Improving the Efficiency of Lepidopteran Pest Detection and Surveillance: Constraints and Opportunities for Multiple-Species Trapping

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Improving the Efﬁciency of Lepidopteran Pest Detection and Surveillance: Constraints and Opportunities for Multiple-Species Trapping

Article in Journal of Chemical Ecology · May 2013 DOI: 10.1007/s10886-012-0223-6 · Source: PubMed

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J Chem Ecol (2013) 39:50–58 DOI 10.1007/s10886-012-0223-6

Improving the Efficiency of Lepidopteran Pest Detection and Surveillance: Constraints and Opportunities for Multiple-Species Trapping

Eckehard G. Brockerhoff & D. Maxwell Suckling & Alain Roques & Hervé Jactel & Manuela Branco & Andrew M. Twidle & Victor C. Mastro & Mark O. Kimberley

Received: 27 April 2012 /Revised: 8 November 2012 /Accepted: 6 December 2012 /Published online: 20 December 2012 # Springer Science+Business Media New York 2012

Abstract Surveillance using attractants for invasive species repellency among lures for gypsy moth, Lymantria dispar, can allow early detection of new incursions and provide fall webworm, Hyphantria cunea, pine processionary moth, decision support to response programs. Simultaneous trap- Thaumetopoea pityocampa, and pine shoot moth, ping for multiple species, by baiting traps with several lures, Rhyacionia buoliana. To assess what factors may be impor- is expected to increase the number of species that can be tant in species compatibility/suitability for multiple-species targeted in surveillance programs and improve the cost- trapping, we combined our results with those of previous effectiveness without affecting surveillance coverage. We studies conducted by the United States Department of tested this hypothesis by choosing four potential forest and Agriculture. For 75 combinations of pheromones, tested urban lepidopteran pest species that are present in Europe singly or in combination, 19 % showed no effect on trap but not yet in New Zealand and many other countries. We catch for any of the species tested. In the other cases, either deployed traps in central and southern Europe with single one or both species showed a reduction in trap catch. lures or all possible species combinations (up to four lures However, few lure combinations caused complete or nearly per trap). There was only limited interference, apparently complete suppression. For most combinations, catches were due to trap saturation, but no evidence for interspecific still sufficiently high for detection purposes. Species from

Electronic supplementary material The online version of this article (doi:10.1007/s10886-012-0223-6) contains supplementary material, which is available to authorized users. E. G. Brockerhoff (*) M. Branco Scion (New Zealand Forest Research Institute), PO Box 29237, Centro de Estudos Florestais (Forest Research Center), Instituto Christchurch 8540, New Zealand Superior Agronomia, Technical University of Lisbon, 1349-017, e-mail: [email protected] Lisbon, Portugal

D. M. Suckling : A. M. Twidle The New Zealand Institute for Plant & Food Research Ltd, PB 4704, Christchurch, New Zealand V. C. Mastro A. Roques USDA APHIS PPQ CPHST, Otis Laboratory, Buzzards Bay, MA INRA UR0633 Zoologie Forestière, 02542, USA 2163 Avenue de la pomme de pin, 45075, Orléans, France

H. Jactel Laboratory of Forest Entomology & Biodiversity, UMR M. O. Kimberley BIOGECO – INRA, 69, route d’Arcachon, Scion (New Zealand Forest Research Institute), PB3020, Rotorua, 33612, CESTAS cedex, France New Zealand Author's personal copy

