Review Received: 11 May 2014 Revised: 27 August 2014 Accepted article published: 22 September 2014 Published online in Wiley Online Library: (wileyonlinelibrary.com) DOI 10.1002/ps.3913 Termite (order Blattodea, infraorder Isoptera) baiting 20 years after commercial release Theodore A Evansa* and Naeem Iqbala,b Abstract Termite baiting is now one of the two main management tools in developed countries after 20 years of commercial release. It has two main goals: to use small amounts of active ingredient and ‘colony elimination’, i.e. death of all individuals in the colony. We consider how well baiting has been evaluated from 100 studies in the scientific literature. Studies have included 15 active ingredients, 23 termite species and 16 countries, yet most studies have focused on the chitin synthesis inhibitor hexaflumuron, Reticulitermes and the United States. Baiting has mostly met its goals: typically about 0.5 g of active ingredient was used, and colony elimination achieved, albeit with rates varying from 0 to 100%, and sometimes supplemented with liquid insecticide. Baiting was most successful using chitin synthesis inhibitors against Reticulitermes and Coptotermes (Rhinotermitidae), in temperate locations, although colony elimination was usually inferred indirectly – mostly by termite absence from baits – and was often slow, from 25 to 450 days. Baiting has been less tested and less successful against higher termites in tropical locations, where they are most diverse and abundant. Future research may have to consider greater termite species diversity and other active ingredients to reduce control times in order to fulfil the potential of baiting. © 2014 Society of Chemical Industry Keywords: colony elimination; Coptotermes; chitin synthesis inhibitor; chlorfluazuron; hexaflumuron; Reticulitermes 1 INTRODUCTION 1.1 Termites as pests Termites are not a large insect group, comprising fewer than 3000 described species;1 however, they are among the most important by many ecological and economic measures. This is because these insects have evolved the capacity to digest the most abundant biological molecules on the planet, cellulose and lignin, on account of their own digestive enzymes2 and those of the symbiotic protozoa, bacteria and archea living in their guts.3 Thus, termites have become important pests of crops and plantations4 and timber-in-service in the human-built environment.5 Their pestiferousness has led to many pest management methods over time, from large quantities of natural plant extracts such as creosotes and neem used in antiquity to modern neurotoxins.6 – 10 1.2 History of trap and treat One form of pest management that requires very small quantities of poisons is ‘trap and treat’. This method first lures termites into a trap using a food as bait, then treats them with a type of poison. Dusting with arsenic (usually Paris Green) was the first form of trap and treat, especially common in tropical Asia and Australia, but also found in Hawaii and other Pacific Islands and California, from the nineteen and early twentieth century. 6,11 – 19 Dusting was largely replaced by chemical soil barriers in the 1940s. Chemical soil barrier treatments aimed to prevent termite access into buildings, and thus they were perceived to be simpler, safer and more persistent. The first active ingredients were organochloride insecticides from the 1940s (e.g. dieldrin and chlordane), which were joined by organophosphate insecticides (e.g. chlorpyrifos) and synthetic pyrethroids (e.g. deltamethrin and bifenthrin). Chemical soil barriers were completely dominant in termite pest management for over 50 years, yet Pest Manag Sci (2014) their use has declined since the 1990s. This was due to environmental concerns arising from the use of large quantities of synthetic insecticides.20,21 1.3 Rise of baiting The rise of environmental concerns created the conditions for research into and development of baiting, the second form of trap and treat. Baiting differs from dusting in that the poison is incorporated into a food in the trap, which occasionally had occurred previously with arsenic instead of dusting.14 Baiting research appeared in the 1950s and 1960s in Indonesia,22 Canada,23 the United States,24,25 and Australia,26,27 to reduce termite damage to trees grown for timber where barrier treatments were not appropriate. Good control was reported from these early studies; however, research stopped, perhaps because the active ingredient used was mirex, which is an organochlorine insecticide, the uses of which were discontinued either because of individual national regulation or as part of the Stockholm Convention on Persistent Organic Pollutants in 2004. Research into termite baiting re-emerged at the end of the 1980s. Most research was laboratory based to identify the utility of various active ingredients as baiting active ingredients.28 – 30 There was other research into the food matrix that would ∗ Correspondence to: Theodore A Evans, Department of Biological Science, National University of Singapore, 117543, Singapore. E-mail: theo.evans@ nus.edu.sg a Department of Biological Science, National University of Singapore, Singapore b Department of Entomology, Faculty of Agricultural Sciences, Bahauddin Zakariya University, Multan, Pakistan www.soci.org © 2014 Society of Chemical Industry www.soci.org contain the active ingredient, specifically a cellulose-based bait that would interest only termites, and a bait station to house this food matrix.31,32 In addition to environmental benefits, baiting could aim for colony elimination, defined as the death of all members of the colony.33,34 Eventually, commercial baiting systems emerged.35,36 Since that time, and after approximately 25 years of field research, there are now multiple commercial baiting systems (e.g. professional systems include, or have included, Sentricon® by DowAgrosciences, FirstLine® by FMC, Exterra® by Ensystex, Zyrox® by Syngenta, Nemesis® by PCT International, Subterfuge® and Advance® by BASF, Xterm® by Sumitomo, plus many others, including do-it-yourself systems). Therefore, it is timely to consider the published information to determine whether baiting has met its aims. This review aimed to consider the evidence for the efficacy of baiting systems as published in the peer-reviewed scientific literature. Specifically, the number of studies, the size of each study, the active ingredient, the target pest species, the location, the elimination success and the time to elimination were recorded from each study to consider the scientific merits of the published research, and to find patterns over time. 2 BAITING FIELD STUDIES We considered only field studies in the peer-reviewed, scientific literature because one of the aims of baiting was colony elimination, which is difficult to determine under realistic conditions in laboratory studies. We found 100 studies published in 59 papers, TA Evans, N Iqbal with a study defined as one active ingredient used against one termite species in one location. Locations were usually within a country, except when locations in large countries were climatically different enough to justify separate consideration. There were 69 