Comparison of Attraction and Trapping Capabilities of Bucket- and Delta-Style Traps With Different Pheromone Emission Rates for Gypsy Moths (Lepidoptera: Erebidae): Implications for Understanding Range of Attraction and Utility in Surveillance

Comparison of Attraction and Trapping Capabilities of Bucket- and Delta-Style Traps With... Abstract Delta- and bucket-style (Universal or Unitrap) traps baited with 1 standard survey lure and 1/3 and 3 lures were compared for their attractiveness and trapping efficiencies for gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae), males. With bucket traps, the numbers of males attracted to within 2 m of traps and the proportion of these actually captured were identical among the three doses although the percentage of attracted males actually captured in bucket traps was low, less than 15%. A three-lure delta trap attracted about 70% more males than traps with the two lower doses. Capture efficiencies were above 80% for 1/3- and one-lure traps and about 60% for traps baited with three lures. The number of males captured in delta traps was equivalent for the three doses although our observations also suggest that a delta trap baited with three lures drew males from a wider range than lower dose lures and therefore would be a more sensitive trap for detecting incipient populations. We also noted that males tended to arrive in clusters, suggesting that attraction over moderate distances requires periods when the wind direction is fairly constant. This observation coupled with the great variability in the direction of male arrival to the traps also suggests that important changes in the area of influence of the plume are driven in such forested areas by slower but greater changes in wind direction compared with open habitats. The spread of gypsy moths, Lymantria dispar L. (Lepidoptera: Erebidae), in North America and the occasional incursion of its Asian form are monitored by a network of more than 200,000 pheromone-baited traps (Lance et al. 2016). Traps for detection in areas with a high potential for introduction are deployed at a density of 1 per 2.6 km2 (USDA 2010), which spaces traps 1,600 m apart. This distance well exceeds a male gypsy moth’s capability for tracking a pheromone plume to its source (Elkinton et al. 1987, Cardé 2016), and it has long been an issue of how likely is such a trapping density apt to miss an incipient population. One of the key factors that should affect the probability of ‘false negatives’, or the failure of a trap to detect a small population, is the efficiency of trap capture (Cardé 2001), which we define here as the probability of capture, given that a moth has oriented to within 2 m of a trap. In simulation modeling of gypsy moths locating pheromone-baited traps in a virtual world, Bau and Cardé (2016) used traps positioned in densities typically used for surveillance and also at higher densities used for delimitation following detection. In simulations, differences in trap efficiency substantially altered the probability of population detection (i.e., capture of at least one male). This study was designed to compare the trapping efficiency of the delta trap (used in surveillance) and a bucket-style trap, a common pheromone trap for other moths. We also evaluated the effect of lure emission rate by comparing numbers of males attracted and caught as well as their direction and temporal pattern of arrival using the standard surveillance lure and 1/3 and 3 lures, so that the emission rate spanned a 10-fold range. Higher emission rates should increase the downwind projection of a trap’s active space, thereby sampling a wider expanse and presumably increasing captures; however, higher rates of emission also may affect orientation near the trap, potentially either decreasing or increasing capture efficiency. Materials and methods Field Site The field performances of bucket- and delta-style traps were evaluated in Cadwell State Forest, Pelham, MA (lat/long: 42.36369°–72.43728°). This site consists of mature trees with a 20-m-high canopy of predominately northern red oak (Quercus rubra L [Fagales: Fagaceae]) mixed with other species, such as maples (Acer rubrum L [Sapindales: Sapindaceae] and Acer saccharum Marshall [Sapindales: Sapindaceae]) and eastern hemlock (Tsuga canadensis (L) Carriere [Pinales: Pinaceae]). Below a 3-m height, the forest is relatively open with little understory. Although there were males moving through the forest and throughout the canopy, they presumably originated from some distance away, as no females or pupae were seen on tree trunks anywhere in our test site. There also was no noticeable defoliation by gypsy moth at the site, but defoliating populations occurred nearby within 10 km (J.S.E., personal observations). Traps and Lures Traps were baited with a 1/3, 1, or 3 standard, 15-cm-long polyvinyl chloride ‘string’ survey lures. Based on extractions and gas-liquid chromatography (GLC) analyses, each standard lure contained 421.8 µg ± 16.9 SE (n = 8) of (7R,8S)-cis-7,8-epoxy-2-methyloctadecane, called disparlure. Purity by GLC was 97.4% with <0.3% of its (−)-enantiomer, determined by the method of Oliver and Waters (1995). Lures were aged outside in the shade in mesh bags for 1 wk prior to our study. Green delta traps (Pherocon IIIC, Trécé Inc., Salinas, CA) were constructed of cardboard and were 19.5-cm long with a triangular cross-section of 10 × 10 × 10 cm and a 3 × 3 × 3 cm triangular entrance at each end; two of the three internal sides were coated with a sticky surface to retain trapped moths. The lure was held in the same cages (see below) used in bucket traps and placed at the center of the trap floor. (In survey traps, the lure is typically stapled 2/3 of the way up the inside.) Traps were stapled to a small tree trunk 12–14 cm diameter at a height of 1.8 m and oriented in the same cardinal direction. Green bucket traps (Universal or Unitrap, Great Lakes IPM, Vestaburg, MI) allow moth entry from any direction via a 2-cm gap between the 15-cm diameter cover and a funnel leading to the bucket containing a Hercon Vaportape strip (10% Dichlorvos toxicant, Great Lakes IPM). To be captured, a moth needs to descend 10 cm down into the funnel and enter the bucket via a 3-cm diameter port. The lure was held in a plastic cage (4 cm high and 2 cm diameter) under the cover and above the funnel. One characteristic of this trap type is that it produces the same pheromone plume structure regardless of wind direction. Traps were placed at a height of 1.6 m on the branches of small saplings free of leaves and several meters away from any tree trunks; therefore, the generated pheromone plume was unaffected by the trap’s orientation to the wind flow and would have provided a relatively continuous pheromone plume to the trap over several meters. Trap Observations Delta traps with the three dose levels were deployed, spaced 40 m apart in a line 5 m from an unpaved lane. A bucket trap with one lure was placed 40 m from the two end positions, thereby to remove an ‘end effect’ whereby traps in the end position capture more males than interior traps (Elkinton and Cardé 1988). One individual observed each trap for 30 min. At the end of each 30-min observation interval, the observers were rotated one position, and the process was repeated. At the end of each 90-min cycle, the traps were rotated to a new position. We had an equal number of observations and observers for each lure dose in every