HORTICULTURAL ENTOMOLOGY
Effect of Bait Formulation and Number of Traps on Detection of Navel Orangeworm (Lepidoptera: Pyralidae) Oviposition Using Egg Traps BRADLEY S. HIGBEE1
AND
CHARLES S. BURKS2
J. Econ. Entomol. 104(1): 211Ð219 (2011); DOI: 10.1603/EC10162
ABSTRACT Egg traps are the primary tool for monitoring egg deposition of the navel orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae), and for timing treatments for this pest in almonds, Prunus amygdalus Batsch, and pistachios, Pistacia vera L. We compared, in almond and pistachio orchards, the number of eggs per trap in traps baited with almond meal, pistachio meal, or the current standard commercial bait. When considering cumulative eggs captured over an extended period, traps baited with pistachio meal prepared from previous-crop nuts generally captured a similar number of eggs compared with the commercial bait, and more eggs than those baited with almond meal prepared from previous-crop nuts. However, differences in eggs per trap between bait formulations were not as evident when examining individual weeks, particularly in weeks with few eggs per trap, as is typical when treatment decisions are made. The variance in eggs per trap was generally greater than the mean and increased with the mean and, when mean eggs per trap was low, most traps did not have eggs. We discuss implications of these Þndings for the relative importance of bait type and trap numbers for monitoring, and for experiments comparing egg trap performance. KEY WORDS Amyelois transitella, oviposition traps, monitoring, almonds, pistachios
The navel orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae), is a highly polyphagous scavenger species and an important economic pest of California crops, including almonds, Prunus amygdalus Batsch; pistachios, Pistacia vera L.; walnuts, Juglans regia L.; and Þgs, Ficus carica L. (Wade 1961, Burks and Brandl 2005, Bentley et al. 2009, Zalom et al. 2009). Control of navel orangeworm in almonds and pistachios, where it is the most important insect pest, emphasizes cultural controls such as timely harvest and orchard sanitation (Bentley et al. 2009, Zalom et al. 2009). When chemical control is necessary in almonds, egg trap data are used in conjunction with degree-day models to time insecticide applications targeting the overwintering generation (Þrst ßight, MarchÐMay) and/or the succeeding generation (second ßight, JuneÐJuly) (Zalom et al. 2009). In pistachios, these data and models are used to time treatment against the third ßight of moths in August (Bentley et al. 2009). Egg traps continue as the primary tool for monitoring navel orangeworm, despite recent advances in knowledge about the pheromone chemistry of this This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the USDA for its use. 1 Paramount Farming Company, 33141 E Lerdo Hwy., BakersÞeld, CA 93308. 2 Corresponding author: San Joaquin Valley Agricultural Sciences Center, USDAÐARS, 9611 S. Riverbend Ave., 644 Parlier, CA 93648 (e-mail:
[email protected]).
species (Leal et al. 2005, Kuenen et al. 2010). This is at least partially because producing a pheromone formulation that is attractive for more than one or two nights has proven difÞcult (Kuenen et al. 2008, Burks et al. 2009). Also, trapping eggs is logically more relevant than trapping males for timing treatments aimed at neonates. Egg traps for navel orangeworm were Þrst developed using clear plastic tubes and laboratory wheat bran diet (Rice 1976, Rice et al. 1976). Subsequent research showed that use of almond press cake, black color, rough surfaces, and addition of crude almond oil increased the number of eggs on traps (Rice et al. 1984, Van Steenwyk and Barnett 1985). More recently, the standard commercial almond formulation has changed, and recent work suggests that crude almond oil may not be as important (Kuenen et al. 2008). The authors of this latter study commented on a large standard error (Kuenen et al. 2008). This observation, along with previous data showing greater treatment difference during periods of higher ovipositional activity on egg traps (Van Steenwyk and Barnett 1985), suggest that the amount of time over which egg trap data are averaged and the time of year at which they are examined can affect Þndings concerning the relative effectiveness of one bait over another. A recent laboratory study suggested that, in a twochoice test, navel orangeworm females oviposit more on ground pistachios than on ground almonds (W. Leal, personal communication).