studies that targeted termite colonies (some in urban areas, others in natural habitats) (see Table 1); the replicates in these studies were the colonies. Another 30 studies targeted built structures (and did not attempt to determine colonies in the structures) (see Table 2); the replicates in these studies were the built structures. The studies that targeted termite colonies were treated separately from those that targeted built structures. Of the 100 studies, 29 included untreated controls (i.e. colonies or structures received baits without an insecticidal active ingredient), 70 studies did not include untreated controls and one study was unclear (stated that controls were used, but data were not presented). The average replication rate for studies targeting colonies was (mean ± standard error) 5.4 ± 1.2 replicates, which was lower than studies targeting built structures (7.9 ± 1.4 replicates). There were 21 studies with just one replicate (17 for colony as replicate, four for structure as replicate), 49 studies with 2–5 replicates (37 for colonies and 12 for structures), 22 studies with 6–15 replicates (11 for colonies and 11 for structures) and just eight with more than 16 replicates (three for colonies and five for structures) (Tables 3 and 4). 2.1 Active ingredients A total of 15 active ingredients belonging to three classes of insecticide with three modes of action were tested: neurotoxins Table 1. The active ingredients, species and locations of termite baiting studies that targeted termite colonies Active ingredient CAS numbera Neurotoxin Mirex Deltamethrin Abamectin Number of studiesb Σ/UTC NA 52918-63-5 65195-56-4 65195-55-3 Avermectin 71751-41-2 65195-55-3 65195-56-4 Fipronil 120068-37-3 Metabolic inhibitor NA A9248d Sulfluramid 4151-50-2 Hydramethylnon 67485-29-4 Zinc borate NA Chitin synthesis inhibitor Hexaflumuron 86479-06-3 Noviflumuron 121451-02-3 8/1 Chlorfluazuron Lufenuron Bistrifluron 71422-67-8 103055-07-8 201593-84-2 6/2 1/1 2/2 Speciesc Country 4/3 1/1 3/1 Mas. darwiniensis, R. flavipes C. formosanus C. formosanus, R. flavipes, R. virginicus Australia, Canada, United States United States United States 1/1 C. formosanus United States 3/3 O. formosanus, R. hageni, R. flavipes United States, China 1/1 2/1 2/0 1/0 C. formosanus C. formosanus C. formosanus, R. speratus R. flavipes, R. virginicus United States United States Japan United States 30/6 C. acinaciformis, C. curvignathus, C. formosanus, C. gestroi, C. travians, Heterotermes sp., N. exitiosus, R. flavipes, R. lucifugus, R. speratus, R. sp., R. virginicus C. formosanus, H. aureus, R. flavipes, R. hageni, R. hesperus, R. virginicus C. acinaciformis, Mac. gilvus, G. sulphureus R. hesperus G. sulphureus, C. acinaciformis Australia, Cayman Islands, Italy, Japan, Malaysia, Puerto Rico, United States United States Australia, Philippines, Thailand United States Australia, Malaysia a CAS number not included for experimental compounds. b For the number of studies, Σ is the total number and UTC represents the studies with untreated controls. c For species: C. = Coptotermes, G. = Globitermes, H. = Heterotermes, Mac. = Macrotermes, Mas. = Mastotermes, N. = Nasutitermes, O = Odontotermes, R = Reticulitermes; sp. = species unknown. d A9248 is a type of diiodomethyl p-tolyl sulfone. wileyonlinelibrary.com/journal/ps © 2014 Society of Chemical Industry Pest Manag Sci (2014) Termite baiting www.soci.org Table 2. The active ingredients, species and locations of termite baiting studies that targeted built structures Chemical CAS number Number of studies Σ/UTC Neurotoxin Mirex NA Ivermectin 70288-86-7 Metabolic inhibitor Sulfluramid 4151-50-2 Chitin synthesis inhibitor Hexaflumuron 86479-06-3 Noviflumuron Chlorfluazuron 2/0 3/2 a 121451-02-3 71422-67-8 Speciesa Country 2/1 2/0 R. sp. C. formosanus, O. formosanus United States China 3/1 R. flavipes Chile, United States 14/1 C. formosanus, C. travians, H. aureus, H. sp., R. flavipes, R. grassei, R. lucifugus, R. separatus, R. sp. C. gestroi, C. formosanus C. curvignathus, C. vastator, Mic. losbanosensis Chile, Italy, United Kingdom, Malaysia, Taiwan, United States, US Virgin Islands Malaysia, United States Indonesia, Philippines Abbreviations as in Table 1, plus Mic. = Microcerotermes. Table 3. The baiting outcomes for baiting studies that targeted termite coloniesa Active ingredient Number of colonies baited [mean (range)] Percentage of colonies eliminated [mean (range)] Neurotoxin Mirex 4 (2–6) Deltamethrin 2(–) Abamectin 2.7 (1–7) Avermectin 3(–) Fipronil 2.3 (2–3) Metabolic inhibitor A9248 3(–) Sulfluramid 6 (3–9) Hydramethylnon 1(–) Zinc borate 2 (1–3) Chitin synthesis inhibitor Hexaflumuron 3.8 (1–35) 0(–) 38.9 (0–78) 50 (0–100) 0(–) Noviflumuron Chlorfluazuron Lufenuron Bistrifluron a 18 (4–72) 5.3 (2–13) 5(–) 9 (6–12) Elimination time (days) [mean (range)] 100 ( – ) 0(–) 0(–) 0(–) 55.6 (50–67) 24 (7–73) Active ingredient (mg) [mean (range)] Reference 1900 ( – ) 250 ( – ) >1 (>1–1) 334 (1–500) 2 (>1–5) 26, 114 114 87, 114 114 53, 67 101 (49–153) 268 ( – ) 180 (59–308) 858 (5–3980) 66 (45–87) ? 129 39, 114 114, 121 87 90.3 (0–100) 173 (25–450) 558 (4–3400) 100 ( – ) 97.4 (85–100) 100 ( – ) 91.7 (83–100) 144 (20–342) 106 (56–126) 65 (37–93) 88 (56–120) 399 (1–1470) 1142 (182–5000) 12 (3–24) 248 (65–1226) 33, 35, 36, 40–42, 64, 69–72, 77, 78, 82, 91, 114, 102, 121,124, 126, 128, 129, 135, 136 58, 69, 79 73–76 60, 119 34, 123 92 (71–150) Means and ranges are across species and locations; — = insufficient data available; ? = no data available. that prevent transmission of nerve signals; metabolic inhibitors that block the electron transport chain in the mitochondria; chitin synthesis inhibitors that block chitin production during moulting. There were six neurotoxins trialled in 14 studies, four metabolic inhibitors trialled in ten studies and five chitin synthesis inhibitors trialled in 75 studies (Tables 1 and 2). 2.2 Termite species There were a total of 23 species used in baiting studies. These included: one species in the Mastotermitidae, Mastotermes darwiniensis Froggatt; 17 species in the Rhinotermitidae, with eight species in Reticulitermes Holmgren; two species in Heterotermes Froggatt; seven species in Coptotermes Wasmann; five species in the Termitidae, with one species each in Macrotermes Holmgren, Odontotermes Holmgren, Globitermes Holmgren, Microcerotermes Pest Manag Sci (2014) Silvestri and Nasutitermes Dudley. There was only a single study against termites belonging to Mastotermitidae. There were a total of 90 studies in Rhinotermitidae with 45 studies in Reticulitermes, 41 studies in Coptotermes and four studies in Heterotermes. There were nine studies in Termitidae with three studies against Macrotermes, two studies against each of Odontotermes and Globitermes and one study each against Microcerotermes and Nasutitermes (Tables 1 and 2). 