trap position. In sum, we observed each trap for 18 intervals of 30 min for a total of 540 min per trap. Bucket traps also were placed in a line, 40 m apart and 20 m into the forest from the forest lane. There were three traps per dose level placed randomly in a complete block design. The nine traps were observed for 30-min intervals. Observers but not traps were rotated every 30 min, so that all observers observed each trap for 30 min, for a total of 270 min per trap. Observations for bucket traps were performed in 2017 on July 12 (0–180 min) and July 13 (180–270 min), and for delta traps on July 15 (0–270 min) and July 16 (270–540 min). The 40-m spacing between traps was chosen even though previous work (Elkinton and Cardé 1988) indicated that there was some interaction between traps at that distance; catch was suppressed by less than a factor of two with milk-carton traps. An 80-m spacing would have eliminated such inter-trap ‘poaching’, but it also might have meant that we were sampling different densities of males. For both trap types, the three observers were stationed approximately 2 m away. Moths could be seen during trap approach from 10 m or more. We characterized an oriented approach (locking-on to the plume, sensuKennedy et al. 1981) as a slowed, generally straight-line flight directed toward the trap, presumably navigation upwind along the pheromone plume. Almost always, locking-on culminated in contact with either a tree trunk/delta trap or a bucket trap. In the case of delta traps, moths landed on the tree trunk or trap, followed by walking while wing fanning until either trap entry or departure. The duration of this behavior was generally a minute or more; one moth performed this behavior for over 6 min. In the case of bucket traps, moths landed on the trap followed by walking while wing fanning. To ensure that we could clearly observe moths during orientation and be certain of either capture or departure, observers altered their vantage points as needed. The simultaneous monitoring of more than two moths was infrequent. In the case of delta traps, the maximum capacity of the sticky inner surface of the trap was ca. 30 moths, and therefore as our observations progressed, moths entering these traps were not permanently captured. Moths exiting delta traps when traps neared capacity usually flew rapidly away, typically upward into the canopy, rather than reorienting to the trap. Once a moth exited a trap, it was removed from the observation pool, but it was counted as captured, as would be the case for an empty trap. In surveillance, it is the capture of just one or perhaps a few moths that is of value in detecting an incipient population. We noted the time to the nearest minute that every male arrived at within 2 m of the trap in a locked-on flight and the direction of arrival with an accuracy of about 45°. We determined how closely in time arrivals were either clumped or dispersed throughout our 30-min observation intervals by binning these into 1-min intervals with a 3-min moving window. This time transect allows each arrival to be compared with the time of all arrivals occurring 3 min before and after. Statistics The numbers of males arriving and entering a trap were counted for every 30-min observation period and averaged for the different replicates (9 for bucket traps and 18 for delta traps). Trap efficiency was calculated as the percentage of those moths arriving at the traps that were captured. The ‘pgirmess’ R package (Giraudoux 2017) was used to perform multiple comparison Kruskal–Wallis tests across lure doses for arrivals and capture efficiencies. The same test was used to ensure that no significant differences were found among observers. Cumulative numbers of males arriving were calculated and plotted for each trap and lure type for the whole observation time. The short periods when observer or trap rotations took place were removed, and observation periods spliced into a continuous time line. The time transect of neighboring arrivals was computed with a sliding window of 3 min around every contact event. For each insect, the total number of males arriving was counted for the first, second, or third minute surrounding (i.e., preceding and following) its time of arrival. Simultaneous (minute zero) arrivals were assigned to the first neighboring minute, therefore counting together neighboring males arriving on min −1, 0, and 1. These results were compared with simulated datasets of equal number of males with randomly distributed times of arrival. In total, 100 matching random datasets were generated for every treatment, and averages and standard deviations were calculated after normality assessment with Shaphiro–Wilk test (P < 0.05). Observed neighboring arrivals were considered higher than expected when they exceeded the random average by more than twice the standard deviation. For delta trap observations, the direction of arrival with oriented flight was recorded for all males as they arrived within 2 m of a trap. The ‘circular’ R package (Agostinelli and Lund 2017) was used to calculate circular statistics. To determine the homogeneity of directional distribution of arrivals, a Rayleigh test was performed to every 30-min interval of data for all lure concentrations. Results No significant differences were found in the number of males attracted to bucket traps loaded with 1/3, 1, or 3 lures (Fig. 1). The numbers of males orienting to delta traps varied somewhat with dose, with the highest dose (three lures) attracting significantly more males than either 1 or 1/3 lure (Fig. 1). Trap efficiencies followed the opposite pattern, with capture proportions being highest at traps baited with 1/3 and a single lure (Fig. 2). These opposing forces resulted in equivalent delta trap captures for the three lure doses. Males often paused at the trap entrance without entering and resumed walking while wing fanning on either the trap or the tree trunk. Pausing at the trap entrance was especially noticeable with the 3X lure. With one exception, males did not fly directly into the trap entrance. Fig. 1. View largeDownload slide Average number of males that arrived at and was captured in the pheromone traps during 30-min periods of observation. The data were collected for 18 periods (540 min in total) with delta traps (upper panel) and 9 periods (270 min in total) with bucket traps (lower panel). Error bars indicate standard error of the mean. Different lowercase letters denote significant differences among lure loads (1/3×, 1×, or 3×) for a given observation category (arrival or caught) (Kruskal–Wallis test; P < 0.05). Fig. 1. View largeDownload slide Average number of males that arrived at and was captured in the pheromone traps during 30-min periods of observation. The data were collected for 18 periods (540 min in total) with delta traps (upper panel) and 9 periods (270 min in total) with bucket traps (lower panel). Error bars indicate standard error of the mean. Different lowercase letters denote significant differences among lure loads (1/3×, 1×, or 3×) for a given observation category (arrival or caught) (Kruskal–Wallis test; P < 0.05). Fig. 2. View largeDownload slide Trap efficiency as the average percent of attracted males that entered the delta or a bucket trap. Error bars indicate standard error of the mean. Different lowercase letters denote significant differences between lure loads for a given trap type (Kruskal–Wallis test; P < 0.05). Fig. 2. View