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Description of experiments examining the effect of the bait used on the number of eggs per trap Date Begin
End
18 June 2003 13 June 2003 26 Sept. 2003 4 Mar. 2004
3 Nov. 2003 16 Sept. 2003 3 Nov. 2003 2 Nov. 2004
Here, we examine whether using ground nuts from the previous-year harvest could either increase effectiveness of the egg traps, or achieve the same effectiveness at reduced cost. We also compared data over shorter intervals during key periods for pest management with results from experiments conducted over longer times to determine how the length of time and time of year of tests impacted the Þndings concerning the relative attractiveness of baits. A series of experiments in 2003 and a season-long experiment in 2004 compared the number of eggs on traps baited with different types of ground tree nuts and commercial navel orangeworm egg bait. We examined how averaging eggs per trap over entire experiments or key periods affected the variance-mean ratio, the number of empty traps, and the relationship between trap occupancy and egg abundance. These were of interest both because of their practical effects on analysis and detection of oviposition, and because of their relevance to inference about relative effectiveness of baits during periods with few eggs per trap using data collected during periods of high numbers of eggs per trap. We then compared differences in mean eggs per trap over the length of experiments (7Ð39 wk) and during key periods when egg traps are used to guide pest management decisions. Finally, nonparametric bootstrapping analysis (Davison and Hinkley 1997) was used to examine number of traps necessary for a 95% probability of detection of eggs during individual weeks of peak oviposition. Materials and Methods Traps, Baits, and Field Sites. We studied the effect of bait types on the number of eggs laid using the standard egg trap; i.e., a black plastic cylinder with a built-in bottom and a snap-on top. It is 8.6 cm in length by 1.6 cm in diameter, with ridges on the top and bottom and three mesh-covered holes, 1.1 cm in diameter, in the lower half of the tube. At the time of the study equivalent traps were sold by Tre´ ce´ (Adiar, OK) and Suterra (Bend, OR). The current commercial standard bait, almond meal sold by Liberty Vegetable Oil Company (Santa Fe Springs, CA) (Kuenen et al. 2008) (hereafter commercial bait), also was used. A series of four experiments compared the number of eggs per trap each week in traps placed in almond and pistachio orchards (Table 1). In the Þrst three experiments almond, pistachio, and walnut meal were ground from kernels from the previous-year harvest, by using a household blender that resulted in aggregates of ⱕ0.5 cm. In the fourth experiment ground
Bait
Crop
Almond, pistachio Almond, pistachio Almond, pistachio, walnut Almond, pistachio, commercial
Almond, pistachio Almond Almond, pistachio Almond, pistachio
almonds and pistachios, prepared in this manner, were compared with commercial almond meal, which is more Þnely ground. The traps were Þlled to a volume of 100 ml (i.e., to top of mesh), and the mean weight of 100 ml of the respective meals were 49.34 g for almond meal, 48 g for pistachio meal, 40.7 g for walnut meal, and 70.7 g for commercial bait. All experiments were conducted on orchards owned by Paramount Farming, LLC (BakersÞeld, CA), and located within 2.4 km of each other and 13 km south of Lost Hills, CA. Experiments. In the Þrst experiment, almond and pistachio meal were compared as bait in adjacent almond and pistachio orchards at two sites located 2.4 km apart. At both of these sites, traps were placed in trees to form grids comprising three rows of 10 traps each within each crop (i.e., 30 traps per crop per site) with rows 73 m apart, and traps 30 m apart with each row. The rows were perpendicular to the interface between the crops, with the Þrst row 22 m from this interface (rows were perpendicular in the two adjacent crops). At each position (tree) in these grids two egg traps, one Þlled with almond meal and the other with pistachio meal, were placed on opposite sides of a tree (i.e., ⬇4.6 m apart), 1.5 m from the ground. These egg traps were checked and meal was replaced weekly for 20 wk. A second concurrent experiment also compared eggs in egg traps baited with almond or pistachio meal in a third almond orchard. In this case, there was no adjacent pistachio orchard. This experiment was conducted for 13 wk. Traps containing almond and pistachio meal were placed on either side of trees, as in the previous experiment, with the position of the bait alternating between trees (east or west). Traps (10 each) were placed on trees at 32-m intervals in orchard rows 30, 66, and 103 m from the boundary of this orchard with a pistachio orchard (i.e., 30 traps). A third experiment was conducted in 2003 to compare the attractiveness of ground walnuts with that of ground almonds and ground pistachios. This experiment was conducted in another part of the adjacent almond and pistachio orchards comprising site two of experiment 1. A grid of 30 egg trap positions in each crop were set up as described for experiment 1. At each position, egg traps containing one of each of the three baits were placed at ⬇120⬚ intervals on a tree. This experiment was conducted for 7 wk. A fourth experiment comparing eggs and adults captured in traps baited with almond meal, pistachio meal, or commercial almond meal was conducted over the entire growing season in 2004 in the almond and pistachio orchards that comprised the second site used
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a) Almond orchard, 2003 75 Almond bait Pistachio bait
50
Eggs per trap
25 0 b) Almond orchard, 2004 75 50 25 0 3/1
5/1
7/1
9/1
11/1
Fig. 1. Weekly eggs per trap (mean and SE) on egg traps baited with almond or pistachio meal and placed in almond orchards. GLM analyses were performed over the length of the experiments, over a 6-wk period of key concern for pest management decisions (gray cross-hatched area), and on a single week of peak egg counts (arrow). (a) Experiment 1, from 18 June to 3 November 2003; n ⫽ 60. (b) Experiment 4, from 4 March to 2 December 2004; n ⫽ 20.
