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Biology, Ecology, and Control of Elaterid in Agricultural Land∗

Michael Traugott,1,† Carly M. Benefer,2 Rod P. Blackshaw,2 Willem G. van Herk,3 and Robert S. Vernon3

1Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, 6020 Innsbruck, Austria; email: [email protected] 2Plymouth University, Plymouth, Devon PL4 8AA, United Kingdom; email: [email protected] 3Pacific Agri-Food Research Center, Agriculture and Agri-Food Canada, Agassiz, British Columbia V0M 1A0, Canada; email: [email protected], [email protected]

Annu. Rev. Entomol. 2015. 60:313–34 Keywords First published online as a Review in Advance on wireworms, click beetles, Elateridae, pest management, agriculture October 17, 2014

The Annual Review of Entomology is online at Abstract ento.annualreviews.org Wireworms, the larvae of click beetles (Coleoptera: Elateridae), have had a This article’s doi: centuries-long role as major soil pests worldwide. With insecticidal 10.1146/annurev-ento-010814-021035 control options dwindling, research on click biology and ecology is of Access provided by University of Innsbruck on 01/07/15. For personal use only. ∗ Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org This paper was authored by employees of the increasing importance in the development of new control tactics. Method- British Government as part of their official duties and is therefore subject to Crown Copyright. ological improvements have deepened our understanding of how larvae and adults spatially and temporarily utilize agricultural habitats and interact with †Corresponding author their environment. This progress, however, rests with a few pest species, and efforts to obtain comparable knowledge on other economically important elaterids are crucial. There are still considerable gaps in our understand- ing of female and larval ecology; movement of elaterids within landscapes; and the impact of natural enemies, cultivation practices, and environmental change on elaterid population dynamics. This knowledge will allow gen- eration of multifaceted control strategies, including cultural, physical, and chemical measures, tailored toward species complexes and crops across a range of appropriate spatial scales.

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INTRODUCTION Click beetles (Coleoptera: Elateridae) are among the most diverse insect families, with nearly 10,000 described species. Elaterids are found worldwide in a range of habitats such as grasslands and forests, and their larvae, commonly called wireworms, dwell in soil, litter, or dead wood, where they feed on plants, , or decaying organic matter. Plant-eating wireworms are of particular agricultural importance: They are generalists, feeding on a large variety of crops, resulting in damage to seeds, roots, stems, and harvestable plant parts, which can facilitate secondary crop damage by pathogens (82). This reduces yields or crop value because of thinning, poor growth, cosmetic damage, or contamination at harvest (9, 111, 119, 164, 172). The complexity of elaterids as pests is unique, as they vary in species occurrence (e.g., up to 100 species economically impor- tant to potato occur in the Holarctic region alone; 172), abundance, and host preferences across the worldwide agricultural landscape, with arable fields often hosting one or more dominant or codominant pest or nonpest species (111, 118, 164, 172, 185). Their severity as pests is exacerbated by their unique subterranean larval life histories and the difficulties in sampling for wireworms, which hamper prediction of plant damage. Pestiferous click beetles are reemerging in importance because residues of effective insecticides are leaving arable land, and no-tillage farming, as well as set-aside schemes, might lead to reestablishment of populations (69). Besides directly affecting plants, root-feeding wireworms can affect multitrophic-level interactions (87, 180), including the interplay between belowground and aboveground herbivores via changing responses of plants to herbivores (4, 15), with important consequences for plants and higher-trophic-level biota (72, 73). Several hundred papers on economically important elaterids have been published to date, so complete coverage of the literature is beyond the scope of this review. Instead, current knowledge of the biology, ecology, and management of elaterids in agricultural land is synthesized and criti- cally discussed. We conclude by identifying research areas that will be important to advance our understanding of click beetles and their management in agricultural land.