2.3 Study locations The baiting studies were performed in 16 countries and territories. The majority of locations and studies were in the United States, across 13 states: Arizona, California, Florida, Georgia, Hawaii, Kentucky, Louisiana, Mississippi, New York, North Carolina, Ohio, Texas and Virginia. There was one location in Canada, three locations in © 2014 Society of Chemical Industry wileyonlinelibrary.com/journal/ps www.soci.org TA Evans, N Iqbal Table 4. The baiting outcomes for baiting studies that targeted built structuresa Active ingredient Number of structures/plots baited [mean (range)] Neurotoxin Mirex 9 (6–12) Ivermectin 4.5 (3–6) Metabolic inhibitor Sulfluramid 17.3 (2–25) Chitin synthesis inhibitor Hexaflumuron 9.5 (1–29) Noviflumuron 5(–) Chlorfluazuron 5 (4–6) a Percentage of infestations eliminated [mean (range)] Elimination time (days) [mean (range)] Active ingredient (mg) [mean (range)] Reference 0 100 ( – ) 0 126 (37–302) 109 (2–220) ? 24, 25 115, 122 54.7 (0–84) 110 (27–196) ? 68, 108 96.8 (80–100) 100 ( – ) 100 ( – ) 205 (27–1170) 340 (34–905) 100 (42–231) 744 (64–3098) 1131 (100–3037) 168 (42–282) 68, 70, 108, 117, 118, 125, 127, 130–134 63, 66 75, 110 Means and ranges are across species and locations; — = insufficient data available; ? = no data available. the Caribbean Sea (Cayman Islands, US Virgin Islands and Puerto Rico) and one in South America in Chile. There were two locations in Europe: in the United Kingdom and Italy. There were three locations in Australia (Queensland, New South Wales and the Northern Territory) and one in New Zealand. Finally, there were eight locations in Asia: in Indonesia, Malaysia, Thailand, Philippines, Taiwan, China (two provinces: Wuhan and Zhejiang) and Japan (Tables 1 and 2). There were 69 studies on termites in their natural, native range and 31 studies on invasive termites37 outside their natural range. 2.4 Quantity of active ingredient Of the 100 studies, 60 included data on the amount of active ingredient removed from bait stations, 46 from studies on colonies and 14 from studies on structures. The overall mean across all studies was 545 mg active ingredient per replicate colony or structure. The lowest amounts were for neurotoxins, and the highest were for chitin synthesis inhibitors: 239 mg for neurotoxins, 500 mg for metabolic inhibitors and 587 mg for chitin synthesis inhibitors. Reflecting on these averages, the minimum amount of bait active ingredient of any kind removed by any one colony was 0.01 mg (for abamectin against Reticulitermes flavipes in Georgia, United States), and the maximum was 5000 mg (for chlorfluazuron against Coptotermes acinaciformis in Queensland, Australia). Nevertheless, there were no obvious patterns between types of active ingredient, because of the variation in study types and scale. For example, in the United States, native Reticulitermes colonies in natural landscapes are smaller than those of invasive Coptotermes colonies in urban landscapes, and thus are likely to require smaller amounts of active ingredient. Perhaps the only comparison that might be considered is between hexaflumuron and noviflumuron owing to the number of studies and similarity of baiting system (both from Dow AgroSciences). Less noviflumuron was required to eliminate colonies than hexaflumuron, in less time (Table 3 and 4). 2.5 Colony elimination Most of the published studies considered ‘colony elimination’ to be the absence of termites in the bait and monitoring stations, and not the actual effect on the colony by examining the nest for termites (see Sections 4.2 and 4.3 below). Colony wileyonlinelibrary.com/journal/ps elimination, i.e. lack of foraging termites in bait stations, was determined to have occurred in 86% of all cases: in 4.7 ± 1.2 colonies or 6.8 ± 1.5 structures per study. Among the neurotoxins, two (mirex and fipronil) eliminated between 56 and 100% of exposed colonies, whereas three (abamectin, avermectin and deltamethrin) did not eliminate any colonies. Two metabolic inhibitors (sulfluramid and hydramethylnon) caused around 50% colony elimination, whereas another two (A9248 and zinc borate) caused none. All five chitin synthesis inhibitors eliminated from 90 to 100% of exposed colonies, depending upon the termite species involved (Tables 3 and 4). The mean minimum time to elimination was similar for studies using colonies and structures as replicates: 111 ± 14 days for colonies and 105 ± 20 days for structures per study. The mean maximum time to elimination was considerably lower for studies using colonies compared with those using structures: 190 ± 16 days for colonies and 272 ± 54 days for structures per study (Tables 3 and 4). Among the active ingredients that eliminated colonies, neurotoxins were the fastest, metabolic inhibitors the slowest and chitin synthesis inhibitors in the middle. The average time to elimination for neurotoxins was less than 4 weeks for mirex and over 13 weeks for fipronil. Colony elimination times for the metabolic inhibitors were over 14 weeks for sulfuramid and over 38 weeks for hydramethylnon. For the chitin synthesis inhibitors, lufenuron was fastest at around 9 weeks, then 12 weeks for bistriflumuron, 15 weeks for chlorfluazuron and over 20 for noviflumuron, and the slowest was over 24 weeks for hexaflumuron (Table 3). There was considerable variation in elimination time for each active ingredient, depending on the species and location and the size of the study – larger studies reported longer control times. Some studies of sulfluramid and hexaflumuron used additional spot treatments in buildings to help control infestations; the relative value of these spot treatments is unknown, yet they are reported to be used often in actual use conditions. Effects other than colony elimination have been considered, including reduction in population size. Population sizes have been estimated using various mark–recapture methods with histological fat stains as markers.33,38 – 42 However, they are not considered here as the method is deeply flawed owing to the violation of all essential assumptions.40,43 – 49 Mark–recapture is no longer used for estimating population size,50 – 54 but is used for territory demarcation.55 – 60 © 2014 Society of Chemical Industry Pest Manag Sci (2014) Termite baiting www.soci.org Chitin synthesis inhibitors Bistrifluron 25 Leufenuron Chlorfluazuron Number of studies 20 Noviflumuron Hexaflumuron Metabolic inhibitors Zinc Borate 15 Hydramethylnon Sulfuramid 10 Neurotoxins A9248 5 Fipronil Iver-, Aver-, Abamectin Deltamethrin 10-12 07-09 04-06 01-03 98-00 95-97 92-94 89-91 86-88 83-85 80-82 77-79 74-76 71-73 Mirex 68-70 0 Time (triennia) Figure 1. The number of termite baiting studies over time. Note that time has been separated into 3 year periods (triennia). Chitin synthesis inhibitors are depicted with stripes, metabolic inhibitors with solid colours and neurotoxins with spots. 3 STUDIES OVER TIME 3.1 Active ingredients The earliest of the modern studies used the organochloride mirex (1960–1980), which was replaced by a variety of neurotoxins and metabolic inhibitors (1986–2003). The chitin synthesis inhibitors, especially hexaflumuron, received the most attention starting in 1989, with the bulk of studies during an 8 year period (1992–2006), and a steep decrease in the number of studies from 2007 onwards (Fig. 1). 