for experiment 1. A grid of traps was placed in trees in two columns 146 m apart, with 10 traps per column spaced 30 m apart, for 20 traps in total in each of the two crops. As in experiment 3, three bait formulations were tested at each position. This experiment was conducted for 39 wk in almonds. Due to labor demands and harvest activity, data were not collected in pistachios for 4 wk in September, thus 35 wk of trap data were obtained from pistachios in this experiment. Data Analysis. Data were initially examined by plotting the weekly means and errors for the two longer experiments, and by examination of the coefÞcient of variance and the percentage of traps with eggs for these experiments, both for all weekly observations and for eggs per trap per wk averaged over the length of the experiment. Based on these observations, we examined the varianceÐmean relationship (trap occupancy and abundance) before proceeding to further analysis. Trap Occupancy and Abundance. Based on the initial examination of the data, we wished to examine the relationship between the proportion of traps with eggs and the number of eggs per trap over the range of the data. Data from the two longer experiments, one and four (Table 1) were therefore Þt to TaylorÕs power law (s2 ⫽ Ax b⫺1)(Southwood 1978) by linear regression of log10(variance) on log10(mean) for weekly groupings of site ⫻ crop ⫻ bait (i.e., groups of 30 traps for experiment 1, n ⫽ 156, and groups of 20 for experiment 4, n ⫽ 184). Differences in regression parameters were compared between crop and bait type within the two experiments, and then between the two experiments, using analysis of covariance (ANCOVA) (Zar 1999). Based on the Þnding of no signiÞcant difference in slope or intercepts, common values of A and b were calculated for the two data sets. These parameters were used with the model of Wilson and Room (1983) to obtain predicted values of the proportion of traps with eggs as a function of mean eggs per trap.
Comparison of Mean Eggs Per Trap. The null hypothesis of equal numbers of eggs per trap between baits in the two crops was tested over the entire length of each experiment, and over key portions of the two longer experiments during which these traps are often used to guide management decisions. In both cases, individual traps were treated as experimental units, and the mean eggs per week over the period examined was used as a response variable. This approach avoided the inßation of degrees of freedom which would have resulted from using many repeated measurements as experiments units, and also avoided problems associated with trying to Þt means or ratios for periods with different dispersion to the same model. Effects of the baits were analyzed separately for the two crops. For whole-experiment analysis, experiment 1 was analyzed with a mixed-model analysis of variance (ANOVA) (SAS Institute 2008) with bait as the sole independent variable and the site as a random variable. Experiment 2 was analyzed with StudentÕs t-test, and experiments 3 and 4 were analyzed with one-way ANOVA. For experiments 1 and 4, this null hypothesis of equal numbers of eggs per trap between baits in the two crops also was tested for periods during which pest managers look for oviposition associated with ßight two in almonds (⬇15 June to ⬇20 July, 6 wk) (Fig. 1) or ßight three in pistachios (August, 4 wk) (Fig. 2). These were examined using generalized linear models (GLMs) with negative binomial distribution (Agresti 2007) after examination of residuals from ANOVAs with these data indicated that the assumption of random distribution of the residual error was violated (Sokal and Rohlf 1995). For both experiments, the response variable was eggs per trap per week. For experiment 1 bait and site were predictor variables and, for experiment 4, bait was the sole predictor. Bootstrap Analysis of Trap Sensitivity. We compared the number of traps necessary to reliably detect
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a) Pistachio orchard, 2003 20 Almond bait Pistachio bait
15 10
Eggs per trap
5 0 b) Pistachio orchard, 2004 150 100 50 15 10 5 0 3/1
5/1
7/1
9/1
11/1
Fig. 2. Weekly eggs per trap (mean and SE) on egg traps baited with almond or pistachio meal and placed pistachio orchards. GLM analyses were performed over the length of the experiments, over a 4-wk period of particular concern for pest management decisions (gray cross-hatched area), and on a single week of peak eggs counts (arrow). (a) Experiment 1, from 18 June to 3 November 2003; n ⫽ 60. (b) Experiment 4, from 4 March to 2 December 2004; n ⫽ 20.