SAMPLING OF WIREWORMS AND ADULT CLICK BEETLES There are currently three main methods of sampling used for infestation risk assessment: soil cores and bait traps for sampling wireworms directly from the soil, and sex pheromone traps for aboveground sampling of adult male click beetles (discussed in detail in 9, 111, 116, 155). Historically, soil cores have been used to estimate wireworm abundance, but this is labor intensive and prone to detection errors because of the high levels of aggregation in wireworm populations and seasonal variation in their vertical distribution (10, 124; but see 30 for a sequential sampling approach). Bait traps can be used to detect the presence of wireworms in bare fields before Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org planting crops, but because the range of the traps as well as species-specific movement ability and responses to variations in the soil environment is unknown, they do not give reliable estimates of abundance or subsequent crop damage (94, 109). Female-produced sex pheromones have been described for approximately 30 elaterids in North America, Europe, and Asia, mostly within the and Melanotus genera (155), and baits and traps have subsequently been developed to capture walking and flying adult male click beetles of several species in Europe and North America (116, 155). These traps were originally intended to be a surrogate for soil sampling, based on the assumption that aboveground adult populations are representative of those of their belowground larvae. However, robust evidence that these methods are useful for estimating populations is lacking, and there is substantial evidence that adult and larval spatial distributions are dissociated (12, 16, 64, 94). A single study has reported a relationship between captures of sex-pheromone-trapped Agriotes adult males and wireworms of the same species—though no data and/or statistics were presented (67).

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The range of attraction to sex pheromone traps is relatively low for , ,andAgriotes lineatus (5–20 m; 147), but as with belowground bait trapping, it is not known when and from where the trapped beetles have emerged. There are species-specific responses to the traps (64, 103, 173; though see 147), likely complicated by variation in individual movement behaviors as well as interactions with other abiotic factors (16, 103). Sampling scale influences observed patterns of adult and wireworm distribution, with inter- and intraspecific (temporal) differences in spatial pattern found between the landscape, field, site, and core scales (10, 17, 18) for Agriotes species. Sex pheromone traps are, however, a good tool to determine if a species is present in a landscape. In comparative studies pheromone traps have been shown to be useful research tools at a landscape scale (17, 25), though less so at the field scale (18). Interpreting both bait and sex pheromone trap counts as direct measures of population abundance requires caution: an issue that has been overlooked in many recent surveys (see Species Assemblages and Distribution in Arable Land). The differences observed between studies employing different sampling methodologies show that it is important to consider the species present as well as trap counts in infestation risk assess- ment. Using a combination of bait traps and soil cores to sample the damaging wireworm phase may improve detection of the full range of species present, including those not currently consid- ered pests but that have the potential to damage crops, and enable assessment of their distribution within and between fields before crop planting. Molecular identification methods (see Species Identification) will be important tools where morphology is ambiguous. Knowledge of abiotic factors associated with species distributions (12, 100, 141) could aid this process for species that have significant environmental preferences. Although pheromone traps can be useful in assessing the emergence and activity periods of adult males, their use in risk assessment remains unreliable, and further information is needed on species-specific male dispersal ability over different scales as well as female oviposition preferences in order to understand trap counts and link adult and larval populations.

SPECIES IDENTIFICATION

Identification Based on Morphological Characters Adult Elateridae are distinctive (Figure 1b), and species are relatively easy to distinguish using taxonomic keys, but although it is generally straightforward to separate wireworms by genus (Figure 1a), many (e.g., Agriotes and Melanotus species) are often impossible to differentiate at the species level, as important morphological characters can be ambiguous, particularly in early instar Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org larvae or where structures are worn or damaged. Several keys and descriptions exist for British (e.g., 159), European (e.g., 84), North American (e.g., 59), and Australian (e.g., 27) wireworms (see http://www.elateridae.com/ for a comprehensive list of literature, species lists, and online resources for Elateridae worldwide). However, considerable time and expertise are needed for reliable identification, and many North American larvae of economic importance have not yet been described (13 and references therein; 172).