J Chem Ecol (2013) 39:50–58 51 the same superfamily exhibited more interference than more Forest Service, 2012). This system has, in many cases, distantly related species. Together, these results suggest that enabled the detection of gypsy moth populations in the year there are opportunities to improve the range of exotic pests of introduction. This early detection system has enabled under surveillance, at little additional cost, by multiple-species treatment of small areas that are not significantly disruptive trapping for which compatibility has been demonstrated. to homeowners or commerce. Eastern, infested states main- tain a strong regulatory program to minimize the artificial Keywords Biological invasions . Pheromones . movement of gypsy moth on items such as nursery stock. Repellency . Lepidoptera . Lymantria dispar . Hyphantria Detection of the introductionoftheAsianformsofthe cunea . Thaumetopoea pityocampa . Rhyacionia buoliana gypsy moth and closely related species (Lymantria dispar japonica, L.d. asiatica, Lymantria umbrosa, Lymantria albescens, Lymantria postalba) (Pogue and Schaefer, Introduction 2007) is also conducted at all high risk sea ports. This has led to the detection and eradication of 19 Asian gypsy moth Insect invasions, facilitated by international trade and move- introductions (J. Spaulding, AGM, APHIS program data). ment of goods and people, are a major threat to forest Detection trapping for gypsy moth is also undertaken in ecosystems. In the United States alone, approximately 2.5 other countries; e.g., Canada (Régnière et al., 2009)and new forest insect species, on average, are detected per year New Zealand (Brockerhoff et al., 2010). Such detection (Aukema et al., 2010), some of which may cause substantial trapping programs can contribute significantly to the early economic and environmental damage (Pimentel et al., 2005; detection of incipient populations, which greatly enhances Aukema et al., 2011). Given the huge amount of interna- the probability of successful eradication or containment tional and inter-continental trade in today’s globalized (Bogich et al., 2008; Brockerhoff et al., 2010). world, the prevention of biological invasions is a challenge. Pheromones are the basis of attractive lures, and can Early detection of new invaders, before significant popula- greatly enhance the effectiveness of traps. Most pheromones tion growth and spread has occurred, can aid substantially in are highly species-specific (El-Sayed, 2012), allowing se- preventing permanent establishment (e.g., Bogich et al., lective targeting and reducing unwanted catch of other 2008; Brockerhoff et al., 2010). Attractant-baited traps are organisms. Typically, traps are baited with lures for a single used widely for detection and population monitoring of species. Thus, the labor cost of operating traps is a limiting exotic and native pest insects in a wide range of ecosystems factor. Although numerous exotic pest species are consid- (e.g., Howse et al., 1998; Tobin et al., 2009; Witzgall et al., ered significant biosecurity threats, surveillance programs 2010). However, the immense diversity of potential pest for a wide range of target species would require a very large insects precludes comprehensive surveillance for all candi- number of traps and prohibitively large financial and staff dates. For example, there are about 150,000 described spe- resources. Simultaneous surveillance for multiple unwanted cies of Lepidoptera, which use an intriguing variety of sex organisms by a single trap would reduce costs and allow pheromone systems that typically are highly species-specific enhanced surveillance activity. There have been previous (Ando et al., 2004). For many taxa, species-specific or attempts at developing multiple-species trapping for detec- general attractants are available (e.g., El-Sayed, 2012). tion (Schwalbe and Mastro, 1988) or population monitoring Despite the large number of potential target species, of existing pests (Johansson et al., 2002; Jones et al., 2009). surveillance trapping programs using synthetic attractants These studies have shown that combining lures may not have been implemented in forest and urban ecosystems for always be possible. Some pheromone combinations are the detection of invasive wood borers and bark beetles (e.g., incompatible because certain pheromones inhibit the attrac- Brockerhoff et al., 2006; Wylie et al., 2008; Rabaglia et al., tion to others. This may be expected to occur especially with 2008). Pheromone trapping at high-risk sites or in trap grids closely related species (Ando et al., 2004). Consequently, is used for several key lepidopteran pests. Over 90,000 traps trapping with lures for multiple species can have varying in a grid system are used annually in the United States to effects. For example, when the pheromones of two species monitor populations of gypsy moth, Lymantria dispar of Cydia (C. pomonella and C. ulicetana) were presented (Lymantriinae), along the front of the invading population together, C. pomonella catch was inhibited, whereas C. in a “slow-the-spread” program (Sharov et al., 1998, 2002). ulicetana catch was not (Stephens et al., 2008). The under- In addition, over 200,000 traps are placed annually through- lying mechanisms that might cause pheromone lure incom- out uninfested portions of the United States to detect pop- patibility are not well understood. To determine whether ulations of gypsy moth artificially transported by human lure combinations for a range of key forestry lepidopteran activities. Since 1973, over 220 isolated populations have pests are compatible, we examined trapping by using pher- been detected in 26 states and these have been eradicated omone lures presented together, as well as singly. We also successfully by using a variety of tactics (United States compiled a data set combining our study with results of Author's personal copy