oviposition activity during individual weeks in the key periods indicated previously (Figs. 1 and 2) by using nonparametric simulation with the basic bootstrap (Davison and Hinkley 1997). This procedure offered a distribution-free way of examining whether the number of traps needed to detect oviposition activity under the conditions in which these traps are used. Bootstrap analysis was performed with the boot package (Davison and Hinkley 1997) in R software (R Development Core Team 2009), by using percentiles to estimate values of the lower and upper 95th percent conÞdence. One thousand bootstrap replications were used, with the sample function was used in the boot package to examine the effect of the number of traps examined on the 95% conÞdence. Exploratory data analysis, regression, ANOVA, t-tests, and GLM were performed using SAS (SAS Institute, Cary, NC). Results Weekly plots of eggs on egg traps reveal three trends in both almonds and pistachios. First, there is large seasonal variation in the number of eggs per trap; second, the periods of concern for management decisions typically occur during periods of relatively few eggs per trap; and third, difference in eggs per trap between bait types is most evident during periods of high trap activity (Figs. 1 and 2). In these four experiments, variability was high, as indicated by large coefÞcients of variance, and 36 Ð 64% of the weekly trap counts were zero (Table 2). The large number of traps with zero observations was of interest for two reasons. First, data sets with large numbers of zero counts are not suitable for analysis by ANOVA, and complicate analysis by generalized linear models with other probability distributions (Reeve and Strom 2004). Second, having no eggs on most traps obviously complicates detection of ovipositional activity. The plot of proportion of traps with eggs against eggs per trap (Fig. 3) illustrates a potential complica-
tion with extrapolating relative bait performance from periods with many eggs per trap to periods with few eggs per trap. When there are many eggs per trap, almost all traps have eggs and differences between baits are due to differences in the number of eggs laid. When there are few eggs per trap, most traps do not have eggs and the presence or absence of eggs becomes more important than the number of eggs laid per trap. The values for A and b of TaylorÕs power law are 6.24 ⫾ 1.04 and 1.32 ⫾ 0.019, respectively (mean ⫾ SE, n ⫽ 341). Based on these parameters, the model of Wilson and Room (1983) Þt of the observed data well, with an r2 of 0.85 for both experiment 1 (Fig. 3a) and experiment 4 (Fig. 3b). Averaging eggs per trap per week over the length of the experiments greatly stabilized and reduced variance, and practically eliminated the problem with empty traps (Table 2). The resulting data were very suitable for analysis with ANOVA or StudentÕs t, as judged from LevineÕs test for homogeneity of variance and from residuals plots. Under these conditions, signiÞcant differences in eggs per trap per week were found between baits in each of the crops and in each experiment (Table 3). Generally traps with pistachio meal had more eggs than traps with almond meal, although that trend was neither signiÞcant nor evident on an experiment-wide basis for experiment 4. Traps Table 2. Effect of weekly averaging on variability and the number of empty traps Averaging None
Weekly
Exp
N
CoefÞcient of variance
% traps without eggs
1 2 3 4 1 2 3 4
4,773 773 417 4,433 240 60 60 120
209 169 141 232 65 52 79 51
55 45 36 44 0 0 2 0
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HIGBEE AND BURKS: NAVEL ORANGEWORM EGG TRAPS a) Experiment 1, 2003
Proportion traps with eggs
1.00 0.75 0.50
Almond Pistachio Commercial
0.25 0.00
b) Experiment 4, 2004 Proportion traps with eggs
1.00 0.75 0.50 0.25 0.00 0
10 20 30 40 Eggs per trap
50
Fig. 3. Weekly occupancy and abundance of egg traps in almond and pistachio orchards in experiments 1 and 4. The solid line indicates predicted proportions of traps with eggs as a function of mean eggs per trap, based on TaylorÕs power law parameters. (a) Experiment 1, from 18 June to 3 November 2003; n ⫽ 30; r2 ⫽ 0.85. (Commercial bait used in 2004 only). (b) Experiment 4, from 4 March to 2 December 2004; n ⫽ 20; r2 ⫽ 0.85. The horizontal scale contains all 2003 observations and 90% of the observations from 2004 (maximum, 204).
with walnut meal had signiÞcantly fewer eggs than traps with pistachio meal in both crops, and, in almond orchards, had numerically fewer eggs than traps with almond meal. Table 3. Comparison of whole-experiment averages (eggs per trap per wk, mean ⴞ SE) in almond and pistachio orchards Exp
Bait
1
Almond Pistachio F (df ⫽ 1, 117) P Almond Pistachio t (df ⫽ 58) P Almond Pistachio Walnut F (df ⫽ 2, 27) P Almond Pistachio Commercial F (df ⫽ 2, 57) P
2
3
4
Crop Almonds
Pistachios
5.1 ⫾ 0.33a 8.8 ⫾ 0.44b 68.83 ⬍0.0001 2.9 ⫾ 0.25a 6.5 ⫾ 0.35b 8.33 ⬍0.0001 11 ⫾ 1.7ab 16 ⫾ 2.0a 9 ⫾ 1.5b 4.99 0.0143 7.8 ⫾ 0.54a 10.7 ⫾ 0.35b 10.3 ⫾ 0.73b 8.69 0.0005
2.5 ⫾ 0.19A 4.3 ⫾ 0.10B 57.69 ⬍0.0001
2.0 ⫾ 0.48A 7.0 ⫾ 0.86B 2.8 ⫾ 0.58A 15.78 ⬍0.0001 23 ⫾ 0.9A 24 ⫾ 0.8A 29 ⫾ 0.9B 15.78 ⬍0.0001
Means in the same experiment and column followed by different lower- or uppercase letters are signiÞcantly different (P ⬍ 0.05; ANOVA).