3.2 Termite species The majority of studies have been on Reticulitermes species, followed by Coptotermes species. The pattern mimics that for active ingredients, with the bulk of studies occurring during the same 8 year period as hexaflumuron (1992–2006). Species in the ‘higher’ termite family Termitidae were considered from 2001 onwards, coincident with a decline in the study of the Rhinotermitidae (Fig. 2). 3.3 Study locations The majority of studies have been in in United States; in fact, almost all studies were in the United States and Canada from 1968 until 1995; the one exception was in Australia. Since 1995 the number of studies in Asia has increased, and now dominate, albeit at a lower (and declining) level (Fig. 3). There has been just one study in South America (Chile), and there have been no studies at all in Africa. 4 BAITING SUCCESS AND ISSUES 4.1 Baiting successes Baiting appears to have achieved its aims, with small quantities of active ingredients used to eliminate or suppress termite colonies. This result was not uniform for all active ingredients, termite species or locations, but was consistent for most common active ingredient, termite genus and location. Of the 100 studies, Pest Manag Sci (2014) 51 studies used the chitin synthesis inhibitor hexaflumuron, 45 studies were against the genus Reticulitermes and 56 studies were performed in the United States. A total of 23 studies, just under one-quarter, were on the exact combination of hexaflumuron + Reticulitermes + USA. The outcomes across these studies were uniformly positive, with small quantities of active ingredient used, and a high average percentage of colonies or infestations in structures eliminated. However, the length of time to control could be long, with an average of 24 weeks and a maximum of 1.5 years. These results are similar for Coptotermes, which is a close relative of Reticulitermes; both genera are in the family Rhinotermitidae. This success for termites in the Rhinotermitidae in temperate locations came with caveats in some studies, as they used additional liquid insecticide spot treatments in structures,61 – 63 which continue to be used in real-world situations. 4.2 Issues in interpretation of study results Even though most studies reported positive results from baiting, there were issues with the study methods. The first method issue is of greater concern: most studies lack untreated controls, which are essential in any standard scientific study. The lack of controls affects the interpretation of results; specifically, the effect of the treatment cannot be separated from the effect of time. Many studies occurred in termite-infested buildings, and it is understandable that the owners of any such building would want the infestation controlled as quickly as possible, and not want their building to serve as an untreated control. In lieu of controls, these studies considered termite activity in ‘monitoring stations’, which were bait stations that did not receive poisonous bait.35,36,40,42,64 – 70 These are a useful and welcome addition; however, monitoring stations do not control for confounding effects of time, especially if monitoring is conducted for no more than one season. Another useful measurement was acoustic emissions in the wood of built structures, which are caused by chewing termites.67 – 71 The second method issue concerns claims of effects on the colony, especially colony elimination. Just ten of the 100 studies © 2014 Society of Chemical Industry wileyonlinelibrary.com/journal/ps www.soci.org TA Evans, N Iqbal Termitidae Nasutitermitinae 1 Nasutitermes 25 Termitinae 1 Microcerotermes Number of studies 20 1 Globitermes Macrotermitinae 1 Odontotermes 15 1 Macrotermes 10 Rhinotermitidae 7 Coptotermes 2 Heterotermes 5 8 Reticulitermes Mastotermitidae 10-12 07-09 04-06 01-03 98-00 95-97 92-94 89-91 86-88 83-85 80-82 77-79 71-73 68-70 74-76 1 Mastotermes 0 Time (triennia) Figure 2. The species trialled in termite baiting studies over time. The Termitidae (subfamilies Nasutitermitinae, Termitinae and Macrotermitinae) are depicted with stripes, the Rhinotermitidae with solid colours and the Mastotermitidae with spots. The number of species precedes each genus name. Pacific 25 Japan China & Taiwan Number of studies 20 SE Asia Australia & New Zealand 15 Europe 10 Central & South Americas USA & Canada 10-12 07-09 04-06 01-03 98-00 95-97 92-94 89-91 86-88 83-85 80-82 77-79 74-76 71-73 0 68-70 5 Time (triennia) Figure 3. The location of termite baiting studies over time. Asia-Pacific is depicted in stripes, Australasia with spots and Europe and the Americas in solid colours. Pacific = Hawaii plus other US territories in the Pacific Ocean; SE Asia = Indonesia, Malaysia, Thailand and the Philippines; Europe = Italy and the United Kingdom; Central and South America include the Caribbean Islands. measured the effect on the colony directly, by dissecting the nest to observe reproductives and dependent castes, and only two of these studies reported 100% colony elimination.26,34,72 – 75 DNA fingerprinting was used in a further ten studies to determine the genetic identify of the termites before and after baiting, which does not measure effects on the reproductives in the nest, but does show whether foragers from baited colonies return or not.58,76 – 78 There remain 80 studies that relied on the presence or absence of termites in bait stations as their only wileyonlinelibrary.com/journal/ps measure, and many of these studies reported 100% colony elimination, especially those testing hexaflumuron. It is difficult, usually impossible, to examine the nest of a cryptic underground nesting species, such as those in Reticulitermes; this was noted as early as 1876,79 and noted for baiting studies from 1996.40 Furthermore, the nests of some species may be diffuse with eggs and larvae in multiple locations.80 Although it is possible, even probable, that a long absence of termites from bait stations is due to the elimination of the colony, it is not the only interpretation. For example, © 2014 Society of Chemical Industry Pest Manag Sci (2014) Termite baiting www.soci.org termites are known to abandon bait stations that are inspected too frequently, as they avoid disturbance, or even for no apparent reason.40,53,58,62,81,82 4.3 Formal assessment criteria The difficulties of measuring colony level effects in (difficult to locate) subterranean nests has resulted in studies that consider more accessible assessment criteria;53,54,83,84 these rules have been formalised in the state of Florida in the United States (Rule 5E-2.0311).59 Criteria include: monitoring of termite activity preand post-treatment using monitoring stations and other ‘natural monitors’ (such as mud tubes or the actual infestation in the building); removal of poisonous bait (usually inferred as ‘consumption’, but removed bait is not always consumed85,86 ); and change in alate numbers. The change in alate numbers is especially indicative of a colony level effect of baiting; however, even this criterion can be influenced by seasonal fluctuations, and records of alate flights pretreatment are needed. All such criteria are enhanced by colony identification with DNA fingerprinting. These issues may be dismissed as quibbles over scientific method and accuracy by those who consider the success of termite baiting in the marketplace as a more important indicator,87 yet such dismissal ignores scientific rigour. 