Molecular Identification Because of the difficulty associated with morphological identification of elaterid larvae, molecular methods have been developed for a number of pest complexes in Europe and North America (see 11 for a detailed review of methods). In Europe the focus has been on Agriotes species, using terminal restriction fragment length polymorphism (45) and diagnostic multiplex polymerase

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a b e

h c i f

j g d k

Figure 1 (a)LarvaofLimonius canus.(b) L. canus adult. (c) Various elaterid species collected in British Columbia. (d ) Pupae and recently pupated Agriotes obscurus, a notable pest in Europe and North America. (e) A. obscurus beetles marked for release-recapture studies. ( f ) Mating A. obscurus.(g) Adult Alaus oculatus preparing for flight (image courtesy of Daniel Marlos, www.whatsthatbug.com). (h) Phorid pupa inside A. obscurus.(i ) Ectoparasite on A. obscurus larva. ( j ) Mermithid nematode emerging from A. obscurus larva (k) A. obscurus larvae infected with Metarhizium brunneum (image courtesy of Todd Kabaluk).

chain reaction (140). In North America, mitochondrial cytochrome c oxidase subunit I sequences for Aeolus, Agriotes, Ampedus, Athous, Conoderus, Dalopius, Hadromorphus, Hemicrepidius, Hypnoidus, Megapenthes, Melanotus, Metanomus,andPseudanostirus species (49, 102) and 16S rDNA sequences for Aeolus, Agriotes, Hypnoidus, , Melanotus,andSelatosomus species (13) are bar-coded. Such Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org approaches have made it feasible to investigate species distribution and diversity in agricultural land (141), though to date these techniques have rarely been applied to other potential pest genera found in mixed populations with Agriotes species (13, 141).

Taxonomy Elateridae systematics have been well studied at higher taxonomic levels, particularly in relation to evolution of characters such as (40, 91; see also the DELTA key of Elater- iformia, http://delta-intkey.com/elateria/www/elat.htm,andtheTreeofLifeWebProject, http://tolweb.org/Elateridae/9190, for further detailed information and references on ). Knowledge of fine-scale relationships within economically important genera, however, is lacking. More recently, as a result of the development of molecular identification techniques, DNA sequence data have been used to construct phylogenies of European (140) and

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North American (13, 102) pest species. There is high similarity between Agriotes proximus and A. lineatus sequences (179), and these two Agriotes species also have very similar female sex pheromone profiles, prompting questions regarding the status of these species. Some North Amer- ican genera have recently been revised following new collections (3, 103), and there likely remain other undescribed (and potential pest) species worldwide.

SPECIES ASSEMBLAGES AND DISTRIBUTION IN ARABLE LAND There is no global overview of elaterid distribution, with substantial zoogeographic understanding limited to countries (e.g., France, 101), provinces (e.g., Maritime Provinces of Canada, 103), and regions (e.g., western Black Sea Region of Turkey, 76; northern Europe, 134; East Asia, 154; East Transcaucasus, 2; Russian plain, 113). These studies are not primarily concerned with pest species. Studies of elaterid distributions in farmland consistently find mixed-species communities (Figure 1c). As would be expected, the communities vary geographically, with changes in species composition (94), but they also shift in species dominance within a range (108). There is some evidence that southern taxa are moving northward (101), suggesting that species complexes may change with time. In some parts of the world the fauna is also changing because of anthropogenic dispersal. For example, the nonnative A. lineatus and A. obscurus are now firmly established in western and eastern Canada (17, 164). Research papers from Europe indicate that crops there are attacked by fewer pest species than, for example, crops in North America. This is questionable. Historically, wireworm research in the United Kingdom has focused on Agriotes spp. because of the extensive survey carried out from 1939 to 1941 (106). Soil samples were collected from 15,877 fields, in contrast to more recent larval surveys that have used around 100 fields (12, 20, 112, 141), and it was concluded that there were three species of economic importance: A. lineatus, A. obscurus,andA. sputator.Thefocuson Agriotes species has been reinforced by the development of sex pheromones for Agriotes spp. (155), and most recent European surveys of elaterid distributions have been based on sex pheromone trapping (e.g., 24, 67, 145, 149). Thus, Agriotes spp. are defined as the main pest species, and the pheromones were developed for them and then used to survey elaterid pest species. This is circular and ignores other genera such as Athous, Conoderus, ,andHypnoidus, which are also pests (9, 39, 146, 151, 164, 172). When wireworm surveys that involve identification to the species level have been conducted in Europe, non-Agriotes species have been found (12, 20, 141, 158). Indeed, the 1939–1941 UK survey found 15 non-Agriotes species were present in nearly 50% of fields. One of these species, Corymbites cupreus (synonymous Ctenicera cuprea), has been shown to cause equivalent damage to Agriotes spp. (23). Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org The location of wireworms within a field is of prime concern for management. Like most soil fauna, they are patchily distributed (10, 18, 25, 131). Early researchers reported that wireworms were aggregated on three (field, plot, submeter) spatial scales (124), and, generally, they have been found to be either aggregated or randomly distributed (31, 100, 132, 184). These conclusions are based on statistical methods such as Taylor’s power law or Moran’s I; a geostatistical analysis of A. lineatus and A. obscurus showed them to have different spatial distributions even though they had identical mean:variance ratios (18), suggesting that parametric approaches are insufficient to fully describe spatial distributions. The size structure of populations differs between grassland and arable land, with relatively large proportions of small larvae in pasture and a more uniform distribution after cultivation (125). This situation arises because of direct mortality from cultivation, surface predation of exposed wireworms, and a failure to replenish with eggs (125). It has been estimated that five consecutive years of cultivation is sufficient to reduce populations below economically damaging