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When eggs per trap per week were examined over only the period of greatest interest for management decisions (grayed boxes, Figs. 1 and 2), there were more empty traps despite averaging eggs per trap over 6 wk for almonds and 4 wk for pistachios (Table 4). This larger number of empty traps resulted in violation of the assumption of random distribution of the residual error when using ANOVA. These data were more suitable for a GLM with negative binomial distribution, as determined by the values of deviance and deviance divided by degrees of freedom (SAS Institute 2008). When examined this way, there were still signiÞcant differences in eggs per trap between the different bait in pistachios orchards in August, but not in almond orchards in June and July (Table 4). Results were similar for analysis of data from the individual weeks indicated by arrows in Figs. 1 and 2 by using GLM with negative binomial distribution (data not shown). There was an adequate Þt, and there were signiÞcant differences in the number of eggs per trap between baits, and means separations were the same as shown in Table 4. Bootstrap analysis further suggests that the bait used in egg traps analysis was of greater importance in pistachios than in almonds (Fig. 4). In both crops and with any bait, eight to 12 traps were generally necessary for zero to fall outside of the 95% conÞdence interval. The bootstrap estimates of the 95% conÞdence in almonds in 2004 suggest differences in variance of eggs per trap between the baits, but not difference in mean eggs per trap (Fig. 4a). In pistachios, in contrast, differences in the 95% were implicit with 20 traps, and evident with 40 Ð 60 traps. Discussion This study is, to our knowledge, the Þrst to characterize or consider the frequency distribution of eggs on egg traps, which have been a standard monitoring tool for navel orangeworm in almonds and pistachios in California for ⬎30 yr. Monitoring oviposition of this pest is of particular concern because it directly attacks the nut of two high value crops, almonds and pistachios, and because once the neonate larva gets inside the nut it generally avoids exposure to residual insecticides and will damage the nut. Timing of treatments is, therefore, very important for this pest. Effect of Time and Duration of Observation on Relative Performance of Baits. The data presented here show that, when considered over extended periods, more eggs were captured on egg traps baited with some of the baits examined compared with others. But further examination indicated that relative advantage of some baits over others was not as great when examined over a shorter period, or during periods of low eggs per trap typical of the time during which these traps are used. In almond orchards, for example, traps baited with pistachio meal captured signiÞcantly more eggs than traps baited with almond meal over the entire experiment for each of the three experiments that included the 6-wk period in June and July as depicted in Fig. 1 (i.e., experiments 1, 2, and 4;
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Table 4. Comparison of averages (eggs per traps per wk, mean ⴞ SE) during critical monitoring periods in almond orchards (15 June–20 July) and pistachio orchards (in August) Almond orchards Exp
Bait
1 (n ⫽ 60)
Almond Pistachio 2 P Almond Pistachio Commercial 2 P
4 (n ⫽ 20)
Eggs/trap 0.66 ⫾ 0.20 0.75 ⫾ 0.28 0.12 0.73 0.79 ⫾ 0.27 1.40 ⫾ 0.46 1.85 ⫾ 0.80 3.15 0.21
Pistachio orchards
% traps without eggs 60 36 40 45 25
Eggs/trap 1.1 ⫾ 0.20a 2.4 ⫾ 0.28b 16.2 ⬍0.0001 0.50 ⫾ 0.18a 1.61 ⫾ 0.32b 2.29 ⫾ 0.48b 15.98 0.0003
% traps without eggs 25 18 55 20 15
Means in the same experiment and column followed by different letters are signiÞcantly different (P ⬍ 0.05; GLM).
Fig. 4. Bootstrap estimates of lower and upper 95% conÞdence intervals of mean eggs per week by bait type during single weeks (see arrows in Figs. 1 and 2) as a function of the number of traps per bootstrap sample. Missing lower markers indicate that the lower limit of the 95% conÞdence interval was zero. (a) Almond orchard in July 2004 (experiment 4). (b) Pistachio orchard in August 2003 (experiment 1). (c) Pistachio orchard in August 2004 (experiment 4).