52 J Chem Ecol (2013) 39:50–58 previous studies conducted by the United States Department 500 μg (+) disparlure [(7R,8S)-cis-7,8-epoxy-2-methylocta- of Agriculture (USDA), to assess factors that may be im- decane] impregnated onto a film. Hyphantria cunea lures portant in affecting species compatibility and suitability for (‘H’) were obtained from Nitto Denko Corporation (Osaka, multiple-species trapping. Japan), with each containing at least 5.4 mg of (9Z,12Z,15Z)-octadecatrienal, (3Z,6Z)-(9S,10R)-cis-9,10- epoxyheneicosadiene, and (9Z,12Z)-octadecadienal impreg- Methods and Materials nated onto a film, in an approximate ratio of 12.3:1.1:1.2 (El-Sayed et al., 2005). Rhyacionia buoliana lures (‘R’) Multiple-Species Trapping for Forest Pests: Target were prepared by Plant & Food Research, and consisted of Species We designed a trapping study relevant for New 100 μgof97%(9E)-dodecen-1-yl acetate with 3 % (9E)- Zealand, which has been operating a national surveillance dodecen-1-ol (both from Pherobank, Wageningen, The program for gypsy moth since 1994, and has experienced Netherlands) on a rubber septum. Rhyacionia duplana lures several interceptions and incursions of Hokkaido gypsy (‘D’) were prepared by Plant and Food Research, and con- moth, L. umbrosa, and other lymantriines and forest pests sisted of 100 μgof(9E)-dodecen-1-yl (sourced from (Armstrong and Ball, 2005; Brockerhoff et al., 2010). Lures Pherobank) on a rubber septum. Lures for T. pityocampa for four major forest pest species present in Europe, which (‘T’) were prepared by INRA Versailles, and consisted of pose biosecurity risks to forests in other parts of the world, 2 mg of pityolure [a mixture of (13Z)-hexadecen-11-yn-1-ol were tested in traps baited with one, two, three, or four lures. and (13E)-hexadecen-11-yn-1-ol in a 97:2 ratio, provided by Unbaited traps were used as controls. The main target spe- SEDQ, Barcelona, Spain] on a rubber septum. cies were gypsy moth, L. dispar, fall webworm, Hyphantria cunea (Arctiidae), pine processionary moth, Thaumetopoea Data Analysis Poisson regression analysis was used to test pityocampa (Notodontidae), and pine shoot moth. the effects of lure type on insect catch (counts). The depen- Rhyacionia buoliana (Tortricidae). dent variable was the total count summed over all inspection periods for each trap. Separate models were fitted for each Study Sites and Traps Used Trapping took place in mixed species. Experimental factors included in these models were forests, where several of the target species were likely to co- replicate (or location), and presence/absence for the four occur (e.g., in a mixed forest of Pinus pinaster and Quercus main lures tested (H, T, R, L) fitted as a four-way factorial. suber in Portugal). In Europe, trapping with the same combi- The basic forms of these models were: nation of lures was carried out at two locations near Orléans, X 4 France (Orléans I, 47°50′16″N, 1°54′12″E, elevation 114 m; ln μ ¼ r þ l t ; ij i k¼1 kij k and Orléans II, 47°50′3″N, 1°54′51″E; elevation 112 m; 30 June to 1 September 2006), two locations near Cestas, France where ln() is the natural log operator, μij is the expected count (44°44′54″N, 00°46′34″W and 44°44′41″N, 00°47′08″W, el- in replication i for treatment j, ri is an effect representing the evation 59 m; 6 July to 17 August 2006) and two locations in ith replication, lkij are dummy variables with values of one, if Portugal (Herdade de Rio Frio, Rio Frio, Pinhal Novo, 38°40′ the treatment includes lure k, and zero otherwise, and tk is an 38″N, 8°51′49″W, elevation 16 m, and Mata das Virtudes, effect representing the kth lure. The models were fitted using Azambuja, 39° 5′21″N, 8°49′42″W, elevation 25 m; 14 July to the SAS Version 9 procedure GENMOD, with estimated 8 September 2006). A total of 96 traps were used. These were variances multiplied by the mean deviance to account for checked and their positions rotated (to avoid position effects) overdispersion. These models also were extended to include every 1–2 wk. In a follow-up trial, we tested the compatibility first-order interactions among lures. Also, to test whether the of lures for pine shoot moth, R. buoliana, and summer shoot negative impact of some lures was due to reduction in attrac- moth, Rhyacionia duplana, at six sites near Orléans (47°49′ tion or trap saturation, a covariate consisting of the log count 53, 1°54′18, elevation 112 m), with three traps per site, from 9 of non-target insects was added to the models. July to 2 September 2007, and one site near Bordeaux (44°44′ The relative strength of lures (either positive or negative) 26″N, 00°44′26″W, elevation 59 m), from 6 April to 17 July was obtained for each species from the model estimates 2008). Sticky traps were used in France (Orléans and using rk0exp(tk). These provided estimates of the ratio of Pierroton, described in Jactel et al., 2006), and green plastic the expected count in the presence of lure k to the expected funnel traps in Portugal (BIOSANI, Palmela, Portugal). Traps count in its absence. A value for rk much greater than 1 were placed at a height of approximately 1.5 m, and all traps indicates that the lure is a powerful attractant for the target were emptied after checking. species, while a value much lower than 1 indicates that it has a strong negative effect. Lures Lymantria dispar lures (‘L’) were obtained from An alternative analysis of the presence/absence of Pherotech (British Columbia, CA), with each consisting of each species was performed using logistic regression Author's personal copy