largeDownload slide Trap efficiency as the average percent of attracted males that entered the delta or a bucket trap. Error bars indicate standard error of the mean. Different lowercase letters denote significant differences between lure loads for a given trap type (Kruskal–Wallis test; P < 0.05). As long as a delta trap contained relatively few previously trapped gypsy moth males, we observed no escape of entering males. In our observations, traps eventually reached capacity and we then observed males exiting the trap, usually departing rapidly upward into the canopy. From the viewpoint of surveillance, however, this means that our capture rates (trap entrance) are appropriate for understanding trap efficiency. Other studies with delta traps found that actual retention of male light brown apple moths (Epiphyas postvittana (Walker) Lepidoptera: Tortricidae) varied with trap length and lure position, evidently related to males not always adhering to the sticky surface (Foster et al. 1991, Foster and Muggleston 1993). With bucket traps, the disparity between orientation to within 2 m and actual capture was pronounced (Fig. 1), with similar numbers of males lured to within 2 m of traps and the number of males trapped, but a remarkably low trap capture efficiency, less than 20% for all three lure doses (Fig. 2). Males usually entered the bucket trap and often spent tens of seconds in contact with the cages containing lures without descending into the funnel below. Arrival rate depicted at a fairly coarse level was reasonably constant for all trap types and doses, except for the final part of 1/3 and 1x dose observations in delta traps (Fig. 3). Wind conditions, plume structure, population density, or all in the area are the most likely factors contributing to this arrival pattern. During the last day of observations of delta traps, the air was, in general, more still than on previous days, and a decrease in global captures in the area of study (data not shown) indicated male flight reached a peak a few days before the start of our study and declined steadily each day over 2–3 subsequent weeks. The design and position of delta traps also contribute to a less homogeneous plume structure compared with bucket traps. Fig. 3. View largeDownload slide Cumulative number of males that contacted the bucket (upper panel) or delta traps (lower panel) for the entire observation time series. Vertical dashed lines delimit experimental blocks of complete observer rotations in bucket traps and also the trap rotation for delta traps. Fig. 3. View largeDownload slide Cumulative number of males that contacted the bucket (upper panel) or delta traps (lower panel) for the entire observation time series. Vertical dashed lines delimit experimental blocks of complete observer rotations in bucket traps and also the trap rotation for delta traps. The pattern of arrival examined every minute shows that males tended to arrive in clusters, with an increased probability of neighboring arrivals, especially within 1–3 min of arrival of a male attracted to a trap (Fig. 4). Byers (1996) also reported clustered arrival-capture patterns over short time scales (1, 2, 4, 5, or 6 min) in two species of bark beetles. He attributed the nonrandom attraction patterns to fluctuating wind directions and speeds that would affect insect orientation in odor plumes. Wind conditions in forested areas produce changes in wind direction that are generally slower but of greater magnitude than those found in open field (Murlis et al. 2000). Grouped arrivals through time, therefore, can be probably linked to wind direction fluctuations that change the area of influence of the pheromone plume, reaching individuals at a different location, while short episodes of relatively stable wind direction can facilitate upwind progress, contributing as well to the observed effect of clustered male arrival and contact with the pheromone traps. The analysis of directional pattern of arrivals at delta traps showed that only 20% of the 30-min intervals had a unimodal distribution of directions (Rayleigh test, P < 0.05), and no consistent mean or modal direction of arrival was observed across simultaneously monitored traps. The insect arrival and, presumably, the wind direction often changed greatly during the 30-min observation periods, which is compatible with relatively frequent and substantial changes in the area of influence of the plume. Fig. 4. View largeDownload slide Cumulative neighboring arrivals around trap contacts for the different lure and trap type computed with a sliding window of 3 min. Lighter bars show the distribution of an equivalent number of contacts randomly distributed through time. Error bars show standard deviation (SD) for 100 datasets randomly generated for every treatment, and asterisks indicate values above twofold SD of random expectation. Fig. 4. View largeDownload slide Cumulative neighboring arrivals around trap contacts for the different lure and trap type computed with a sliding window of 3 min. Lighter bars show the distribution of an equivalent number of contacts randomly distributed through time. Error bars show standard deviation (SD) for 100 datasets randomly generated for every treatment, and asterisks indicate values above twofold SD of random expectation. Discussion Although pheromone-baited traps are widely used to monitor populations of many pest moths, relatively few studies have compared their attractive and trapping efficiencies. Designing a trap that captures a high number of attracted males per se, indicative of ‘sensitivity’, may not be of importance in many applications such as phenology or density estimation. In applications, however, in which the objective is surveillance of a pest’s presence, high attraction and trapping efficiency may be crucial to lowering the probability of false negatives of presence (Bau and Cardé 2016). Capture in a pheromone trap requires three successive behaviors: ranging flight to enable plume contact, navigation along the plume to its source, and landing/trap entry. Ranging strategies (flight direction prior to plume contact) in moths appear to be random with respect to contemporaneous wind flow (Elkinton and Cardé 1983, Cardé et al. 2012). Navigation upwind along a pheromone plume necessitates detection of wind direction, which is accomplished by using visual feedback to ensure an upwind heading. A front-to-rear image flow viewed below without any transverse flow signifies alignment of trajectory with wind flow. To enable landing, a second optomotor reaction is employed: allowing the object head to expand in the visual field (see reviews by Cardé and Willis 2008, Cardé 2016). Landing also may be linked with perception of changes in the plume’s concentration (Baker and Roelofs 1981), the presence of an appropriate landing site (Charlton et al. 1990), and perhaps changes its fine-scale structure (Justus et al. 2002). Cardé and Hagaman (1979) and Charlton et al. (1993) showed that gypsy moths in a wind tunnel slowed their rate of upwind flight as the concentration of pheromone was increased, both as the source was approached and by using differing doses on the pheromone dispenser. A flight speed reduction has been also observed in the field, where male gypsy moths reduced speed as they progressed from 10 to 2.5 m away from the source (Willis et al. 1991). In the present observations, moths lowered their flight speed markedly as they approached a trap or tree prior to