h of colour-marked oriental beetle males released at 1.9–30.5 m from a trap lured with a virgin female or a red rubber septum loaded with different sex pheromone amounts (0.3, 1.0 or 3.0 μg). In brackets are best fit equations and r-squared values. n = 4. Data are means ±SE.

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Capture of unmarked males from the background population was also significantly affected by pheromone source (F = 5.03; d.f. = 3, 9; P < 0.03) but not by repetition (capture day) (F = 1.24; d.f. = 3, 9; P = 0.35). Capture was higher for the 3-μg septum (mean ± SE = 69.5 ± 9.2) than the 0.3-μg septum (13.5 ± 5.9) (P ≤ 0.05), with the 1-μg septum (25.5 ± 14.0) and virgin females (18.0 ± 8.2) not significantly different from either (P > 0.05).

Long-term mating disruption

Trap shutdown

In all 3 years (2010–2012), male oriental beetle captures in traps were 87% lower (range = 77–92%) in fields treated with pheromone dispensers than in untreated control plots (significant treatment effect, Table 1A; fig. 3). There was also an effect of trap location (edge vs. interior) on number of beetles captured; however, this effect was influenced by treatment such that 3 times more males were captured in traps placed along field edges than in the interior of fields in the disrupted fields but not in the non-disrupted fields (significant treatment × location interaction, Table 1A; fig. 3). Percentage reduction in trap captures in disrupted fields compared with non-disrupted fields averaged across the 3 years was 92% for traps in the field interior and 82% for traps in the field exterior. Although not significant, the number of males tended to be higher on the edge than the interior also in the non-disrupted fields in both 2011 and 2012 but not in 2010 (fig. 3). The number of beetles captured in traps also varied by year; however, there was no effect of farm or any other interaction effects (Table 1A), indicating that the effect of mating disruption on oriental beetle populations was similar across multiple years.

Table 1. Analysis of variance (anova) results from field experiments (2010–2012) testing the effects of mating disruption (treatment), trap location (edge vs. interior), lure (female or 0.3 or 1.0 μg pheromone), year, farm (block) and interactions on male oriental beetle captures in pheromone traps
SourceFd.f.aP
  1. a

    numerator, denominator (error).

(A) Trap shutdown
Treatment137.281, 33<0.001
Location20.041, 33<0.001
Year6.652, 330.004
Farm (random)0.893, 330.458
Treatment × Location4.331, 330.045
Treatment × Year2.332, 330.113
Location × Year2.12, 330.139
Treatment × Location × Year0.182, 330.837
(B) Female-mimic lures
Treatment96.531, 69<0.001
Lure60.353, 69<0.001
Year9.722, 69<0.001
Farm (random)8.633, 69<0.001
Treatment × Lure15.073, 69<0.001
Treatment × Year0.422, 690.661
Lure × Year4.316, 690.001
Treatment × Lure × Year0.286, 690.945
image

Figure 3. Mean (±SE) numbers of oriental beetle males captured in traps baited with 300 μg of the sex pheromone. (a): 2010; (b): 2011; (c): 2012. Traps were placed in commercial blueberry fields treated with hand-applied pheromone ((Z)-7-tetradecen-2-one) dispensers at 50 dispensers per ha (total of 2.5 g a.i. per ha) (disrupted fields; n = 4). Control fields had no dispensers (non-disrupted fields; n = 4). Within each field, traps were placed along field borders (n = 5) and in field interiors (n = 3). Columns with the same letter are not significantly different by Tukey's test (P > 0.05).

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Female-mimic lures

Number of oriental beetle males captured in traps baited with females and 0.3- and 1.0-μg pheromone lures were 93% lower in the disrupted fields compared with the non-disrupted fields (significant treatment effect, Table 1B; fig.  Fig. 4 ). Lure type had a significant effect on number of males captured; however, the effect of lure was affected by treatment and year (Table 1B; fig.  Fig. 4 ). In 2010 and 2011, male captures in the non-disrupted fields were 93% higher with the 1-μg lures than virgin females and controls, while captures in the 0.3-μg lures were similar to virgin females but higher than the controls (fig.  Fig. 4 a,b). No differences in number of male captures were found among all lure types (female and female-mimic lures) in disrupted fields in 2010 and 2011 (fig.  Fig. 4 a,b). In 2012, male captures in the disrupted and non-disrupted fields were 97% higher with the 0.3- and 1-μg lures than virgin females and controls (fig.  Fig. 4 c). The number of beetles captured in traps also varied by year and farm, indicating temporal and spatial variation in oriental beetle populations; however, there were no treatment × year or treatment × lure × year interactions (Table 1B). Percentage reduction in trap captures in disrupted fields compared with non-disrupted fields averaged across the 3 years was 92% for virgin females, 94% for 0.3-μg lures and 93% for 1.0-μg lures.

image

Figure  Fig. 4 . Mean (±SE) numbers of oriental beetle males captured in traps baited with a virgin female or a red rubber septum loaded with different sex pheromone amounts (0.3 or 1.0 μg) or neither (Control). (a): 2010; (b): 2011; (c): 2012. Traps were placed in commercial blueberry fields treated with hand-applied pheromone ((Z)-7-tetradecen-2-one) dispensers at 50 dispensers per ha (total of 2.5 g a.i. per ha) (disrupted fields; n = 4). Control fields had no dispensers (non-disrupted fields; n = 4). Columns with the same letter are not significantly different by Tukey's test (P > 0.05).