J Chem Ecol (2013) 39:50–58 53 models, fitted using GENMOD. At each site, traps were Table 1 T statistics and associated P-values obtained from Poisson inspected four or five times during the trial every 1– regression models, testing the significance of association between counts and lure type for each of the species of Lepidoptera 3 wk. The dependent variable used in the logistic regression models was the number of inspections in which Lure Thaumetopoea Lymantria dispar Rhyacionia at least one individual was trapped out of the total pityocampa buoliana number of inspections for that trap. t-value P-value t-value P-value t-value P-value For all analyses, we excluded locations where no, or too few, individuals of a species were caught. This meant that, H −1.45 0.152 0.28 0.781 −1.78 0.086 for R. buoliana, only data from Orléans were used, whereas R −1.05 0.295 −0.17 0.856 9.08 <0.001 for T. pityocampa and L. dispar, data from all three locations L −0.36 0.723 23.63 <0.001 −1.84 0.078 were used. T 34.74 <0.001 −5.28 <0.001 −4.91 <0.001

Review and Synthesis of Lure Combinations Pheromone H lure for Hyphantria cunea, R lure for R. buoliana, L lure for L. dispar, T 0 lure for T. pityocampa traps with a range of pheromone combinations were placed in locations in Australia, France, India, Ivory Coast, South Africa, and the USA (Mastro et al., Results 1984, 1985) by the USDA Animal and Plant Health Inspection Service (APHIS) and collaborators, so as to Multiple-Species Trapping for Forest Pests In 2006, 2852 T. identify possible lure combinations without antagonisms pityocampa, 2452 L. dispar, and 373 R. buoliana were (Schwalbe and Mastro, 1988). Our results were added to caught, which was sufficient to assess trapping interactions those in Mastro et al. (1984, 1985), and the combined among these species. We expected to trap some H. cunea, data set (see Supplementary Table 1a for a list of which were thought to be present in the parts of France species and their pheromones) analyzed for the frequen- where traps were set, but none was caught. However, we cy of inhibition of catch in 2-way combinations of still were able to evaluate the presence of H. cunea lures on lures. Although the combined data set included 27 spe- catches of the other species. The effects of the different lure cies of Lepidoptera, not all possible combinations could types on catches of each species in terms of counts are be tested. The trapping experiments analyzed here in- shown in Fig. 1, and the results of the corresponding cluded 75 out of the 351 possible two-way combina- Poisson regression analyses are in Table 1. Counts of T. tions (i.e., pairs of species). Cases were excluded from pityocampa were strongly positively related to lure T, while the analysis in which the outcome of combining lures the other three lures had no influence on catch of this could only be ascertained for one of the two species species. Counts of L. dispar were strongly positively related within a pair, unless a significant reduction in trap catch was to lure L, but negatively related to lure T (note, we also observed in one species, indicating an incompatible pair. caught 7 nun moths, Lymantria monacha, all in traps con- Therefore, our analysis was conservative, as some potentially taining lure L in combination with one or several of the suitable combinations could not be considered (until compat- other lures). Counts of R. buoliana were positively related to ibility has been demonstrated for both species). After trans- lure R and negatively related to lure T, with some indication formation to [log(n+1)], mean catches to lure combinations of a negative response to the other two lures. Interactions were compared with those to single-species lures by ANOVA between lure types were not significant and are not shown. and post-hoc tests. USDA experiments were carried out in a The follow-up trial, testing the combination of lures for R. randomized complete block design, typically with five repli- buoliana (‘R’) and R. duplana (‘D’), revealed that catches of cates, and sometimes with more (for details see Mastro et al., R. buoliana were not affected by the presence of the D lure. 1984, 1985,andSchwalbeandMastro,1988). Mean catches of R. buoliana to R, R+D, and D lures, Contingency tables were used to determine the effects respectively, were 4.7 (±2.3), 5.7 (±2.9), and 1.0 (±0.8). of taxonomic relatedness (superfamily, family, see The lack of catches of R. duplana may be explained, per- Supplementary Table 1b) on lure compatibility. We hy- haps, by the lure not being especially attractive, trapping pothesized that species that are more closely related taking place outside the flight season, or R. duplana not would be less compatible for combining lures in the being present at the site. same trap because of evolution for species isolation To determine the relative strength of these effects, we (Ando et al., 2004). A similar test was carried out to expressed the results in terms of the ratio of counts in the determine the effects of overlapping ranges (i.e., shared presence and absence of each lure (Fig. 2). For T. pity- natural geographic distribution, see Supplementary ocampa, lure T increased the count 190 fold, but the ratio Table 1b), which we hypothesized would also reduce was close to one for other lures, indicating they had no the probability of lure compatibility. effect on this species. For L. dispar, lure L increased the Author's personal copy