landing. Therefore, lowered efficiency of trap capture at the highest dose tested could be the result of an increased concentration of pheromone or it could be caused by the increased concentration of the (−)-enantiomer of disparlure, an antagonist of attraction (Cardé et al. 1977, Miller et al. 1977, Cardé and Hagaman 1979), at the highest doses tested. Besides the ability to effectively retain the moths attracted to its vicinity, trap design and positioning also have a significant effect on plume structure and the moth’s behavioral response to it, displaying lower speeds and wider flight paths toward point-source plumes than toward wider, more diffuse plumes (Willis et al. 1994). A prescient study to examine trap capture efficiency was conducted by Lewis and Macaulay (1976) with the pea moth, Cydia nigricana (F; Lepidoptera: Tortricidae). They evaluated several trap designs that retained attracted moths using either a sticky surface or a water pan below the lure. A delta-style trap aligned with wind flow reportedly attracted about 40% more males than when it was aligned crosswind; however, this trap captured 21% of arriving males when aligned with the wind and 30% when aligned crosswind. Both orientations resulted in the same number of captured moths. An “omnidirectional” water trap that generated the same form of a coherent plume regardless of wind direction lured as many males to the trap vicinity as a delta trap aligned with wind flow, but the former’s capture efficiency was 49%. Elkinton and Childs (1983) compared trapping efficiencies of Pherocon IC traps (sticky “wing” traps) and USDA milk-carton traps (Schwalbe 1981) for gypsy moths, also following arrival within 2 m, and found that capture efficiencies of only 20 and 10%, respectively. These studies illustrate that relying simply on numbers that are captured as a guide to the value of a trap in surveillance is potentially misleading. A delta trap’s lower efficiency at the highest dose tested did not significantly alter number captured although males may have been sampled from a larger area. Bucket traps are efficient in luring males, likely because their plume structure would be well defined and elongated, regardless of wind direction. Capture efficiency, however, was remarkably low, and clearly these traps would not be useful for gypsy moth surveillance programs, although they are useful for heliothine moths (Gregg and Wilson 1991). Significance for Surveys and Modeling The finding that delta traps capture similar numbers of gypsy moth males at the three tested pheromone doses and that the capture efficiencies were fairly high indicates that the standard survey trap and standard lure are well suited for surveillance and delimitation, even if lure potency should drop off after deployment, and it clearly shows that changes in trap design can strongly affect the detection sensitivity. Therefore, any change in current standard practices would not be necessary nor advisable. What remains unclear, however, is the distance of attraction or sampling range of a trap. It was somewhat surprising that a 10-fold increase in pheromone dose did not significantly increase the number of overall captures. Although the highest dose attracted more males to delta traps, its capture efficiency decreased, suggesting a trade-off between long-range and close-range attraction. This effect could result in significant differences of false-negative probabilities when wind conditions and forest structure are very different, thus inducing changes in pheromone plume structure and reach. Here, computer modeling might help to shed some light into the possible extent of such differences. Elkinton et al. (1987) tracked released gypsy moth males that had just sensed a pheromone plume, demonstrating that successful source location (males were hand netted upon arrival at the pheromone source) diminished rapidly as distance to the source increased (45% at 20 m, 27% at 40 m, 17% at 80 m, and 8% at 120 m). The impediments to navigating along a plume to its source are fragmentation of the plume by turbulent forces that create pheromone-free gaps within the plume, and changes in wind direction or encounter with objects that misalign the instantaneous direction upwind with the plume’s long axis (David et al. 1982, Elkinton et al. 1987). Such misalignment would then lead an upwind flying moth out of the plume (Cardé 2016). Moths that have thereby “lost” contact with the plume engage in sideways casting (oscillations crosswind) that is presumed to increase the probability of re-contacting the plume (David et al. 1983, Kuenen and Cardé 1994). Modeling of different types of casting behavior indicates that orientation success is affected by the number of casting oscillations (Byers 1996) and also by the width and temporal pattern of the casting flight (Bau and Cardé 2015). The pattern of plume dispersal and reaction to plume loss explain the long transit times for moths orienting over long distances (e.g., a mean of 9 min for orientations from 120 m). As moths are presumed to periodically encounter segments of the plume aligned with wind flow, it is during these episodes of little variation in wind direction that moths can make sustained progress toward the plume’s source (Elkinton et al. 1987). The similar numbers of males attracted to within 2 m of lures spanning a decade range in dose with delta and bucket traps suggest that males are not navigating along the plume to traps over many tens of meters. Instead, we believe that the principal factor influencing male attraction to traps is their movement prior to plume contact. Gypsy moths orient randomly with respect to contemporaneous wind flow in evident absence of a pheromone plume (Elkinton and Cardé 1983). Simulation models show that the rapidity of such ranging flight, its daily periodicity, and especially the extent to which its trajectory is straightened out together will determine the probability of plume contact (Bau and Cardé 2015, Miller et al. 2015). These factors and longevity will also determine how far a gypsy moth strays from its natal position (Bau and Cardé 2016). Acknowledgments We are grateful to Allard Cossé for supplying the lures and delta traps and for information on lure composition. 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Principles, and applications to pest monitoring and management . Springer, Heidelberg, Germany. Google Scholar CrossRef Search ADS   Murlis J. Willis M. A. Cardé R. T.. 2000. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol . 25: 211– 222. Google Scholar CrossRef Search ADS   Oliver J. S., and Waters R. M.. 1995. Determining enantiomeric composition of disparlure. J. Chem. Ecol . 21: 199– 211. Google Scholar CrossRef Search ADS PubMed  Schwalbe C. P. 1981. Disparlure-baited traps for survey and detection, pp. 542– 548. In Doane C. C. McManus M. L. (eds.). USDA Technical Bulletin 1584 . (USDA) U.S. Department of Agriculture. 2010. Gypsy Moth Program Manual. https://www.aphis.usda.gov/import_export/plants/manuals/domestic/downloads/gypsy_moth.pdf Willis M. A. Murlis J., and Cardé R. T.. 1991. Pheromone-mediated upwind flight of male gypsy moths, Lymantria dispar L., in a forest. Physiol. Entomol . 16: 507– 521. Google Scholar CrossRef Search ADS   Willis M. A. David C. T. Murlis J., and Cardé R. T.. 1994. Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind flight of male gypsy moths (Lymantria dispar L.) in a forest. J. Insect Behav . 7: 385– 409. Google Scholar CrossRef Search ADS   © The Author(s) 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Comparison of Attraction and Trapping Capabilities of Bucket- and Delta-Style Traps With Different Pheromone Emission Rates for Gypsy Moths (Lepidoptera: Erebidae): Implications for Understanding Range of Attraction and Utility in Surveillance