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numbers (121). The obverse of this is that minimum or conservation tillage practices will provide a physically stable habitat that continues to support high numbers, and this has been postulated as the explanation for an upsurge in wireworm damage in all-arable rotations (111).

DISPERSAL AND HABITAT SELECTION Both adults and larvae are capable of movement, but dispersal in its biological sense is restricted to the former. Wireworm movement is localized, and estimates of the horizontal distances traveled in soil are around 1 to 1.5 m, as determined by mark-release-recapture (MRR), such as for Melanotus okinawensis (7), or by comparing isotope ratios, such as for A. obscurus larvae (127). These distances are consistent with results from field experiments deploying trap crops (95, 142, 170). Some authors (127) have argued that wireworms will rarely move between crops as long as the soil environment is favorable (i.e., food is available and conspecific densities are low; 136), whereas a shift from peas (Pisum sativum) to adjacent potatoes (Solanum tuberosum) as the season progresses has been recorded (95). In addition to horizontal movement, there are seasonal vertical movements through the soil that appear to be largely driven by temperature (51, 55), at least in the spring. Wireworm counts tend to be lower in the summer (123) because they are further down the soil profile. For much of the last one hundred years or so, the focus for research has been on wireworms at a field scale because that is where the damage is seen. More recently, expansion of organic production, reduction in availability of insecticides, and development of ideas about area-wide management have resulted in increased interest in how these species interact with the environment at a landscape scale. A survey of A. lineatus and A. obscurus distributions over 950 ha of mixed farmland led to the conclusion that uncropped areas (field margins) were important population sources for invading nearby crops (17). This view has been reinforced in a study that related potato (S. tuberosum) damage caused by wireworms with landscape features and reported a significant correlation with grassy field margins (63). Understanding movement of adults between uncropped and cropped areas is a possible source of new management tactics. One question that has been addressed is how far individuals may move. These studies have tended to use some form of MRR (Figure 1e), of males and have provided minimum estimates for dispersal of 80 m for A. obscurus (129), 144 m for M. okinawensis (186), and 194 m for Melanotus sakishimensis (8). These figures almost certainly underestimate the dispersal power of adult elaterids, with one MRR study catching A. obscurus males more than 30 m into a field from the release point at a field margin in <19 h (19). When MRR was used to compare species’ responses to sex pheromone traps, it was concluded that A. lineatus moved farther than A. obscurus and A. sputator (64), providing an explanation for Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org observations in other field studies (18) and emphasizing the importance of differentiating between species in dispersal studies. A significant difference in pitfall trap catches of released male A. lineatus and A. obscurus has been shown in the field, and this is influenced by whether a crop is present or not (191). The evidence from mixed farming landscape studies is that adult Agriotes spp. males, at least, are widely distributed and can be trapped in fields where there are no detectable larval populations (12, 16). A limitation to many of these studies is that reliance on sex pheromone trapping provides data only on male behavior, whereas it is (ovipositing) females that are of interest. The limited data available for females (A. obscurus) suggest that they too disperse across farmland, albeit at lower numbers than males and earlier in the season (191). Although this may be true for other species that also have a long adult stage, it may not be the case for species such as Agriotes ustulatus and Agriotes litigiosus, which mate soon after emergence and complete oviposition within days (53, 55). Similarly, we do not know if females traversing fields oviposit. It has been suggested that

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oviposition sites are determined by soil density, vegetation, and moisture (42, 79, 88, 97), and this may be why fewer eggs are found in arable fields compared with grassland (60).