4.4 Future directions Baiting faces one serious challenge within the marketplace: that the time to achieve control is slow, especially compared with chemical soil barriers.88,89 This is often a consequence of a low contact rate to bait stations.61,63,81,90 – 93 Not surprisingly, considerable effort has been invested in methods to attract termites to bait stations, including amino acids, sugars, even sports drinks,92,94 – 102 carbon dioxide103,104 and bait station placement, including auxiliary stations,58,68,90,92,105 – 108 although results have been inconsistent. There is notably little published research on aspects of bait station design, such as size,82 and varying inspection frequency, from 2 weeks to 3 months, and even to 1 year.58,59,107,109 The need to improve termite baiting goes well beyond increasing success for the well-studied pest species in the Rhinotermitidae in the United States and similar temperate regions of the northern hemisphere. Of the total of 371 known pest termite species, 105 belong to the Rhinotermitidae, one to the Mastotermitidae, ten to the Termopsidae, 49 to the Kalotermitdae and 206 (56%) to the Termitidae.1 The species in the Termitidae are overwhelmingly found in the tropical regions of the world,110 and have received very limited attention: four species with eight studies in total (Tables 1 and 2). Termitid species do not appear to respond well to chitin synthesis inhibitors, especially compared with species in the family Rhinotermitidae, perhaps for two reasons. The first is that the chitin synthesis inhibitors developed for the Rhinotermitidae may not disrupt the chitin synthesis enzymes in the Termitidae, as they are too distantly related. The second reason is that most species in the Termitidae moult fewer times than species in the Rhinotermitidae,111 thus decreasing their vulnerability to this mode of action. Clearly, more research is needed on termite baiting, especially the Kalotermitidae and the Termitidae, and in the tropics. The ‘drywood termites’ in the Kalotermitidae are often treated with fumigation; yet there has been research into baiting with hydramethylnon in a gel.112 If results for chitin synthesis inhibitors continue to be disappointing for the Termitidae, then new bait active ingredients will be sought, perhaps neurotoxins. Neurotoxins were Pest Manag Sci (2014) once considered to be too fast acting for baiting; however, several baiting studies found some success if they were used at very low doses.65,113,114 Future developments in termite baiting may come from Asia, as suggested by the increasing number of Asian baiting studies (Fig. 3), driven by growing environmental awareness and increasing wealth, combined with the difficulty in managing more diverse pest assemblages.115,116 ACKNOWLEDGEMENT NI was funded by the Pakistani Higher Education Commission International Research Support Initiative Programme. REFERENCES 1 Krishna K, Engel MS, Grimaldi DA and Krishna V, Treatise on the Isoptera of the world, Vol. 1. Bull Am Mus Nat Hist 377:1–200 (2013). 2 Watanabe H, Noda H, Tokuda G and Lo N, A cellulase gene of termite origin. Nature 394:330–331 (1998). 3 Ohkuma M and Brune A, Diversity, structure, and evolution of the termite gut microbial community, in Biology of Termites: a Modern Synthesis, ed. by Bignell DE, Roisin Y and Lo N. Springer, Dordrecht, The Netherlands, pp. 413–438 (2011). 4 Rouland-Lefèvre C, Termites as pests of agriculture, in Biology of Termites: a Modern Synthesis, ed. by Bignell DE, Roisin Y and Lo N. Springer, Dordrecht, The Netherlands, pp. 499–517 (2011). 5 Su NY and Scheffrahn RH, Termites as pests of buildings, in Termites: Evolution, Sociality, Symbioses, Ecology, ed. by Abe T, Bignell DE and Higashi M. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 437–453 (2000). 6 Kofoid CA, Light SF, Horner AC, Randall M, Herms WB and Bowe EE, Termites and Termite Control. University of California Press, Berkeley, CA (1934). 7 Snyder TE, Our Enemy the Termite, 2nd edition. Comstock Publishing, Ithaca, NY (1948). 8 Harris WV, Termites: their Recognition and Control. Longman, London, UK (1961). 9 Edwards R and Mill AE, Termites in Buildings, their Biology and Control. Rentokil Library, London, UK (1986). 10 Pearce MJ, Termites: Biology and Pest Management. CAB International, London, UK (1997). 11 Cleghorn HFC, The Forests and Gardens of South India. WH Allen Co., London, UK (1861). 12 Froggatt WW, Economic entomology. White ants (Termitidae) with suggestions for dealing with them in houses and orchards. Agric Gaz NSW 16:632–656, 753–774 (1905). 13 Fullaway DT, Termites, or white ants, in Hawaii. Hawaiian For Agric 17:294–301 (1920). 14 Keuchenius PE and Corporaal JB, Dierlijke vijanden van Hevea brasiliensis (Animal enemies of Hevea brasiliensis), in Handboek voor de Rubber Cultuur in Nederlandsch-Indie (Handbook for Rubber Culture in Netherlands-India), ed. by Swart NL and Rutgers AAL. JH de Bussy, Amsterdam, pp. 216–229 (1922). 15 Jepson FP, The control of tea termites. Trop Agric 75:191–195 (1930) 16 Kelsey JM, A termite damaging coconut palms on Suwarro Island: Calotermes (Neotermes) rainbowi Hill. NZ J Sci Technol 27B:69–75 (1945). 17 Hickin NE, Termites: a World Problem. Hutchinson and Co. Ltd, London, UK (1971). 18 Roonwal ML, Termite Life and Termite Control in Tropical South Asia. Scientific Publishers, Bombay, India (1979). 19 Watson JAL, Termites in the Canberra Region, 2nd edition. CSIRO Publishing, Canberra, Australia (1988). 20 Carson R, Silent Spring, Houghton Mifflin, Boston, MA (1962). 21 Cropper ML, Evans WN, Berardi SJ, Ducla-Soares MM and Portney PR, The determinants of pesticide regulation: a statistical analysis of EPA decision making. J Polit Econ 100:175–197 (1992). 22 Kalshoven LGE, The ability of Coptotermes to locate exposed timber. Idea 10:43–49 (1955). 23 Esenther GR and Gray DE, Subterranean termite studies in southern Ontario. Can Entomol 100:827–834 (1968). 24 Esenther GR and Beal RH, Attractant-mirex bait suppresses activity of Reticulitermes spp. J Econ Entomol 67:85–88 (1974). © 2014 Society of Chemical Industry wileyonlinelibrary.com/journal/ps www.soci.org 25 Esenther GR and Beal RH, Insecticidal baits on field plot perimeters suppress Reticulitermes. J Econ Entomol 71:604–607 (1978). 26 Paton R and Miller LR, Control of Mastotermes darwiniensis Froggatt (Isoptera: Mastrotermitidae) with mirex baits. Aust For Res 10:249–258 (1980). 27 Lenz M and Evans TA, Termite bait technology: perspectives from Australia, in Proceedings of the 4th International Conference on Urban Pests, ed. by Jones SC, Zhai J and Robertson WH. Charleston, SC, pp. 27–36 (2002). 28 Prestwich GD, Mauldin JK, Engstrom JB, Carvalho JF and Cupo DY, Comparative toxicity of fluorinated lipids and their evaluation as bait-block toxicants for the control of Reticulitermes spp. (Isoptera: Rhinotermitidae). J Econ Entomol 76:690–695 (1983). 29 Jones SC, Evaluation of two insect growth regulators for the bait-block method of subterranean termite (Isoptera: Rhinotermitidae) control. J Econ Entomol 77:1086–1091 (1984). 