Table 3). However, when only this 6-wk period was considered, the difference in eggs per trap was not signiÞcant (Table 4). Bootstrap examination of eggs per trap in a single week revealed that, for the number of traps examined, the baits differed asymmetrically in the number of eggs per trap; i.e., the upper 95% conÞdence interval differed between baits, whereas the lower 95% conÞdence interval did not (Fig. 4). The comparison of frequency distributions between weekly and averaged trap data offers one reason for these different results. Averaging traps over the duration of the experiments reduced the variance, made the frequency distribution more symmetrical, and practically eliminated the occurrence of traps with zero eggs. Large numbers of zero counts are problematic because they can inßate P values, and because they are not corrected by variance-stabilizing transformations (Reeve and Strom 2004). Averaging eggs per trap over longer periods and/or over periods with higher numbers of eggs per trap corrects this problem, but creates a problem with inference. From a statistically signiÞcant difference, one can say that traps with one bait had signiÞcantly more eggs than those with another bait during part of the examination period, or on average over the whole examination period. It does not, however, follow that the number of eggs per trap differed during the shorter period when the trap are used to detect ovipositional activity of an emerging cohort. If other information is lacking then, it might be supposed that relative performance of one trap bait over time or during periods of high oviposition on egg traps is the best indication of performance during the critical monitoring periods when oviposition is low. Such extrapolation should be approached cautiously, however, as demonstrated here by using the model of Wilson and Room (1983) to examine the occupancyabundance relationship for egg traps (Fig. 3). The range of eggs per trap is much larger when most traps have eggs than when few do, indicating that differences between eggs per trap evident when oviposition is more abundant might be reduced or absent when oviposition is not abundant. This conclusion is consistent with the weekly plots (Figs. 1 and 2) and the bootstrap analyses of key individual weeks (Fig. 4).
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Effect of Number of Traps on Detection. The foregoing observations are not intended to argue that the bait used in egg traps is irrelevant, but rather that its importance must be balanced with when the traps are to be used, and how many are used to support a treatment decision. For example, for almond orchards one recommendation suggests “1 trap per 10 acres [4 ha] for at least four traps per orchard”, further stating that “orchards that exceed 1000 acres [405 ha] can be divided into larger sampling blocks if conditions within each block are uniform” (http://www.ipm. ucdavis.edu/PMG/C003/m003bceggtrapsnvl.html) (Zalom et al. 2009). In the southern and central San Joaquin Valley management blocks are often 32Ð 64 ha and generally monitored with ⱕ4 traps per management block. However, monitoring and treatment decisions are often made in consultation with pest control advisors, who often provide services for tens or hundreds of such blocks within a region. A pest control advisor monitoring a large number of blocks with two to four traps per block thus has adequate data to make judgments about regional phenology of navel orangeworm, but not about individual blocks. However, if it is important to detect changes in activity in a single block, then the bootstrap estimates of the number of traps needed to exclude zero from the 95% conÞdence interval indicate that it is necessary to use eight to 16 traps to monitor this single block. Relative Performance of Baits. We found that egg traps baited with pistachio meal generally captured similar numbers of eggs compared with the current standard commercial bait, whereas traps baited with almond meal captured fewer eggs, and those baited with walnuts still fewer. In pistachio orchards, more eggs were captured with commercial bait than with pistachio meal when examined over an entire Þeld season (experiment 4; Table 3), and pistachio meal did not capture signiÞcantly more eggs than almond meal. However, when examined in pistachio orchards during the critical monitoring period, pistachio meal captured signiÞcantly more eggs than almond meal and numerically (but not signiÞcantly) fewer eggs than commercial bait. It is noteworthy that there were fewer empty traps with commercial bait than with pistachio meal, because detection is important and the proportion of traps with eggs might be more important than eggs per trap. However, the greater sensitivity of the commercial bait compared with pistachio meal must be traded off against the greater expense of the former compared with the latter. If large numbers of traps are going to be used to determine periods of peak oviposition over an area, then pistachio meal obtained more economically as a by-product of local orchard sanitation or processing may be preferable to the more expensive commercial bait used in this study. The results here are broadly consistent with earlier studies, particularly the more recent study by Kuenen et al. (2008). Earlier studies brought the egg trap to its present form, Þrst replacing laboratory diet with almond press cake (the commercial diet of this study) (Rice et al. 1984), and then changing the color and form of the trap itself from smooth clear plastic to