PHENOLOGY AND LIFE HISTORY

Life Cycle Overview Recently described elaterid life histories characterize Hapatesus hirtus (66), Conoderus rudis (130), A. ustulatus (53, 54), and (55). These reports, with older literature, indicate that elaterid life histories vary substantially between species, which is an important consideration for pest management given that several economic species usually coexist in agricultural fields (141, 172). The time required to complete development varies within species depending on food avail- ability, climatic conditions, and latitude and possibly genetic variation and sex (55, 79, 97, 164, 172), suggesting development in the field may be affected by cropping practices and difficult to model from laboratory studies. The number and development duration of larval instars vary between and within semivoltine species, sometimes considerably, but commonly seven to nine instars are completed over two to four years (84, 172). Many species pupate in late summer, with adults emerging when the soil reaches a threshold temperature the following spring, whereas others pupate in late spring or early summer, with adults emerging several weeks later (22, 53–55, 97). Some species complete development in one or two years; others take one year to develop and overwinter as larvae pupating in spring (185) (Figure 1d). Multivoltine species include C. rudis and Conoderus falli (130, 185), and those that overwinter as both larvae and adults cause overlapping broods (185), further com- plicating management. Several elaterids have parthenogenetic forms, and some mate only once (164, 172), whereas others can mate more often (53) (Figure 1f ). Mean fecundity ranges from <20 eggs in Melanotus caudex to >100 for most described species (79, 97, 115, 172), but estimates can vary widely between studies (164).

Activity Periods Larval activity periods differ with species, developmental stage, and environmental conditions. Assessing these from collection data alone is complicated by population changes due to pupation, molting cycles, seasonal vertical movements, and the sampling method employed (54, 68, 164, 172). Larvae of Holarctic semivoltine species generally have two (spring, early fall) activity periods per year, between which they burrow downward to avoid adverse soil conditions (22, 26, 68, 97, Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org 111). These seasonal movements largely coincide with their molting and feeding cycles, larvae typically only feeding for a brief part of each stadium, remaining quiescent some time before and after molting (54, 55, 189). However, wireworms in a feeding state will endure suboptimum soil conditions if food is present (164, 172). Peak larval activity periods are different for univoltine and bivoltine species, particularly when there are overlapping broods. In the southern United States, counts of some Conoderus spp. are greatest in summer and decline thereafter (29, 132). Adult activity periods vary depending on life histories. C. falli and C. rudis adults are caught throughout the year and may have multiple periods of peak abundance (36, 130). Overwintering adult beetles of semivoltine species are predominantly present in spring, with females typically emerging after males but living longer (22, 55, 79, 143). In some species activity levels are affected by time of day [e.g., they are greatest at night for A. obscurus, A. lineatus, A. sputator, Melanotus longulus,andConoderus vespertinus, (22, 115, 122, 144) and greatest during the day for A. ustulatus (53)], sex, or ability to fly (164). Flight (Figure 1g) may depend on a temperature threshold

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(33, 42) or sex [e.g., only males of Horistonotus uhlerii and Selatosomus destructor fly (150, 164), whereas in it is predominantly females that fly (133)] and increase as the season progresses (Aeolus mellillus, Limonius agonus) (164). Postmating longevity depends on temperature, food, natural enemies, and diseases (143, 160), but males of some species die shortly after mating (188). Indirect evidence on longevity of some species (e.g., 64) suggests that other species have prolonged adult stages (39, 115). The implications of elaterid activity periods for management are reviewed elsewhere (172).