54 J Chem Ecol (2013) 39:50–58

A the negative effect of lure T on L. dispar and R. buoliana counts could be due to the large numbers of trapped T. pityocampa swamping the trap, or there could be a negative interaction that would have occurred even if T. pityocampa were absent at the site. To test whether the negative impact of some lures was due to reduction in attraction or trap saturation, we incorporated the log of the count of non- B target insects trapped for each species as a covariate in the regression model. When this covariate was included in the model, the negative effect of lure T on L. dispar was eliminated (t0−1.02; P00.31), but the negative effect of lure T on R. buoliana remained (t0−4.08; P<0.001); the effects of Mean catch per day per Mean catch lures H (t0−2.28, P00.031) and L (t0−2.38, P00.025) also were significant. This indicates that, for L. dispar, the effects C of lure L are not negated by the presence of lure T. However, for R. buoliana, the attraction of lure R appears to be reduced by the presence of lure T and possibly lures H and L. For L. dispar, there was no noticeable effect of trap type, because catch ratios in the presence and absence of lure T did not differ between sticky traps and funnel traps. As R. buoliana was not trapped in Portugal, effects of trap type could not be evaluated for this species. Fig. 1 Number of individuals of Lymantria dispar (L, panel A), To test if multiple lures were suitable for the purpose of Thaumetopoea pityocampa (T, panel B), and Rhyacionia buoliana (R, panel C) caught [mean and standard error of log(catch per trap detecting the presence/absence of a species (versus analyz- day + 1)] to different lures and combinations of lures of the four target ing actual counts of moths caught, which would be more species (i.e., L, T, R and H, Hyphantria cunea); N06 relevant if the objective were population monitoring), we conducted logistic regression analyses (Table 2). These count 16 fold, but lure T reduced it by 35 %. For R. analyses showed that each lure had significant effects only buoliana, lure R increased the count 35 fold, but when lure on its target species, with almost invariably at least one T was present, the count was reduced by 28 %. individual trapped of the target species, regardless of the The reductions in trap catch in the presence of lures for presence of additional lures. Differences in counts of species other species could have been caused by two main mecha- caught to other lures had little impact on whether the target nisms: actual reduction in attraction, caused by lures of species was present or not. This confirms that using multiple other species (i.e., chemical or physiological interference), lures for these particular species does not affect the useful- or trap saturation, caused by swamping of the trap collec- ness of the method for detection trapping, although it may tion mechanism by catches of other species. For example, not be suitable for population monitoring.

1000 Review and Synthesis of Lure Combinations We reviewed

Tha_pit Lym_dis Rhy_buo the effects of combining lures for 27 potentially invasive species. Given that not all species were present at the study 100 sites, not all the possible combinations (pairs of species) could be tested. Of the 75 species pairs for which informa- 10 tion was available for both species, there were 14 cases in which combining lures did not cause a reduction in trap

Catch rate ratio catch in either species (Table 3). In 61 cases, catches of 1 either one or both species were reduced when both lures were present. However, among the cases in which a reduc- 0.1 HRLTtion occurred, there were many that did not cause a func- Lure tional reduction, in the sense that catches were still sufficient to enable detection of a species (Table 3). Hereafter, we refer Fig. 2 Ratio of counts of Lymantria dispar (L), Thaumetopoea pity- to ‘functional reduction’ when catches in multiple-lure traps ocampa (T) and Rhyacionia buoliana (R) caught in the presence and absence of lures for each species (i. e., L, T, R, and H 0 Hyphantria are less than 33 % of the catch when only the lure of a target cunea). Error bars show 95 % confidence intervals species is present. For eight of 61 species pairs in which a Author's personal copy

J Chem Ecol (2013) 39:50–58 55

Table 2 χ2 statistics and associated P-values obtained from logistic regression models, testing the significance of association between presence/ absence of each of the species of Lepidoptera and lure type

Lure Thaumetopoea pityocampa Lymantria dispar Rhyacionia buoliana

χ2 value P-value χ2 value P-value χ2 value P-value

H 0.20 0.65 0.06 0.80 0.00 1.0 R 0.20 0.65 0.06 0.80 17.13 <0.001 L 0.20 0.65 125.1 <0.001 0.00 1.0 T 257.7 <0.001 2.98 0.084 0.00 1.0