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Abstract

Abstract Delta- and bucket-style (Universal or Unitrap) traps baited with 1 standard survey lure and 1/3 and 3 lures were compared for their attractiveness and trapping efficiencies for gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae), males. With bucket traps, the numbers of males attracted to within 2 m of traps and the proportion of these actually captured were identical among the three doses although the percentage of attracted males actually captured in bucket traps was low, less than 15%. A three-lure delta trap attracted about 70% more males than traps with the two lower doses. Capture efficiencies were above 80% for 1/3- and one-lure traps and about 60% for traps baited with three lures. The number of males captured in delta traps was equivalent for the three doses although our observations also suggest that a delta trap baited with three lures drew males from a wider range than lower dose lures and therefore would be a more sensitive trap for detecting incipient populations. We also noted that males tended to arrive in clusters, suggesting that attraction over moderate distances requires periods when the wind direction is fairly constant. This observation coupled with the great variability in the direction of male arrival to the traps also suggests that important changes in the area of influence of the plume are driven in such forested areas by slower but greater changes in wind direction compared with open habitats. The spread of gypsy moths, Lymantria dispar L. (Lepidoptera: Erebidae), in North America and the occasional incursion of its Asian form are monitored by a network of more than 200,000 pheromone-baited traps (Lance et al. 2016). Traps for detection in areas with a high potential for introduction are deployed at a density of 1 per 2.6 km2 (USDA 2010), which spaces traps 1,600 m apart. This distance well exceeds a male gypsy moth’s capability for tracking a pheromone plume to its source (Elkinton et al. 1987, Cardé 2016), and it has long been an issue of how likely is such a trapping density apt to miss an incipient population. One of the key factors that should affect the probability of ‘false negatives’, or the failure of a trap to detect a small population, is the efficiency of trap capture (Cardé 2001), which we define here as the probability of capture, given that a moth has oriented to within 2 m of a trap. In simulation modeling of gypsy moths locating pheromone-baited traps in a virtual world, Bau and Cardé (2016) used traps positioned in densities typically used for surveillance and also at higher densities used for delimitation following detection. In simulations, differences in trap efficiency substantially altered the probability of population detection (i.e., capture of at least one male). This study was designed to compare the trapping efficiency of the delta trap (used in surveillance) and a bucket-style trap, a common pheromone trap for other moths. We also evaluated the effect of lure emission rate by comparing numbers of males attracted and caught as well as their direction and temporal pattern of arrival using the standard surveillance lure and 1/3 and 3 lures, so that the emission rate spanned a 10-fold range. Higher emission rates should increase the downwind projection of a trap’s active space, thereby sampling a wider expanse and presumably increasing captures; however, higher rates of emission also may affect orientation near the trap, potentially either decreasing or increasing capture efficiency. Materials and methods Field Site The field performances of bucket- and delta-style traps were evaluated in Cadwell State Forest, Pelham, MA (lat/long: 42.36369°–72.43728°). This site consists of mature trees with a 20-m-high canopy of predominately northern red oak (Quercus rubra L [Fagales: Fagaceae]) mixed with other species, such as maples (Acer rubrum L [Sapindales: Sapindaceae] and Acer saccharum Marshall [Sapindales: Sapindaceae]) and eastern hemlock (Tsuga canadensis (L) Carriere [Pinales: Pinaceae]). Below a 3-m height, the forest is relatively open with little understory. Although there were males moving through the forest and throughout the canopy, they presumably originated from some distance away, as no females or pupae were seen on tree trunks anywhere in our test site. There also was no noticeable defoliation by gypsy moth at the site, but defoliating populations occurred nearby within 10 km (J.S.E., personal observations). Traps and Lures Traps were baited with a 1/3, 1, or 3 standard, 15-cm-long polyvinyl chloride ‘string’ survey lures. Based on extractions and gas-liquid chromatography (GLC) analyses, each standard lure contained 421.8 µg ± 16.9 SE (n = 8) of (7R,8S)-cis-7,8-epoxy-2-methyloctadecane, called disparlure. Purity by GLC was 97.4% with <0.3% of its (−)-enantiomer, determined by the method of Oliver and Waters (1995). Lures were aged outside in the shade in mesh bags for 1 wk prior to our study. Green delta traps (Pherocon IIIC, Trécé Inc., Salinas, CA) were constructed of cardboard and were 19.5-cm long with a triangular cross-section of 10 × 10 × 10 cm and a 3 × 3 × 3 cm triangular entrance at each end; two of the three internal sides were coated with a sticky surface to retain trapped moths. The lure was held in the same cages (see below) used in bucket traps and placed at the center of the trap floor. (In survey traps, the lure is typically stapled 2/3 of the way up the inside.) Traps were stapled to a small tree trunk 12–14 cm diameter at a height of 1.8 m and oriented in the same cardinal direction. Green bucket traps (Universal or Unitrap, Great Lakes IPM, Vestaburg, MI) allow moth entry from any direction via a 2-cm gap between the 15-cm diameter cover and a funnel leading to the bucket containing a Hercon Vaportape strip (10% Dichlorvos toxicant, Great Lakes IPM). To be captured, a moth needs to descend 10 cm down into the funnel and enter the bucket via a 3-cm diameter port. The lure was held in a plastic cage (4 cm high and 2 cm diameter) under the cover and above the funnel. One characteristic of this trap type is that it produces the same pheromone plume structure regardless of wind direction. Traps were placed at a height of 1.6 m on the branches of small saplings free of leaves and several meters away from any tree trunks; therefore, the generated pheromone plume was unaffected by the trap’s orientation to the wind flow and would have provided a relatively continuous pheromone plume to the trap over several meters. Trap Observations Delta traps with the three dose levels were deployed, spaced 40 m apart in a line 5 m from an unpaved lane. A bucket trap with one lure was placed 40 m from the two end positions, thereby to remove an ‘end effect’ whereby traps in the end position capture more males than interior traps (Elkinton and Cardé 1988). One individual observed each trap for 30 min. At the end of each 30-min observation interval, the observers were rotated one position, and the process was repeated. At the end of each 90-min cycle, the traps were rotated to a new position. We had