30 Su N-Y, Tamashiro M and Haverty MI, Characterization of slow-acting insecticides for the remedial control of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 80:1–4 (1987). 31 Su N-Y, Tamashiro M and Haverty MI, Effects of three insect growth regulators, feeding substrates, and colony origin on survival and presoldier production of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 78:1259–1263 (1985). 32 Su N-Y and Scheffrahn RH, A method to access, trap, and monitor field populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 12:299–304 (1986). 33 Su NY, Field evaluation of hexaflumuron bait from population suppression of subterranean termites (Isoptera: Rhinotermitidae). J Econ Entomol 87:389–397 (1994). 34 Evans TA, Rapid elimination of field colonies of subterranean termites (Isoptera: Rhinotermitidae) using bistrifluron solid bait pellets. J Econ Entomol 103:423–432 (2010). 35 Su NY, Thoms EM, Ban PM and Scheffrahn RH, Monitoring/baiting station to detect and eliminate foraging populations of subterranean termites (Isoptera: Rhinotermitidae ) near structures. J Econ Entomol 88:932–936 (1995). 36 Su NY, Ban PM and Scheffrahn RH, Control of subterranean termites (Isoptera: Rhinotermitidae) using commercial prototype above ground stations and hexaflumuron baits. Sociobiology 37:111–120 (2001). 37 Evans TA, Forschler BT and Grace JK, Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474 (2013). 38 Jones SC, Colony size of the desert subterranean termite Heterotermes aureus (Isoptera: Rhinotermitidae). SW Nat 35:285–291 (1990). 39 Su NY, Scheffrahn RH and Ban PM, Effects of sulfluramid-treated bait blocks on field colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 88:1343–1348 (1995). 40 Grace JK, Tome CHM, Shelton TG, Oshiro RJ and Yates JR, Baiting studies and considerations with Coptotermes formosanus (Isoptera: Rhinotermitidae) in Hawaii. Sociobiology 28:511–520 (1996). 41 Su NY, Ban PM and Scheffrahn RH, Remedial baiting with hexaflumuron in above-ground stations to control structure-infesting population of Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 90:809–817 (1997). 42 Tsunoda K, Matsuoka H and Yoshimura T, Colony elimination of Reticulitermes speratus (Isoptera: Rhinotermitidae) by bait application and the effect on foraging territory. J Econ Entomol 91:1383–1386 (1998). 43 Forschler BT and Townsend ML, Mark–recapture estimates of Reticulitermes spp. (Isoptera: Rhinotermitidae) colony foraging populations from Georgia, USA. Environ Entomol 25:952–962 (1996). 44 Thorne BL, Russek-Cohen E, Forschler BT, Breisch NL and Traniello JFA, Evaluation of mark recapture methods for estimating forager population size of subterranean termite (Isoptera: Rhinotermitidae) colonies. Environ Entomol 25:938–951 (1996). 45 Evans TA, Lenz M and Gleeson PV, Testing assumptions of mark–recapture protocols for estimating population size using Australian, mound-building, subterranean termites (Isoptera: Rhinotermitidae and Termitidae). Ecol Entomol 23:139–159 (1998). 46 Evans TA, Lenz M and Gleeson PV, Estimating population size and forager movement in a tropical subterranean termite (Isoptera: Rhinotermitidae). Environ Entomol 28:823–830 (1999). 47 Evans TA, Estimating relative decline in populations of subterranean termites (Isoptera: Rhinotermitidae) due to baiting. J Econ Entomol 94:1602–1609 (2001). wileyonlinelibrary.com/journal/ps TA Evans, N Iqbal 48 Evans TA, Tunnel specificity and forager movements in subterranean termites (Isoptera: Rhinotermitidae and Termitidae). Bull Entomol Res 92:193–201 (2002). 49 Evans TA, Comparing mark–recapture and constant removal protocols for estimating population size of the subterranean termite Coptotermes lacteus (Isoptera: Rhinotermitidae). Bull Entomol Res 94:1–9 (2004). 50 Jones DT, Verkerk RHJ and Eggleton P, Methods for sampling termites, in Insect Sampling in Forest Ecosystems, ed. by Leather SR. Blackwell, Oxford, UK, pp. 221–253 (2005). 51 Hu J, Zhong J-H and Guo M-F, Foraging territories of the black-winged subterranean termite Odontotermes formosanus (Isoptera: Termitidae) in Southern China. Sociobiology 48:1–12 (2006). 52 Long CE and Thorne BL, Resource fidelity, brood distribution and foraging dynamics in complete laboratory colonies of Reticulitermes flavipes (Isoptera Rhinotermitidae). Ethol Ecol Evol 18:113–125 (2006). 53 Forschler BT and Jenkins TM, Subterranean termites in the urban landscape: understanding their social structure is the key to successfully implementing population management using bait technology. Urban Ecosyst 4:231–251 (2000). 54 Thorne BL and Forschler BT, Criteria for assessing efficacy of stand-alone bait treatments at structures. Sociobiology 36:245–255 (2000). 55 Atkinson TH, Use of dyed matrix in bait stations for determining foraging territories of subterranean termites (Isoptera: Rhinotermitidae: Reticulitermes spp. and Termitidae: Amitermes wheeleri). Sociobiology 36:149–167 (2000). 56 Crosland MWJ and Su NY, Mark–recapture without estimating population sizes: a tool to evaluate termite baits. Bull Entomol Res 96:99–103 (2006). 57 Nobre T, Nunes L and Bignell DE, Estimation of foraging territories of Reticulitermes grassei through mark–release–recapture. Entomol Exp Applic 123:119–128 (2007). 58 Eger JE, Lees MD, Neese PA, Atkinson TH, Thoms EM, Messenger MT et al., Elimination of subterranean termite (Isoptera: Rhinotermitidae) colonies using a refined cellulose bait matrix containing noviflumuron when monitored and replenished quarterly. J Econ Entomol 105:533–539 (2012). 59 Thoms EM, Eger JE, Messenger MT, Vargo E, Cabrera B, Riegel C et al., Bugs, baits, and bureaucracy: completing the first termite bait efficacy trials (quarterly replenishment of noviflumuron) initiated after adoption of Florida Rule, Chapter 5E-2.0311. Am Entomol 55:29–39 (2009). 60 Bowen CJ and Kard B, Termite aerial colony elimination using lufenuron bait (Isoptera: Rhinotermitidae). J Kansas Entomol Soc 85:273–284 (2012). 61 Pawson BM and Gold RE, Evaluation of baits for termites (Isoptera: Rhinotermitidae) in Texas. Sociobiology 28:485–510 (1996). 62 Haagsma KA and Rust MK, Effect of hexaflumuron on mortality of the Western subterranean termite (Isoptera: Rhinotermitidae) during and following exposure and movement of hexaflumuron in termite groups. Pest Manag Sci 61:517–531 (2005). 63 Austin JW, Glenn GJ and Gold RE, Protecting urban infrastructure from Formosan termite (Isoptera: Rhinotermitidae) attack: a case study for United States Railroads. Sociobiology 51:231–247 (2008). 64 Sajap AS, Lee LC, Ouimette D and Jaafar AM, Field evaluation of noviflumuron for controlling asian subterranean termite, Coptotermes gestroi (Isoptera: Rhinotermitidae), in Proc 5th Int Conf on Urban Pests, ed. by Lee CY and Robinson WH. Perniagaan, Malaysia, pp. 239–241 (2005). 65 Huang QY, Lei CL and Xue D, Field evaluation of a fipronil bait against subterranean termite Odontotermes formosanus (Isoptera: Termitidae). J Econ Entomol 99:455–461 (2006). 66 Ripa R, Luppichini P, Su NY and Rust MK, Field evaluation of potential control strategies against the invasive eastern subterranean termite (Isoptera: Rhinotermitidae) in Chile. J Econ Entomol 100:1391–1399 (2007). 