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Larval infestation

The number of oriental beetle larvae per pot was affected in 2011 by the mating disruption treatment but not in 2012 (treatment × year interaction: F = 4.72; d.f. = 1,73; P = 0.033). In 2011, the number of larvae per pot was 85% lower in disrupted fields (mean ± SE = 0.2 ± 0.2) compared with control fields (1.0 ± 0.4) (F = 4.20; d.f. = 1,35; P = 0.048). In 2012, 0.3 ± 0.2 larvae were found per pot in disrupted fields and 0.8 ± 0.4 larvae per pot in control fields (F = 0.92; d.f. = 1, 35; P = 0.343). There was no effect of farm in both years (P > 0.05).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The results from our studies show that: (i) rubber septa baited with 0.3 μg of (Z)-7-tetradecen-2-one–the oriental beetle sex pheromone–can be used as a female mimic to evaluate mating disruption success of this insect pest; (ii) the range of attraction of this lure (i.e. estimated area where 99.9% of released males were attracted to the lure) is about 30 m; (iii) mating disruption can provide consistent long-term control of oriental beetle populations in blueberry fields; and (iv) mating disruption was more effective in the middle of fields than along the field edges.

This study tested and found for the first time a pheromone-dispensing device and dose that is similarly attractive to male oriental beetles as virgin females (i.e. a female mimic) and that could be used instead of virgin females by researchers and farmers to assess the efficacy of mating disruption for this insect. As indicated by Doye and Koch (2005), assessing the effectiveness of mating disruption can be challenging. In moths, mating disruption is typically assessed by measuring male captures in pheromone traps (trap shutdown), mating frequency of tethered virgin females and fruit injury at harvest (Cardé and Minks 1995). Because tethered females are openly exposed and thus easily consumed by predators, researchers often use cages or traps to enclose the females (Cardé et al. 1975; Schmidt and Seabrook 1979; Doye and Koch 2005; Stelinski et al. 2006; Briand et al. 2012). In oriental beetle, caged virgin females have previously been used to assess the success of mating disruption in both blueberries (Rodriguez-Saona et al. 2009, 2010) and turfgrass (Koppenhöfer et al. 2008). However, collecting and rearing oriental beetles to obtain virgin females is laborious. Our data indicate that the use of virgin oriental beetle females can be substituted with the use of 0.3-μg pheromone lures.

Our experiments could not clarify, however, whether cages or traps are more representative of the natural mate finding conditions. Although cages and traps provided similar results in blueberries, traps caught significantly higher numbers of males than cages in turfgrass. Cages might restrict mate finding to some extent due to the limited access to the female which may lead some males that find the caged female to give up before finding one of the cage openings. On the other hand, in turfgrass, traps might lead to greater than natural mate finding because the small cages containing the females are suspended near the top of the trap about 13 cm above the soil surface rather than in the grass where the females would naturally call. This should result in a less obstructed and easier to trace pheromone plume in the dense albeit low groundcover of a turfgrass area. In blueberries, the bottom of traps sat on top of, or just above, the soil–a practice commonly used to avoid predation by ants–which placed the lure at about 30 cm above the ground. Possibly this even higher placement in blueberries was detrimental to male capture thus reducing the advantage of freer access to the traps. Alternatively, in the blueberry fields which had very little ground cover (but rows of about 1.5 m high bushes), the higher placement of the lures had a smaller positive effect on male capture than in turfgrass. Direct observations might be needed to determine whether cages restrict male access to pheromone sources as compared with traps. Determining mating status after exposure of tethered but non-caged females might be the most natural (but also very labour-intensive) option; however, based on previous experiences (Koppenhöfer et al. 2005), such females cannot be left unprotected in the field because they can be predated by birds and ground predators.