an equal number of observations and observers for each lure dose in every trap position. In sum, we observed each trap for 18 intervals of 30 min for a total of 540 min per trap. Bucket traps also were placed in a line, 40 m apart and 20 m into the forest from the forest lane. There were three traps per dose level placed randomly in a complete block design. The nine traps were observed for 30-min intervals. Observers but not traps were rotated every 30 min, so that all observers observed each trap for 30 min, for a total of 270 min per trap. Observations for bucket traps were performed in 2017 on July 12 (0–180 min) and July 13 (180–270 min), and for delta traps on July 15 (0–270 min) and July 16 (270–540 min). The 40-m spacing between traps was chosen even though previous work (Elkinton and Cardé 1988) indicated that there was some interaction between traps at that distance; catch was suppressed by less than a factor of two with milk-carton traps. An 80-m spacing would have eliminated such inter-trap ‘poaching’, but it also might have meant that we were sampling different densities of males. For both trap types, the three observers were stationed approximately 2 m away. Moths could be seen during trap approach from 10 m or more. We characterized an oriented approach (locking-on to the plume, sensuKennedy et al. 1981) as a slowed, generally straight-line flight directed toward the trap, presumably navigation upwind along the pheromone plume. Almost always, locking-on culminated in contact with either a tree trunk/delta trap or a bucket trap. In the case of delta traps, moths landed on the tree trunk or trap, followed by walking while wing fanning until either trap entry or departure. The duration of this behavior was generally a minute or more; one moth performed this behavior for over 6 min. In the case of bucket traps, moths landed on the trap followed by walking while wing fanning. To ensure that we could clearly observe moths during orientation and be certain of either capture or departure, observers altered their vantage points as needed. The simultaneous monitoring of more than two moths was infrequent. In the case of delta traps, the maximum capacity of the sticky inner surface of the trap was ca. 30 moths, and therefore as our observations progressed, moths entering these traps were not permanently captured. Moths exiting delta traps when traps neared capacity usually flew rapidly away, typically upward into the canopy, rather than reorienting to the trap. Once a moth exited a trap, it was removed from the observation pool, but it was counted as captured, as would be the case for an empty trap. In surveillance, it is the capture of just one or perhaps a few moths that is of value in detecting an incipient population. We noted the time to the nearest minute that every male arrived at within 2 m of the trap in a locked-on flight and the direction of arrival with an accuracy of about 45°. We determined how closely in time arrivals were either clumped or dispersed throughout our 30-min observation intervals by binning these into 1-min intervals with a 3-min moving window. This time transect allows each arrival to be compared with the time of all arrivals occurring 3 min before and after. Statistics The numbers of males arriving and entering a trap were counted for every 30-min observation period and averaged for the different replicates (9 for bucket traps and 18 for delta traps). Trap efficiency was calculated as the percentage of those moths arriving at the traps that were captured. The ‘pgirmess’ R package (Giraudoux 2017) was used to perform multiple comparison Kruskal–Wallis tests across lure doses for arrivals and capture efficiencies. The same test was used to ensure that no significant differences were found among observers. Cumulative numbers of males arriving were calculated and plotted for each trap and lure type for the whole observation time. The short periods when observer or trap rotations took place were removed, and observation periods spliced into a continuous time line. The time transect of neighboring arrivals was computed with a sliding window of 3 min around every contact event. For each insect, the total number of males arriving was counted for the first, second, or third minute surrounding (i.e., preceding and following) its time of arrival. Simultaneous (minute zero) arrivals were assigned to the first neighboring minute, therefore counting together neighboring males arriving on min −1, 0, and 1. These results were compared with simulated datasets of equal number of males with randomly distributed times of arrival. In total, 100 matching random datasets were generated for every treatment, and averages and standard deviations were calculated after normality assessment with Shaphiro–Wilk test (P < 0.05). Observed neighboring arrivals were considered higher than expected when they exceeded the random average by more than twice the standard deviation. For delta trap observations, the direction of arrival with oriented flight was recorded for all males as they arrived within 2 m of a trap. The ‘circular’ R package (Agostinelli and Lund 2017) was used to calculate circular statistics. To determine the homogeneity of directional distribution of arrivals, a Rayleigh test was performed to every 30-min interval of data for all lure concentrations. Results No significant differences were found in the number of males attracted to bucket traps loaded with 1/3, 1, or 3 lures (Fig. 1). The numbers of males orienting to delta traps varied somewhat with dose, with the highest dose (three lures) attracting significantly more males than either 1 or 1/3 lure (Fig. 1). Trap efficiencies followed the opposite pattern, with capture proportions being highest at traps baited with 1/3 and a single lure (Fig. 2). These opposing forces resulted in equivalent delta trap captures for the three lure doses. Males often paused at the trap entrance without entering and resumed walking while wing fanning on either the trap or the tree trunk. Pausing at the trap entrance was especially noticeable with the 3X lure. With one exception, males did not fly directly into the trap entrance. Fig. 1. View largeDownload slide Average number of males that arrived at and was captured in the pheromone traps during 30-min periods of observation. The data were collected for 18 periods (540 min in total) with delta traps (upper panel) and 9 periods (270 min in total) with bucket traps (lower panel). Error bars indicate standard error of the mean. Different lowercase letters denote significant differences among lure loads (1/3×, 1×, or 3×) for a given observation category (arrival or caught) (Kruskal–Wallis test; P < 0.05). Fig. 1. View largeDownload slide Average number of males that arrived at and was captured in the pheromone traps during 30-min periods of observation. The data were collected for 18 periods (540 min in total) with delta traps (upper panel) and 9 periods (270 min in total) with bucket traps (lower panel). Error bars indicate standard error of the mean. Different lowercase letters denote significant differences among lure loads (1/3×, 1×, or 3×) for a given observation category (arrival or caught) (Kruskal–Wallis test; P < 0.05). Fig. 2. View largeDownload slide Trap efficiency as the average percent of attracted males that entered the delta or a bucket trap. Error bars indicate standard error of the mean. Different lowercase letters denote significant differences between lure