67 Cabrera BJ and Thoms EM, Versatility of baits containing noviflumuron for control of structural infestations of Formosan subterranean termites (Isoptera: Rhinotermitidae). Fla Entomol 89:20–31 (2006). 68 Potter MF, Eliason EA, Davis K and Bessin RT, Managing subterranean termites (Isoptera: Rhinotermitidae) in the Midwest with a hexaflumuron bait and placement considerations around structures. Sociobiology 38:565–584 (2001). © 2014 Society of Chemical Industry Pest Manag Sci (2014) Termite baiting www.soci.org 69 Su NY, Ban PM and Scheffarhn RH, Control of subterranean termite populations at San Cristóbal and El Morro, San Juan National Historic Site. J Cult Herit 3:217–225 (2002). 70 Su NY, Freytag E, Bordes ES and Dycus R, Control of Formosan subterranean termite infestations using baits containing an insect growth regulator. Stud Conserv 45:30–38 (2000). 71 Ferrari R and Marini M, Subterranean termite Reticulitermes spp. (Isoptera: Rhinotermitidae) baiting and control in historical public buildings in Italy, in Proc 3rd Int Conf on Urban Pests, ed. by Robinson WH. Czech University of Agriculture, Prague, Czech Republic, pp. 357–365 (1999). 72 Peters BC and Fitzgerald CJ, Field evaluation of the bait toxicant chlorfluazuron in eliminating Coptotermes acinaciformis (Froggatt) (Isoptera: Rhinotermitidae) J Econ Entomol 96:1828–1831 (2003). 73 Peters BC and Broadbent S, Evaluating the Exterra™ termite interception and baiting system in Australia, Thailand and the Philippines, in Proc 5th Int Conf on Urban Pests, ed. by Lee CY and Robinson WH. Perniagaan, Malaysia, pp. 229–232 (2005). 74 Garcia CM, Giron MY and Broadbent SG, Termite baiting system: a new dimension of termite control in the Philippines. International Research Group on Wood Protection (Stockholm) 38th Annual Meeting, Moran, WY, Document No. IRG/WP 07-10608 (2007). 75 Dhang P, A preliminary study on elimination of colonies of the mound building termite Macrotermes gilvus (Hagen) using a chlorfluazuron termite bait in the Philippines. Insects 2:486–490 (2011). 76 Vargo EL, Genetic structure of Reticulitermes flavipes and R. virginicus (isoptera: Rhinotermitidae) colonies in an urban habitat and tracking of colonies following treatment with hexaflumuron bait. Environ Entomol 32:1271–1282 (2003). 77 Messenger MT, Su NY, Husseneder C and Grace JK, Elimination and reinvasion studies with Coptotermes formosanus (Isoptera: Rhinotermitidae) in Louisiana. J Econ Entomol 98:916–929 (2005). 78 Husseneder C, Simms DM and Riegel C, Evaluation of treatment success and patterns of reinfestation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 100:1370–1380 (2007). 79 Hagen HA, The probable danger from white ants. Am Nat 10:401–410 (1876). 80 Lenz M, Kard B, Evans TA, Mauldin JK, Etheridge JL and Abbey HM, Differential use of identical food resources by Reticulitermes flavipes (Isoptera: Rhinotermitidae) in two types of habitats. Environ Entomol 38:35–42 (2009). 81 Forschler BT and Ryder JC, Subterranean termite, Reticulitermes spp. (lsoptera: Rhinotermitidae), colony response to baiting with hexaflumuron using a prototype commercial termite baiting system. J Entomol Sci 31:143–151 (1996). 82 Evans TA and Gleeson PV, The effect of bait size, composition, presentation and inspection frequency on bait consumption in termites (Isoptera: Rhinotermitidae). Bull Entomol Res 96:85–90 (2006). 83 Traniello JFA and Thorne BL, Termite baits in theory and practice, in Proc Natl Conf on Urban Entomology, ed. by Robinson WH. Atlanta, GA, pp. 28–40 (1994). 84 Forschler B, Sustainable termite management using an integrated pest management approach, in Urban Pest Management: an Environmental Perspective, ed by Dhang P. CABI, London, UK, pp. 133–144 (2011). 85 Duncan FD, Behavioural responses to poison baits by the termite Hodotermes mosambicus (Hagen). Insect Sci Applic 17:221–225 (1997). 86 Forschler BT, Baiting Reticulitermes (Isoptera: Rhinotermitidae) field colonies with abamectin and zinc borate-treated cellulose in Georgia. Sociobiology 28:459–484 (1996). 87 Lax AR and Osbrink WLA, United States Department of Agriculture–Agriculture Research Service research on targeted management of the Formosan subterranean termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Pest Manag Sci 59:788–800 (2003). 88 Potter M, The changing face of termite control. PCT Mag 27:32–42 (1999). 89 Are you smarter than a termite researcher? PCT Mag 36:36–43 (2008). 90 Getty GM, Haverty MI, Coperen KA and Lewis VR, Response of Reticulitermes spp. (Isoptera: Rhinotermitidae) in Northern California to baiting with hexaflumuron with Sentricon termite colony elimination system. J Econ Entomol 93:1498–1507 (2000). 91 Foster BT, Cognato AI and Gold RE, Characterization of subterreanean termite populations as part of bait evalution, in Proc 4th Int Conf Pest Manag Sci (2014) 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 of Urban Pests, ed. by Robinson WH. Charleston, SC, pp. 335–340 (2002). Getty GM, Solek CW, Sbragia RJ, Haverty MI and Lewis VR, Large-scale suppression of a subterranean termite community using the Sentricon® termite colony elimination system: a case study in Chatsworth, California, USA. Sociobiology 50:1041–1050 (2007). Riegel C, Gilberg M, Freytag E, Su NY and Bordes ES, Long-term protection of Madame John’s legacy house from subterranean termites using hexaflumuron. Stud Conserv 50:267–274 (2005). Chen J and Henderson G, Determination of feeding preference of Formosan subterranean termite (Coptotermes formosanus Shiraki) for some amino acid additives. J Chem Ecol 22:2359–2369 (1996). Waller DA and Curtis AD, Effects of sugar-treated foods on preference and nitrogen fixation in Reticulitermes flavipes (Kollar) and Reticulitermes virginicus (Banks) (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 96:81–85 (2003). Swoboda LE, Miller DM, Fell RJ and Mullins DE, The effect of nutrient compounds (sugars and amino-acids) on bait consumption by Reticulitermes spp. (Isoptera: Rhinotermitidae). Sociobiology 44:547–563 (2004). Cornelius ML, Effect of bait supplements on the feeding and tunneling behavior of the Formosan subterranean termite (Isoptera: Rhinotermitidae), in Proc 5th Int Conf on Urban Pests, ed. by Lee C-Y and Robinson WH. Perniagaan, Malaysia, pp. 159–163 (2005). Haifig I, Costa-Leonardo AM and Marchetti FF, Effects of nutrients on feeding activities of the pest termite Heterotermes tenuis (Isoptera: Rhinotermitidae). J Appl Entomol 132:497–501 (2008). Saran RK and Rust MK, Phagostimulatory sugars enhance uptake and horizontal transfer of hexaflumuron in the Western Subterranean Termite (Isoptera: Rhinotermitidae). J Econ Entomol 101:873–879 (2008). Cornelius ML, Lyn M, Williams KS, Lovisa MP, De Lucca AJ and Lax AR, Efficacy of bait supplements for improving the rate of discovery of bait stations in the field by Formosan subterranean termites (Isoptera: Rhinotermitidae). J Econ Entomol 102:1175–1181 (2009). Wallace BA and Judd TM, A test of seasonal responses to sugars in four populations of the termite Reticulitermes flavipes. J Econ Entomol 103:2126–2131 (2010). Castillo VP, Sajap AS and Sahri MH, Feeding response of subterranean termites Coptotermes curvignathus and Coptotermes gestroi (Blattodea: Rhinotermitidae) to baits supplemented with sugars, amino acids, and cassava. J Econ Entomol 106:1794–1801 (2013). Bernklau EJ, Fromm EZ, Judd TM and Bjostad LB, Attraction of subterranean termites (Isoptera) to carbon dioxide. J Econ Entomol 98:476–484 (2005). Broadbent S, Farr M, Bernklau EJ, Siderhurst MS, James DM and Bjostad LB, Field attraction of termites to a carbon dioxide-generating bait in Australia (Isoptera). Sociobiology 48: 771–779 (2006). Jones SC, Targeted versus standard bait station placement affects subterranean termite (Isoptera: Rhinotermitidae) infestation rates. J Econ Entomol 96:1520–1525 (2003). Paysen ES, Zungoli PA, Benson EP and Demark JJ, Impact of auxiliary stations in a baiting program for subterranean termites (Isoptera: Rhinotermitidae). Fla Entomol 87:623–624 (2004). Glenn GJ, Austin JW and Gold RE, Efficacy of commercial termite baiting systems for management of subterranean termites (Isoptera: Rhinotermitidae) in Texas. Sociobiology 51:333–362 (2008). Smith J, Su NY and Ascobar NR, An areawide population management project for the invasive eastern subterranean termite (Isoptera: Rhinotermitidae) in a low-income community in Santiago, Chile. Am Entomol 52:253–260 (2006). Sukartana P, Sumarni G and Broadbent S, Evaluation of chlorfluazuron in controlling the subterranean termite Coptotermes curvignathus (Isoptera: Rhinotermitidae) in Indonesia. J Trop For Sci 21:13–18 (2009). Eggleton P, Williams PH and Gaston KJ, Explaining global termite diversity: productivity or history? Biodivers Conserv 3:318–330 (1994). Grassé PP, Termitologia, Tome 1: Anatomie, Physiologie, Reproduction des Termites. Masson, Paris, France (1982). Indrayani Y, Yoshimura T and Imamura Y, A novel control strategy for dry-wood termite Incisitermes minor infestation using a bait system. Wood Sci 54:220–224 (2008). © 2014 Society of Chemical Industry wileyonlinelibrary.com/journal/ps www.soci.org 113 Henderson G and Forschler BT, Termite bait screening using naturally-infested trees, in Proc 2nd Int Conf on Urban Pests, ed. by Wildey KB. Edinburgh, UK, pp. 449–460 (1996). 114 Wang Z, Guo J, Gong Y, Lu W, Lei A, Sun W et al., Control of dam termites with a monitor-controlling device. Sociobiology 50:1–9 (2007). 115 Lenz M and Evans TA, Termite bait technology: perspectives from Australia, in Proc 4th Int Conf on Urban Pests, ed. by Jones SC, Zhai J and Robertson WH. Charleston, SC, pp. 27–36 (2002). 116 Lee C-Y, Vongkaluang C and Lenz M, Challenges to subterranean termite management of multi-genera faunas in Southeast Asia and Australia. Sociobiology 50:213–221 (2007). 117 Atkinson TH, Smith MS and Williams RE, Control of structural infestations of Heterotermes aureus in Arizona with the Sentricon system. Down to Earth 53:18–26 (1998). 118 Gambetta A, Zaffagnini V and De Capua E, Use of hexaflumuron baits against subterranean termites for protection of historical and artistic structures: experiment carried out in selected test areas at the church of Santa Maria della Sanità in Naples. J Cult Herit 1:207–216 (2000). 119 Haverty MI, Tabuchi RL, Vargo EL, Cox DL, Nelson LJ and Lewis VR, Response of Reticulitermes hesperus (Isoptera: Rhinotermitidae) colonies to baiting with lufenuron in Northern California. J Econ Entomol 103:770–780 (2010). 120 Lee CY, Control of foraging colonies of subterranean termites, Coptotermes travians (Isoptera: Rhinotermitidae), in Malaysia using hexaflumuron baits. Sociobiology 39:411–416 (2002). 121 Matsuoka H, Tsunoda K, Yoshimura T and Takahashi M, Elimination of colonies of Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) and Reticulitermes speratus (Kolbe) (Isoptera: Rhinotermitidae) by bait system. Wood Res 85:84–86 (1998). 122 Mo J, Wang Z, Song X, Guo J, Gong Y, Lu W et al., Combination of ivermectin and a monitoring device for the control of Coptotermes formosanus (Isoptera: Rhinotermitidae) in the field. Sociobiology 48:1–10 (2006). 123 Neoh KB, Jalaludin NA and Lee CY, Elimination of field colonies of a mound-building termite Globitermes sulphureus (Isoptera: Termitidae) by bistrifluron bait. J Econ Entomol 104:607–613 (2011). 124 Sajap AS, Amit S and Welker J, Evaluation of hexaflumuron for controlling the subterranean termite Coptotermes curvignathus (Isoptera: Rhinotermitidae) in Malaysia. J Econ Entomol 93:429–433 (2000). 125 Sajap AS, Jaafar MA and Ouimette D, Above ground baiting for controlling the subterranean termites, Coptotermes travians (Isoptera: Rhinitermitidae), in Selangor Peninsular, Malaysia. Sociobiology 39:345–352 (2002). wileyonlinelibrary.com/journal/ps TA Evans, N Iqbal 126 Stansly PA, Su NY and Conner JM, Management of subterranean termites, Reticulitermes spp. (Isoptera: Rhinotermitidae), in a citrus orchard with hexaflumuron bait. Crop Prot 20:199–206 (2001). 127 Su NY and Hsu EL, Managing subterranean termite populations for protection of the historic Tzu-Su Temple of San-Shia, Taiwan (Isoptera: Rhinotermitidae). Sociobiology 41:529–545 (2003). 128 Su NY, Ban PM and Scheffrahn RH, Control of Coptotermes havilandi (Isoptera: Rhinotermitidae) with hexaflumuron baits and a sensor incorporated into a monitoring and baiting program. J Econ Entomol 93:415–421 (2000). 129 Su NY, Ban PM and Scheffrahn RH, Supression of foraging population of the Formosan subterranean termite (Isoptera: Rhinotermitidae) by field application of slow-acting toxicant bait. J Econ Entomol 84:1525–1531 (1991). 130 Su NY, Hillis-Starr Z, Ban PM and Scheffrahn RH, Protecting historic properties from subterranean termites: a case study with Fort Christiansvaern, Christiansted National Historic Site, United States, Virgin Islands. Am Entomol 49:20–32 (2003). 131 Su NY, Thomas JD and Scheffrahn RH, Elimination of subterranean termite populations from the Statue of Liberty national monument using a bait matrix containing an insect growth regulator, hexaflumuron. J Am Inst Cult Stud 37:282–292 (1998). 132 Verkerk RHJ and Bravery AF, A case study from the UK of possible successful eradication of Reticulitermes grassei. Final Workshop COST Action E22 on Environmental Optimisation of Wood Protection, Lisbon, Portugal (2004). 133 Weissling TJ and Thoms EM, Use of an acoustic emission detector for locating Formosan subterranean termite (Isoptera: Rhinotermitidaef ) feeding activity when installing and inspecting aboveground termite bait stations containing hexaflumuron. Fla Entomol 82:60–71 (1999). 134 Yates JR and Grace JK, Effective use of above ground hexaflumuron bait stations for Formosan subterranean termite control (Isoptera: Rhinotermitidae). Sociobiology 35:333–356 (2000). 135 Lenz M, Gleeson PV, Miller LR and Abbey HM, How predictive are laboratory experiments for assessing the effects of chitin synthesis inhibitors (CSI) on field colonies of termites? A comparison of laboratory and field data from Australian mound-building species of termite. International Research Group on Wood Preservation, Doc. IRG/WP 96-10143 (1996). 136 Ross MG, Responding to incursions of Australian subterranean termites in New Zealand. Proc 5th Int Conf on Urban Pests, ed. by Lee CY and Robinson WH. Perniagaan, Malaysia, pp. 233–238 (2005). © 2014 Society of Chemical Industry Pest Manag Sci (2014)