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black plastic with roughened surfaces (Van Steenwyk and Barnett 1985). The latter study also found commercial bait with 10% crude almond oil more effective than the commercial bait by itself. A more recent study found no difference in eggs per traps between commercial bait by itself or with 3, 5, or 10% crude almond oil (Kuenen et al. 2008). That study also found no signiÞcant difference in eggs per trap between traps baited with almond meal, pistachio meal, or commercial bait with 10% crude almond oil. In that study, the experiments described here were conducted in pistachios and Þgs (Kuenen et al. 2008) during the spring period typiÞed by higher abundance in those crops (Burks and Brandl 2004; Fig. 2). The data presented here demonstrate that egg traps are poor indexes of population density compared with other trapping methods, and that the way they are affected by crop phenology differs between almonds and pistachios. The observation that ßuctuations in eggs per egg traps do not increase in later season (post hull split) to the same extent as pheromone or blacklight traps has already been noted in almonds (Rice 1976, Rice et al. 1984). In the current study, the Þnding of 10 to 30 times as many eggs in pistachio orchards in March and April compared with the rest of the year (Fig. 2) is in distinct contrast to data indicating a general upward trend in the number of males captured in pistachios between March and September (Burks et al. 2008, 2009). In almond orchards, reduced effectiveness of egg traps after hull split is presumably due to competition from almonds which became more attractive at this stage. In Kern County, hull split in almonds typically occurs in late June in the earliest varieties, whereas in pistachios shell split Þrst occurs in August. In pistachios, however, there are malformed pea splits that support navel orangeworm growth and occur as early as June, suggesting that competition from the developing current year crop also suppresses eggs on egg traps in pistachios. In almond orchards a single tree typically contains 5,000 Ð 8,000 current-crop almonds (USDAÐNASS 2010), whereas in pistachios a single tree contains 9,000 Ð 13,000 current-season nuts (USDAÐNASS 2003) with pistachio orchards typically planted with 1.67 times the tree density of almond orchards. The forgoing observations indicate the egg traps are unreliable as a relative index of population density for comparisons between crops or between different points in crop maturity. But that is not their function in monitoring; they instead show relative increases in population fertility and oviposition to target treatments against eggs or neonate larvae. What is important for this purpose is the interplay of abundance, population fertility, and the relative attraction of the egg trap compared with the surrounding crop. These observations underline the importance of testing egg trap bait formulations in the crop in which they are to be used for monitoring and at the time when monitoring data are most critical for that crop. It is somewhat perplexing that almond meal generally performed worse than pistachio meal, but the
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commercial bait, produced from almonds, performed as well or better. One possible reason is that the commercial bait has a qualitatively different volatile proÞle compared with almond meal. For example, the commercial bait is prepared from almonds rejected from food grade uses and therefore may be more likely to have been infested by navel orangeworm, which has previously been shown to increase eggs on traps by a factor of 5- to 10-fold (Andrews and Barnes 1982). However, it is possible that the difference is primarily because the denser, more Þnely-ground commercial product releases the same attractive volatiles more effectively. If the latter is the primary reason for the difference, then it may be possible to increase the attractiveness of pistachio meal by grinding it more Þnely. In conclusion, the data from this study indicate that pistachio meal can be a cost-effective alternative to the commercial bait examined, particularly if conclusions concerning treatment timing are based on ⬎20 traps (e.g., a number more typical of those examined in a region than in a single management block). The advantage of pistachio meal and commercial bait over almond meal is more apparent in pistachio orchards when monitoring for third ßight in August than in almond orchards when monitoring for second ßight in June and July. In almond orchards in June and July, pistachio meal and commercial bait captured numerically but not statistically more eggs than almond meal. In this situation, basing treatment timing decisions on an adequate number of traps is even more important. Finally, any future studies comparing navel orangeworm egg trap characteristics or formulations should include at least conÞrmatory tests that are speciÞc to a particular crop and conducted at the time during which monitoring is most relevant in this crop. Experiments conducted during periods when many traps do not have eggs should include sufÞcient replicates (e.g., ⱖ20), and should be analyzed by nonparametric methods or with models by using an appropriate probability distribution for the random component (Agresti 2007). Acknowledgments We acknowledge technical assistance by Lori Smith, Mike Bryant, Reuben Larrios, and Justin Green. We are grateful to two anonymous reviewers for suggestions that improved the manuscript.
References Cited Agresti, A. 2007. An introduction to categorical data analysis, 2nd ed. Wiley, Hoboken, NJ. Andrews, K. L., and M. M. Barnes. 1982. Differential attractiveness of infested and uninfested mummy almonds to navel orangeworm moths. Environ. Entomol. 11: 280 Ð282. Bentley, W. J., R. H. Beede, K. M. Daane, and D. R. Haviland. 2009. UC IPM pest management guidelines: pistachio. Publication 3461. University of California Agriculture and Natural Resources, Oakland, CA. (http://www.ipm. ucdavis.edu/PDF/PMG/pmgpistachio.pdf).