loads for a given trap type (Kruskal–Wallis test; P < 0.05). Fig. 2. View largeDownload slide Trap efficiency as the average percent of attracted males that entered the delta or a bucket trap. Error bars indicate standard error of the mean. Different lowercase letters denote significant differences between lure loads for a given trap type (Kruskal–Wallis test; P < 0.05). As long as a delta trap contained relatively few previously trapped gypsy moth males, we observed no escape of entering males. In our observations, traps eventually reached capacity and we then observed males exiting the trap, usually departing rapidly upward into the canopy. From the viewpoint of surveillance, however, this means that our capture rates (trap entrance) are appropriate for understanding trap efficiency. Other studies with delta traps found that actual retention of male light brown apple moths (Epiphyas postvittana (Walker) Lepidoptera: Tortricidae) varied with trap length and lure position, evidently related to males not always adhering to the sticky surface (Foster et al. 1991, Foster and Muggleston 1993). With bucket traps, the disparity between orientation to within 2 m and actual capture was pronounced (Fig. 1), with similar numbers of males lured to within 2 m of traps and the number of males trapped, but a remarkably low trap capture efficiency, less than 20% for all three lure doses (Fig. 2). Males usually entered the bucket trap and often spent tens of seconds in contact with the cages containing lures without descending into the funnel below. Arrival rate depicted at a fairly coarse level was reasonably constant for all trap types and doses, except for the final part of 1/3 and 1x dose observations in delta traps (Fig. 3). Wind conditions, plume structure, population density, or all in the area are the most likely factors contributing to this arrival pattern. During the last day of observations of delta traps, the air was, in general, more still than on previous days, and a decrease in global captures in the area of study (data not shown) indicated male flight reached a peak a few days before the start of our study and declined steadily each day over 2–3 subsequent weeks. The design and position of delta traps also contribute to a less homogeneous plume structure compared with bucket traps. Fig. 3. View largeDownload slide Cumulative number of males that contacted the bucket (upper panel) or delta traps (lower panel) for the entire observation time series. Vertical dashed lines delimit experimental blocks of complete observer rotations in bucket traps and also the trap rotation for delta traps. Fig. 3. View largeDownload slide Cumulative number of males that contacted the bucket (upper panel) or delta traps (lower panel) for the entire observation time series. Vertical dashed lines delimit experimental blocks of complete observer rotations in bucket traps and also the trap rotation for delta traps. The pattern of arrival examined every minute shows that males tended to arrive in clusters, with an increased probability of neighboring arrivals, especially within 1–3 min of arrival of a male attracted to a trap (Fig. 4). Byers (1996) also reported clustered arrival-capture patterns over short time scales (1, 2, 4, 5, or 6 min) in two species of bark beetles. He attributed the nonrandom attraction patterns to fluctuating wind directions and speeds that would affect insect orientation in odor plumes. Wind conditions in forested areas produce changes in wind direction that are generally slower but of greater magnitude than those found in open field (Murlis et al. 2000). Grouped arrivals through time, therefore, can be probably linked to wind direction fluctuations that change the area of influence of the pheromone plume, reaching individuals at a different location, while short episodes of relatively stable wind direction can facilitate upwind progress, contributing as well to the observed effect of clustered male arrival and contact with the pheromone traps. The analysis of directional pattern of arrivals at delta traps showed that only 20% of the 30-min intervals had a unimodal distribution of directions (Rayleigh test, P < 0.05), and no consistent mean or modal direction of arrival was observed across simultaneously monitored traps. The insect arrival and, presumably, the wind direction often changed greatly during the 30-min observation periods, which is compatible with relatively frequent and substantial changes in the area of influence of the plume. Fig. 4. View largeDownload slide Cumulative neighboring arrivals around trap contacts for the different lure and trap type computed with a sliding window of 3 min. Lighter bars show the distribution of an equivalent number of contacts randomly distributed through time. Error bars show standard deviation (SD) for 100 datasets randomly generated for every treatment, and asterisks indicate values above twofold SD of random expectation. Fig. 4. View largeDownload slide Cumulative neighboring arrivals around trap contacts for the different lure and trap type computed with a sliding window of 3 min. Lighter bars show the distribution of an equivalent number of contacts randomly distributed through time. Error bars show standard deviation (SD) for 100 datasets randomly generated for every treatment, and asterisks indicate values above twofold SD of random expectation. Discussion Although pheromone-baited traps are widely used to monitor populations of many pest moths, relatively few studies have compared their attractive and trapping efficiencies. Designing a trap that captures a high number of attracted males per se, indicative of ‘sensitivity’, may not be of importance in many applications such as phenology or density estimation. In applications, however, in which the objective is surveillance of a pest’s presence, high attraction and trapping efficiency may be crucial to lowering the probability of false negatives of presence (Bau and Cardé 2016). Capture in a pheromone trap requires three successive behaviors: ranging flight to enable plume contact, navigation along the plume to its source, and landing/trap entry. Ranging strategies (flight direction prior to plume contact) in moths appear to be random with respect to contemporaneous wind flow (Elkinton and Cardé 1983, Cardé et al. 2012). Navigation upwind along a pheromone plume necessitates detection of wind direction, which is accomplished by using visual feedback to ensure an upwind heading. A front-to-rear image flow viewed below without any transverse flow signifies alignment of trajectory with wind flow. To enable landing, a second optomotor reaction is employed: allowing the object head to expand in the visual field (see reviews by Cardé and Willis 2008, Cardé 2016). Landing also may be linked with perception of changes in the plume’s concentration (Baker and Roelofs 1981), the presence of an appropriate landing site (Charlton et al. 1990), and perhaps changes its fine-scale structure (Justus et al. 2002). Cardé and Hagaman (1979) and Charlton et al. (1993) showed that gypsy moths in a wind tunnel slowed their rate of upwind flight as the concentration of pheromone was increased, both as the source was approached and by using differing doses on the pheromone dispenser. A flight speed reduction has been also observed in the field, where male gypsy moths reduced speed as they progressed from 10 to 2.5 m away from the source (Willis et al. 1991). In the present observations, moths lowered