H lure for Hyphantria cunea, R lure for R. buoliana,LL. dispar, T lure for T. pityocampa reduction occurred, catch still exceeded 33 % of control for many of these, we expect the reverse combination also to catch. There were just four cases in which the presence of be compatible. another lure prevented catch entirely, although in nine other If one considers all species pairs as compatible for cases cases catch was reduced to less than 5 % of that of the in which combining lures did not cause a reduction in catch, controls. In addition to 75 species pairs for which we or for cases in which a reduction occurred but catch was still obtained results for both species, there were 44 one-way greater than 33 % of the control catch, then 22 out of 75 comparisons in which no catch reduction occurred (Table 3); (29 %) combinations were compatible. Some species

Table 3 Overview of two-way interactions between pheromone lures of control catch are indicated with an asterisk (or in brackets) and light of 27 moth species, showing trap catch of target species to combined grey highlighting; those with significant reductions to ≤33 % are lures as percentages of ‘control’ catch to lures for the target species indicated with a double asterisk (or ‘X’) and dark grey highlighting; only (i.e., those in the first row). Two-way combinations with no cells with neither indicate cases in which only one-way comparisons significant reduction compared with controls are shown in cells with are available (see text for further details) bold cell margins; combinations with significant reductions to >33 % Species A ora T leu C fun C pom E ins E pos H arm H pun L bot L dis P gos P scu R buo S exe S lito S litu T pit Summerfruit tortrix Adoxophyes orana A ora - X 56 3** 1** 5** 14** 3** Red-banded leafroller Argyrotaenia velutinana A vel 0** 70 1** 12** False codling moth Thaumatotibia leucotreta T leu 27** - 5** 3** 27 93 42* 106 3** 46 64* 134 X 97 93 Plum fruit moth Cydia funebrana C fun 27** X - 28 134 3** 121 97 85 Codling moth Cydia pomonella C pom 138 9** 152 - 114 125 122 117 Red bollworm Diparopsis castanea D cas 72 48* 169 113 Spiny bollworm Earias insulana E ins 8** - 60* 81 83 X 138 X Lt. brown apple moth Epiphyas postvittana E pos X-54* Eu grape berry moth Eupocelia ambiguella E amb 72 92 69 30** 62* Oriental fruit moth Grapholitha molesta G mol 11** 27** 77 0** Lesser apple worm Grapholitha prunivora G pru 11** 124 111 Tomato fruit worm Helicoverpa armigera H arm (66) (111) - 119 15** 44* (99) 95 159 Australian bollworm Helicoverpa punctigera H pun 24** 16** - 28** 5** 47 67 35* Tobacco budmoth Heliothis virescens H vir 15** 32 31** 6** 8** 21** 29** 96 26** Corn earworm Heliothis zea H zea 117 156 95 94 72 107 124 100 156 Fall webworm Hyphantria cunea H cun 112 71 95 Eur. grape vine moth Lobesia botrana L bot 61 X 65 69 83 - 90 91 Gypsy moth Lymantria dispar L dis 6** 94 95 56 51 (125) 52* 208 108 - 107 129 69 (114) 156 (93) grape berry moth Paralobesia viteana P vit 27** 75 24** 57 Pink bollworm Pectinophhora gossypiella P gos X (71) 24 29* 144 80 - 4** 126 126 Pink-spotted bollworm Pectinophhora scutigera P scu 85 20** 10* 106 X - 119 52 Tufted apple budmoth Platynota idaeusalis P ida 0** 91 21 13** Pine shoot moth Rhyacionia buoliana R buo 95 - (97) Nutgrass armyworm Spodoptera exempta S exe 33** 17** 74 94 79* 76 - 7** 11** Egyptian cottonworm Spodoptera littoralis S lito 15** 3** 17** 37* 80 63 11** - 174 Cotton leafworm Spodoptera litura S litu 15** 0** 10** 18** 61 X 100 - Pine process. moth Thaumetopoea pityocampa T pit 75* 40* - Study area (ISO 3166 FR ZA, CI FR US IN AU AU AU FR US, US AU FR CI ZA, CI AU FR, country code) FR, PT PT Referencesa 1 1,2 1 1 2 2 1 1 1 1,2,3 1 1 3 2 1,2 1 1,3 a 1, Mastro et al. (1984); 2, Mastro et al. (1985); 3, Brockerhoff et al. (this paper) Author's personal copy