In turfgrass, the range of attraction of the 0.3-μg pheromone lures was similar to that of virgin females, that is ≤30 m from the source. These results indicate that the lures need to be placed apart a certain distance depending on what level of recapture relative to the maximum possible recapture can be considered as significant interference. For example, the developed equation for the 0.3-μg lure predicted a maximum recovery of 11.7% at 0 m distance from the trap, with recovery declining to 1% (9% of maximum) at 11.71 m and 0.1% (0.9% of maximum) at 22.8 m. Hence, traps should probably be placed at least 20 m apart to minimize any interference among them. For comparison, the distance at which 0.1% of males were attracted was 44.2 m for 1.0 μg and 122.0 m for 3.0 μg (present study), and 210.7 m for 10 μg and 477.0 m for 30 μg (A.M. Koppenhöfer, unpublished data).

Rodriguez-Saona et al. (2010) also reported the range of attraction for oriental beetle females to be about 30 m in blueberries, suggesting that crop architecture might not affect how far the pheromone plume can travel. The lower recapture rates with virgin females and the 0.3-μg pheromone lures as compared with the 1- and 3-μg lures might be in part due to the fact that the former two treatments emit less pheromone. In the case of virgin females, it might also be because they call only for a few hours around dusk and their pheromone production declines with age (Facundo et al. 1994; Zhang et al. 1994). In contrast, red rubber septa loaded with 10, 100, 300 or 1000 μg provided a constant release over a 4-week period (Behle et al. 2008). Pheromone production may also have been affected by the unnatural female placement in cages.

Beyond replacing virgin females as an evaluation tool for mating disruption success, we also envisioned for the low-dose female mimic (0.3 μg lure) to replace the high dose (30–300 μg lure) used in previous studies (e.g. Koppenhöfer et al. 2005, 2008; Rodriguez-Saona et al. 2009, 2010). The assumption had been that a lower dose lure, similar to a virgin female, would be more sensitive by being less competitive with the actual pheromone dispensers which contain 50 mg of (Z)-7-tetradecen-2-one in blueberries. Thus, we had expected to observe greater reduction in male trap captures in disrupted fields with the lower dose lures than with the high-dose lures. However, percentage reduction in trap captures in disrupted fields compared with non-disrupted fields averaged across the 3 years was 92% (only using traps in the field interior; it was 82% for traps in the field exterior) for the 300-μg lures and 92% for virgin females, 94% for 0.3-μg lures and 93% for 1.0-μg lures. It may be that the high release rates from the 50-mg dispensers were so much greater that the difference between the 300-μg and the 0.3-μg lures was irrelevant. The comparison might have come to a different result in turfgrass using pelletized pheromone dispensers of smaller pheromone content (0.8–1.4 mg) but higher density (Koppenhöfer et al. 2008). Intuitively, a lure that attracts similar numbers of males from a similar distance as a virgin female should be a better indicator of how mate finding by males is affected by pheromone application. Considering that the distance at which 0.1% of males would be attracted is more than 20 times greater for a 30-μg lure (477 m) than 0.3-μg lure (22.8 m), it stands to argue that a 300-μg lure would be much more likely to be affected by edge effects as observed in this study and by interference with other traps.

In the present study, we also document for the first time the long-term effects of mating disruption on oriental beetle using commercially available hand-applied plastic dispensers deployed in entire blueberry fields. Although in the past four decades, mating disruption has proven effective for the control of several Lepidoptera pests, including pink bollworm (Pectinophora gossypiella (Saunders)), codling moth (Cydia pomonella (L.)), oriental fruit moth (Grapholita molesta (Busck)), obliquebanded leafroller (Choristoneura rosaceana (Harris)) and gypsy moth (Lymantria dispar L.) (Cardé 1990, 2007; Miller et al. 2006), only recently has it been explored for pest control in the Coleoptera. So far, mating disruption has been tested for seven species in the Coleoptera and shown to be effective for oriental beetle control in blueberries, turfgrass, cranberries and ornamental nurseries (Table 2). Two predictions were tested in our studies: first, that the efficacy of mating disruption changes in time; and second, that the efficacy of mating disruption is greater in the field interiors than along the field edges. An application rate of 50 dispensers per ha (2.5 g a.i. per ha) to blueberry fields provided 87% trap inhibition in all 3 years of this study. As opposed to our prediction, this level of trap inhibition did not vary significantly in time and was comparable to those reported in previous studies carried out in blueberries (90–95%; Polavarapu et al. 2002; Rodriguez-Saona et al. 2009), using smaller hectares under mating disruption, as well as in turfgrass (87–97%; Koppenhöfer et al. 2005, 2008) and cranberries (80–99%; Wenninger and Averill 2006), indicating that the efficacy of mating disruption for oriental beetle is not crop- or scale dependent. However, Rodriguez-Saona et al. (2010) showed that the density of dispensers has an effect on the efficacy of mating disruption in oriental beetle because under low-dose dispensers, the behavioural mechanism of disruption in this insect is via competitive attraction (Miller et al. 2006); thus, greater disruption is expected under higher number of dispensers. Here, we used a dispenser density shown to be effective and economically feasible (Rodriguez-Saona et al. 2009).