their flight speed markedly as they approached a trap or tree prior to landing. Therefore, lowered efficiency of trap capture at the highest dose tested could be the result of an increased concentration of pheromone or it could be caused by the increased concentration of the (−)-enantiomer of disparlure, an antagonist of attraction (Cardé et al. 1977, Miller et al. 1977, Cardé and Hagaman 1979), at the highest doses tested. Besides the ability to effectively retain the moths attracted to its vicinity, trap design and positioning also have a significant effect on plume structure and the moth’s behavioral response to it, displaying lower speeds and wider flight paths toward point-source plumes than toward wider, more diffuse plumes (Willis et al. 1994). A prescient study to examine trap capture efficiency was conducted by Lewis and Macaulay (1976) with the pea moth, Cydia nigricana (F; Lepidoptera: Tortricidae). They evaluated several trap designs that retained attracted moths using either a sticky surface or a water pan below the lure. A delta-style trap aligned with wind flow reportedly attracted about 40% more males than when it was aligned crosswind; however, this trap captured 21% of arriving males when aligned with the wind and 30% when aligned crosswind. Both orientations resulted in the same number of captured moths. An “omnidirectional” water trap that generated the same form of a coherent plume regardless of wind direction lured as many males to the trap vicinity as a delta trap aligned with wind flow, but the former’s capture efficiency was 49%. Elkinton and Childs (1983) compared trapping efficiencies of Pherocon IC traps (sticky “wing” traps) and USDA milk-carton traps (Schwalbe 1981) for gypsy moths, also following arrival within 2 m, and found that capture efficiencies of only 20 and 10%, respectively. These studies illustrate that relying simply on numbers that are captured as a guide to the value of a trap in surveillance is potentially misleading. A delta trap’s lower efficiency at the highest dose tested did not significantly alter number captured although males may have been sampled from a larger area. Bucket traps are efficient in luring males, likely because their plume structure would be well defined and elongated, regardless of wind direction. Capture efficiency, however, was remarkably low, and clearly these traps would not be useful for gypsy moth surveillance programs, although they are useful for heliothine moths (Gregg and Wilson 1991). Significance for Surveys and Modeling The finding that delta traps capture similar numbers of gypsy moth males at the three tested pheromone doses and that the capture efficiencies were fairly high indicates that the standard survey trap and standard lure are well suited for surveillance and delimitation, even if lure potency should drop off after deployment, and it clearly shows that changes in trap design can strongly affect the detection sensitivity. Therefore, any change in current standard practices would not be necessary nor advisable. What remains unclear, however, is the distance of attraction or sampling range of a trap. It was somewhat surprising that a 10-fold increase in pheromone dose did not significantly increase the number of overall captures. Although the highest dose attracted more males to delta traps, its capture efficiency decreased, suggesting a trade-off between long-range and close-range attraction. This effect could result in significant differences of false-negative probabilities when wind conditions and forest structure are very different, thus inducing changes in pheromone plume structure and reach. Here, computer modeling might help to shed some light into the possible extent of such differences. Elkinton et al. (1987) tracked released gypsy moth males that had just sensed a pheromone plume, demonstrating that successful source location (males were hand netted upon arrival at the pheromone source) diminished rapidly as distance to the source increased (45% at 20 m, 27% at 40 m, 17% at 80 m, and 8% at 120 m). The impediments to navigating along a plume to its source are fragmentation of the plume by turbulent forces that create pheromone-free gaps within the plume, and changes in wind direction or encounter with objects that misalign the instantaneous direction upwind with the plume’s long axis (David et al. 1982, Elkinton et al. 1987). Such misalignment would then lead an upwind flying moth out of the plume (Cardé 2016). Moths that have thereby “lost” contact with the plume engage in sideways casting (oscillations crosswind) that is presumed to increase the probability of re-contacting the plume (David et al. 1983, Kuenen and Cardé 1994). Modeling of different types of casting behavior indicates that orientation success is affected by the number of casting oscillations (Byers 1996) and also by the width and temporal pattern of the casting flight (Bau and Cardé 2015). The pattern of plume dispersal and reaction to plume loss explain the long transit times for moths orienting over long distances (e.g., a mean of 9 min for orientations from 120 m). As moths are presumed to periodically encounter segments of the plume aligned with wind flow, it is during these episodes of little variation in wind direction that moths can make sustained progress toward the plume’s source (Elkinton et al. 1987). The similar numbers of males attracted to within 2 m of lures spanning a decade range in dose with delta and bucket traps suggest that males are not navigating along the plume to traps over many tens of meters. Instead, we believe that the principal factor influencing male attraction to traps is their movement prior to plume contact. Gypsy moths orient randomly with respect to contemporaneous wind flow in evident absence of a pheromone plume (Elkinton and Cardé 1983). Simulation models show that the rapidity of such ranging flight, its daily periodicity, and especially the extent to which its trajectory is straightened out together will determine the probability of plume contact (Bau and Cardé 2015, Miller et al. 2015). These factors and longevity will also determine how far a gypsy moth strays from its natal position (Bau and Cardé 2016). Acknowledgments We are grateful to Allard Cossé for supplying the lures and delta traps and for information on lure composition. Cameron Smith-Freedman and Alexyss Langevin provided assistance in the field observations. We thank Dave Lance, Vic Mastro, and two anonymous reviewers for valuable comments. JB was partially supported by the Research Intensification Program (2017DIR003) from the University of Vic – Central University of Catalonia. References Cited Agostinelli C., and Lund U.. 2017. R package “circular”: Circular Statistics (version 0.4–93). https://r-forge.r-project.org/projects/circular/ Baker T. C., and Roelofs W. L.. 1981. Initiation and termination of oriental fruit moth male response to pheromone concentrations in the field. Environ. Entomol . 10: 211– 218. Google Scholar CrossRef Search ADS   Bau J., and Cardé R. T.. 2015. Modeling optimal strategies for finding a resource-linked, windborne odor plume: theories, robotics, and biomimetic lessons from flying insects. Integr. Comp. Biol . 55: 461– 477. Google Scholar CrossRef Search ADS PubMed  Bau J., and Cardé R. T.. 2016. 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Environmental EntomologyOxford University Press

Published: Feb 1, 2018

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