56 J Chem Ecol (2013) 39:50–58 appeared to offer numerous options for combining lures. In Lures for other species also may be possible, as our review L. dispar, for example, up to 11 two-species combinations indicated the potential compatibility of gypsy moth lures with appeared compatible (Table 3). However, this number was lures for up to seven other species. Multiple-species trapping reduced for combinations of more than two target species. requires substantially fewer traps, less staff travel and time to For example, while both Thaumatotibia leucotreta (false check trap catches, reduced diagnostic effort (to verify catches codling moth) and Cydia funebrana (plum fruit moth) were of non-target species), and ultimately should reduce costs and compatible with gypsy moth, catches of C. funebrana were increase benefits of surveillance, compared with operating an reduced by 95 % when the lure for T. leucotreta was present, equivalent program that uses traps for each species separately. rendering this combination incompatible. Some of these efficiencies could also be achieved by placing The compatibility of lures was reduced in species pairs traps for two or more species together, but this would require a that are more closely related. Species from the same super- corresponding increase in trap use and expense. family were less compatible than species from different Our study also provided new insight into mechanisms superfamilies (Table 4). Similar results were obtained at that may affect trapping studies and lure compatibility. It is the family level, although the difference was only margin- known that the sex pheromones of some closely related ally significant. A comparison at the genus level was not moths are mutually antagonistic, a mechanism that aids possible, because there were only five cases in our dataset, reproductive isolation among species (Ando et al., 2004). too few to test this adequately. There was no apparent For example, (8E,10E)‐dodecadien‐1‐yl acetate, the sex limitation in compatibility for species from the same geo- pheromone of the gorse pod moth, Cydia ulicetana graphic region, compared with that from different regions (0 Cydia succedana), is a strong antagonist for C. pomo- (Table 4). nella (Stephens et al., 2008). Our hypothesis that such antagonistic relationships are more likely among more closely related species was confirmed by our analysis of Discussion the combined data. However, interactions also occur among distantly related species. For example, we observed reduced Our studies indicate that combining lures for improved catches of R. buoliana in the presence of the lure for T. efficiency of detection trapping of Lepidoptera is possible pityocampa. In their native ranges, these two species are for many species combinations. Our tests for the four for- sympatric, with both feeding on the foliage of pine trees. estry pests, conducted in Europe, successfully demonstrated Therefore, avoidance mechanisms may have evolved be- compatibility of lures for simultaneous trapping of these tween the two species as a way to reduce direct competition. species, although more trials are required to demonstrate Other mechanisms also influence the usefulness of com- catch of H. cunea. Our trial included all possible lure combining lures, including trap saturation, which we observed binations for the four target species, more than the usual when abundant catches, such as those of the pine proces- two-way comparisons of other studies, and demonstrated sionary moth, reduced the capacity of sticky and other traps that multiple lures for all four pests could be used in existing (Elkinton, 1987) to catch other target species. This trap surveillance trapping programs, such as those operated sole- saturation, which is reflected in at least some cases of ly for gypsy moth, in use in a number of countries, including inter-specific interference, is not due to lure incompatibility, the United States (Sharov et al., 1998), Canada (Régnière et and is unlikely to affect the usefulness of surveillance traps al., 2009), and New Zealand (Brockerhoff et al., 2010). as a “detection trapping” system, because of the low

Table 4 Contingency tables (Fisher’s exact tests) comparing Same superfamily Different superfamily frequencies of pairs of species of Trap catch not significantly reduced 3 (7 %) 11 (37 %) P00.002 Lepidoptera, in which combined Trap catch significantly reduced 42 (93 %) 19 (63 %) pheromone lures caused a re- Total 45 30 duction in trap catch in one or both species, assessing the Same family Different family effects of shared taxonomic Trap catch not significantly reduced 3 (9 %) 11 (26 %) P00.077 groupings and natural geograph- Trap catch significantly reduced 30 (91 %) 31 (74 %) ic range Total 33 42 Same geogr. range Different geogr. range Trap catch not significantly reduced 8 (26 %) 6 (14 %) P00.23 Trap catch significantly reduced 23 (74 %) 38 (86 %) Total 31 44 Author's personal copy