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Burks, C. S., and D. G. Brandl. 2004. Seasonal abundance of navel orangeworm (Lepidoptera: Pyralidae) in Þgs and effect of peripheral aerosol dispensers on sexual communication. J. Insect Sci. 4: 40. Burks, C. S., and D. G. Brandl. 2005. Quantitative assessment of insect pest damage to Þgs. Crop Manage. (doi: 10/1094/CM-2005-0510-01-RS). Burks, C. S., B. S. Higbee, D. G. Brandl, and B. E. Mackey. 2008. Sampling and pheromone trapping for comparison of abundance of Amyelois transitella in almonds and pistachios. Entomol. Exp. Appl. 129: 66 Ð76. Burks, C. S., B. S. Higbee, L.P.S. Kuenen, and D. G. Brandl. 2009. Monitoring Amyelois transitella males and females with phenyl propionate traps in almonds and pistachios. Entomol. Exp. Appl. 133: 283Ð291. Davison, A. C., and D. V. Hinkley. 1997. Bootstrap methods and their application. Cambridge University Press, Cambridge, United Kingdom. Kuenen, L.P.S., W. J. Bentley, H. C. Rowe, and B. Ribeiro. 2008. Bait formulations and longevity of navel orangeworm egg traps tested. Calif. Agric. 62: 36 Ð39. Kuenen, L.P.S., J. S. McElfresh, and J. G. Millar. 2010. IdentiÞcation of critical secondary components of the sex pheromone of the navel orangeworm (Lepidoptera: Pyralidae). J. Econ. Entomol. 103: 314 Ð330. Leal, W. S., A.-L. Parra-Pedrazzoli, K.-E. Kaissling, T. I. Morgan, F. G. Zalom, D. J. Pesak, E. A. Dundulis, C. S. Burks, and B. S. Higbee. 2005. Unusual pheromone chemistry in the navel orangeworm: novel sex attractants and a behavioral antagonist. Naturwissenschaften 92: 139 Ð146. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www. R-project.org). Reeve, J. D., and B. L. Strom. 2004. Statistical problems encountered in trapping studies of scolytids and associated insects. J. Chem. Ecol. 30: 1575Ð1590. Rice, R. E. 1976. A comparison of monitoring techniques for the navel orangeworm. J. Econ. Entomol. 69: 25Ð28. Rice, R. E., L. L. Sadler, M. L. Hoffman, and R. A. Jones. 1976. Egg traps for the navel orangeworm, Paramyelois transitella (Walker). Environ. Entomol. 5: 697Ð700. Rice, R. E., T. W. Johnson, J. C. Profita, and R. A. Jones. 1984. Improved attractant for navel orangeworm (Lepidoptera: Pyralidae) egg traps in almonds. J. Econ. Entomol. 77: 1352Ð1353. SAS Institute. 2008. SAS/STAT 9.2 userÕs guide. SAS Institute, Cary, NC. Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research, Freeman and Co., New York. Southwood, T.R.E. 1978. Ecological Methods with particular reference to the study of insect populations. Chapman & Hall, London, United Kingdom. [USDA–NASS] U.S. Department of Agriculture–National Agricultural Statistics Service. 2003. 2003 California pistachio objective measurement report. U.S. Department of Agriculture, National Agricultural Statistics Service, Washington, DC. [USDA–NASS] U.S. Department of Agriculture–National Agricultural Statistics Service. 2010. 2010 California almond objective measurement report. U.S. Department of Agriculture, National Agricultural Statistics Service, Washington, DC. Wade, W. H. 1961. Biology of the navel orangeworm, Paramyelois transitella (Walker), on almonds and walnuts in northern California. Hilgardia 31: 129 Ð171.
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Wilson, L. T., and P. M. Room. 1983. Clumping patterns of fruit and arthropods in cotton, with implications for binomial sampling. Environ. Entomol. 12: 50 Ð54. Van Steenwyk, R. K., and W. W. Barnett. 1985. Improvements of navel orangeworm (Lepidoptera: Pyralidae) egg traps. J. Econ. Entomol. 78: 282Ð286. Zalom, F. G., C. Pickel, W. J. Bentley, D. R. Haviland, R. A. Van Steenwyk, W. D. Gubler, J. E. Adaskaveg, R. Duncan,
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J. J. Stapleton, B. A. Holtz, et al. 2009. UC IPM pest management guidelines: almond. Publication 3431. University of California, Davis, Oakland, CA. (http:// www.ipm.ucdavis.edu/PDF/PMG/pmgalmond.pdf). Zar, J. H. 1999. Biostatistical analysis, 4th ed. Prentice Hall, Upper Saddle River, NJ. Received 4 May 2010; accepted 28 October 2010.