Table 2. Case studies of mating disruption in the Coleoptera
Species (Family)PheromoneCommodityType of dispenserReference
Cylas brunneus F. (Apionidae)Decyl- and dodecyl (E)-2-butenoateSweetpotatoPVC resin, controlled release formulationDownham et al. 2001
Cylas puncticollis Boheman (Apionidae)Decyl- and dodecyl (E)-2-butenoateSweetpotatoPVC resin, controlled release formulationDownham et al. 2001
Melanotus okinawensis Ohira (Elateridae)Dodecyl acetateSugarcanePolyethylene tubesArakaki et al. 2008
Megaplatypus mutatus (Chapuis) (Curculionidae)(+)-6-Methyl-5-hepten-2-ol, 6-methyl-5-hepten-2-one, 3-pentanolHazelnut and poplarGlass vials with polyethylene semipermeable cap/Polyethylene bagsFunes et al. 2011
Prionus californicus Motschulsky (Cerambycidae)(3R,5S)-3,5-dimethyl dodecanoic acidHopClear polyethylene sachetsMaki et al. 2011
Dasylepida ishigakiensis Niijima et Kinoshita (Scarabaeidae)(R)-2-butanolSugarcanePolyethylene tubesYasui et al. 2012
Anomala orientalis (Waterhouse) (Scarabaeidae)(Z)-7-tetradecen-2-oneBlueberriesMicroencapsulated sprayable formulation; Hand-applied plastic formulation; SPLAT-OrBPolavarapu et al. 2002; Sciarappa et al. 2005; Rodriguez-Saona et al. 2009, 2010;
  TurfgrassMicroencapsulated sprayable formulation; Wax-based granule formulationKoppenhöfer et al. 2005, 2008; Behle et al. 2008
  CranberriesRetrievable wax discsWenninger and Averill 2006
  Ornamental nurseriesMicroencapsulated sprayable formulationPolavarapu et al. 2002

Our data do support our second prediction that the efficacy of oriental beetle mating disruption varies within fields. Although oriental beetle male captures in pheromone-baited traps positioned at the perimeter and interior of blueberry fields were reduced in disrupted blueberry fields compared with non-disrupted fields, male captures in disrupted fields were threefold higher along the field edges than in the field interiors, and these findings were consistent over a 3-year period. These data indicate that to optimize field-wide oriental beetle mating disruption, higher dispenser density might be needed along field edges than in field interiors. Similarly, Knight (2007) reported reduced captures of male codling moth in sex pheromone traps located inside compared with those located at the border of apple orchards under mating disruption. Isaacs et al. (2012) reported greater levels of fruit infestation by the grape berry moth, Paralobesia viteana (Clemens), at the perimeter than in the interior of vineyards under pheromone mating disruption. These studies together with ours indicate movement of males from nearby areas into the pheromone-treated fields and suggest that the efficacy of mating disruption might be highest when deployed as an area-wide approach to account for possible pest migration (Calkins et al. 2000; McGhee et al. 2011; Tollerup et al. 2012).

The findings presented here have important implications for future implementation and assessment of mating disruption in oriental beetle. Area-wide application of dispensers for oriental beetle mating disruption may be the most effective approach to control this pest; however, its economic investment might be too high. Currently, blueberry growers treat individual fields with imidacloprid based on oriental beetle population levels in traps, and this same practice will likely be used with mating disruption. In addition, the labour costs associated with dispenser application will likely limit the area under oriental beetle mating disruption. The use of less labour-intensive methods of pheromone application such as wax matrices that can be mechanically applied is under investigation (Rodriguez-Saona et al. 2010). Moreover, we tested mating disruption for oriental beetle control in three consecutive years. Future studies need to compare the efficacy of continuous vs. interrupted applications of mating disruption. Finally, a remaining challenge is the assessment of crop injury. Measuring root injury by oriental beetle can only be carried out via crop destruction, which is not feasible in commercial blueberry farms. Instead, we have used sentinel plants baited with tethered females that often reflect the success of mating disruption (Rodriguez-Saona et al. 2009, 2010; this study). Alternatively, here, we provide a new easy-to-use and effective method, that is female mimics, to assess mating disruption for oriental beetle. The use of this more realistic low-rate trapping method would make the use of other methods such as caged virgin females or high-rate traps (trap shutdown), and ideally also sentinel plants, unnecessary.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank Dr. A.R. Prasad (Indian Institute of Chemical Technology, Hyderabad, India), and Eugene Fuzy, Dan Goldbacher, Dan Rice, and Jennifer Frake for technical assistance. Funding for this work was provided by the USDA Sustainable Agriculture Research and Education program (USDA SARE Grant No. 2008-38640-18866), the IR-4 Biopesticide and Organic Support Research program, and the US Golf Association.

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  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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