J Chem Ecol (2013) 39:50–58 57 probability of two or more target species invading at the Lymantria dispar japonica (Motschulsky), dissolute tussock same time in large numbers. Therefore, in terms of mutual moth, Lymantria dissoluta Swinhoe, nun moth Lymantria interference of lures, our results are conservative, especially monacha (L.), Indian gypsy moth, Lymantria obfuscata as many of the cases in which a significant reduction in Walker, Ryukyu gypsy moth, Lymantria postalba Inoue, catch occurred are still likely to be useful for a detection pulverea tussock moth, Lymantria pulverea Pogue and program. Moreover, it may be possible to avoid trap satura- Schaefer, and Hokkaido gypsy moth, Lymantria umbrosa tion by using non-saturating trap designs. Other problems (Butler). Lymantri umbrosa recently was caught in a gypsy that could lead to reduced trap catches are catches of non- moth surveillance trap in Hamilton, New Zealand, prompt- target species (Schwalbe and Mastro, 1988), and the accu- ing an eradication campaign across a large part of the city mulation/decomposing of dead insects in traps (Elkinton, (Brockerhoff et al., 2010.) For other species of Lymantria 1987; Jactel et al., 2006). However, neither of these situa- and other Lymantriinae, additional compounds are needed tions would necessarily limit the use of multiple lure sys- to ensure lures are attractive (Supplementary Table 2). These tems for detection. It should be noted that trap saturation and may or may not be compatible with (+)-disparlure for multi- the other problems are not limited to systems that use species trapping. For example, it would be advantageous to multiple lures; it may also happen with single-lure traps, add a lure (6Z-heneicosen-11-one) for the white-spotted tus- and even non-sticky traps (Elkinton, 1987). Nevertheless, sock moth, Orgyia thyellina Butler, to (+)-disparlure if com- the probability of catching non-target species increases patibility were to be demonstrated. Addition of 6Z- when several lures are used at the same time. Other potential heneicosen-11-one lures may also enable surveillance of problems with the use of multiple lures could occur when Douglas fir tussock moth, Orgyia pseudotsugata trap design or trap placement differentially affect target (McDunnough) and other species of Orgyia (Supplementary species; e.g., if two species are optimally trapped at different Table 2). This would require testing to ensure there are no heights or positions on a tree (e.g., trunk vs. twig). However, inhibitory effects among the target species. these effects may not be problematic if the objective is The incompatibility of lures cannot be explained solely in detection rather than population monitoring. terms of ultimate mechanisms of reproductive isolation or Recent studies that have explored multiple-species trapping competition avoidance. Some incompatibilities may be co- for population monitoring, rather than detection, have found incidental, such as that of gypsy moth (Lymantriidae) catch varying degrees of compatibility. Lures were combined with- being inhibited by several, but not all species, of Heliothis out mutual interference for two defoliators, Malacosoma diss- (Noctuidae). Another example is the strong inhibition of gyp- tria Hübner (Lepidoptera: Lasoicampidae) and Choristoneura sy moth catch by the pheromone of summerfruit tortrix, conflictana (Walker) (Lepidoptera: Tortricidae), of Populus Adoxophyes orana (Tortricidae). These incompatibilities are tremuloides in western Canada (Jones et al., 2009). A six- strange, given the hydrocarbon epoxide structure of (+)-dis- way combination of lures for pine defoliators (four moths and parlure, compared to the fatty acid derivatives used by totri- two sawflies) showed that catches of three of these species cids and heliothines, and may be explained by saltational were greatly reduced, precluding simultaneous population shifts in odor perception (Symonds and Elgar, 2008). When monitoring (Johansson et al., 2002). odor perception is acquired following a mutation, it may be The choice of pheromone blend for a species in multiple- functional, and thus selected for, or be neutral and not selected species detection can be important. For example, a blend for or eliminated. Neutral mutations may explain some of the specific for nun moth, Lymantria monacha (L.), consisting unusual incompatibilities of lures. of (7R,8S)-cis-7,8-epoxy octadecane, (7Z)-2-methyl-octade- After a number of years of research, the USDA has cene, and (+)-disparlure is highly attractive to nun moth but implemented multiple-species trapping only on a limited not to gypsy moth. However, use of (+)-disparlure alone basis. The national Cooperative Agricultural Pest Survey catches both species (Gries et al., 1996), in numbers suffi- program, coordinated by the USDA, has a suite of approx- cient for detection. Blend choice, however, may depend on imately 120 pest species from which state co-operators the region where trapping is carried out: the effects of (+)- choose relevant target species. Given the large number of disparlure on nun moth from Japan and central Europe differ potential target species, the USDA currently advises users markedly (Gries et al., 1996, 2001). (+)-Disparlure by itself not to combine lures for multiple species of Lepidoptera is suitable as a lure for several other species of Lymantria unless it has been confirmed by USDA experts that lures are (Supplementary Table 2), including Okinawa gypsy moth, compatible. Our findings highlight the potential for combin- Lymantria albescens Hori and Umeno, orange winged tus- ing lures of compatible species, facilitating increased cost sock moth, Lymantria atemeles Collenette, concolorous tus- efficiency in pest surveillance. sock moth, Lymantria concolor Walker, Asian gypsy moth, Lymantria dispar asiatica Vnukovskii, European gypsy Acknowledgments We thank Ashraf El-Sayed and Lee-Anne Manning moth, Lymantria dispar dispar (L.), Japanese gypsy moth, for advice on pheromone compounds and two anonymous reviewers for Author's personal copy

58 J Chem Ecol (2013) 39:50–58

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