FEEDING ECOLOGY Click beetles occurring in agricultural land occupy different trophic levels. Although the adults usually feed on plant material and hardly inflict crop damage (14, 39, 97), the larval stages can feed on plants, animals, or both. Stable isotope analysis has revealed that wireworm assemblages in arable land typically comprise phytophagous (Agriotes spp.) and carnivorous/omnivorous (Agryp- nus spp., Athous spp., Hemicrepidius spp.) species (158). This technique indicated that wireworms exhibit intraspecific dietary preferences and that trophic plasticity can be considerable within phy- tophagous species, including carnivorous specimens within their populations (158). Cannibalistic interactions and scavenging, reported for several plant-eating wireworm species (42, 54, 79, 97, 115), might explain this carnivorous feeding behavior. Soil organic matter (SOM) has been pro- posed as a food source for pestiferous wireworms (126), leading to the notion that plants are well protected from wireworm feeding in humus-rich and moist soils (97, 126). However, recent work could not corroborate Agriotes larvae feeding on SOM (157, 158), and early instar wireworms are not able to survive on it (54), raising doubts about the validity of this idea. Phytophagous wire- worms seem to be physiologically well adapted to cope with several months of food shortage (157), although early instar larvae can survive only a few days without living plant material (50, 54). When soil temperatures exceed a certain threshold (8–10◦CinAgriotes species, 42, 55, 79), wire- worms move upward from deeper layers in the soil and feed. Feeding ceases when soil conditions become inhospitable (126). In temperate climates two main feeding periods have been proposed: one in spring/early summer and one in late summer/autumn (see Phenology and Life History). However, work where plant feeding was tracked by molecular means suggests that Agriotes larvae are feeding throughout the whole vegetation period (181). The duration of the feeding phase is often longer in early instar larvae than in late instar

larvae, and this period is characterized by intense locomotor activity (39, 54, 189). CO2 emitted by belowground plant tissue attracts wireworms (38, 86) and is supposed to trigger an unspecific search response, leading click beetle larvae from food-depleted to food-rich areas (136). There is Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org no information on whether the behavioral response changes following exposure to a nonhost, but it is interesting to note the proposition that wireworms may be able to learn to avoid insecticides (167), which suggests that adaptive behaviors might be found. Other root volatiles and exudates are likely involved in fine-tuned decisions of phytophagous wireworms, allowing them to locate their preferred host plants (58), including probing of plant tissue by biting (74, 152). Root morphology and toughness were shown to affect wireworm food choice, with preferences for thin (46) and soft (71) roots. Wireworms will tunnel into hydrous tubers and roots, most likely to satisfy their need for water (97), explaining why both carnivorous and omnivorous wireworms can inflict crop damage. Phytophagous wireworms typically feed by masticating plant tissues with their mandibles, regurgitating amylase-containing fluids, and imbibing the liquefied products through a dense filter of branched hairs in the preoral cavity (43, 97). Agriotes larvae have a highly folded front gut, which should allow them to digest their nutrient-poor plant food more efficiently (97), but little is known about the digestive system in wireworms.

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Plants can differ markedly in their suitability as food for click beetle larvae (79, 81, 133) and adults (22), with primary and defensive plant compounds governing their attractiveness (28, 74). Agriotes larvae were found to have preferences for specific plants under field conditions, with seasonally changing levels of attractiveness (142, 181). Mesocosm experiments indicate that the dietary choice of Agriotes larvae is determined by plant-specific traits rather than root abundance (128, but see 135), with feeding preferences modulated by plant diversity. It has been suggested that the dietary requirements of wireworms change as the larvae grow (50), although there is little empirical evidence from field investigations (181).

PATHOGENS, NATURAL ENEMIES, AND BIOLOGICAL CONTROL

Bacteria Reports of bacterial diseases of wireworms recur in the literature (151). Wireworm pathogens include Pseudomonas fluorescens (89), Pseudomonas aeruginosa (190), Rahnella aquatilis, and various Bacillus spp., some of which may have potential for development into biocontrol agents (35, 92). These bacteria likely enter the wireworm midgut during molting and invade the hemocoel there- after, as crossing the intact integument is difficult and ingestion is obstructed by an oral filter (44, 190). Bacterial abundance and diversity may depend on wireworm feeding state and collection site (92, 187), and pathogenicity may depend on larval instar, soil moisture, and molting cycle (188, 190). An intracellular organism, Rickettsiella agriotidis, was recently isolated from a field-collected Agriotes sp. larva, although it is not yet known whether this bacterium is pathogenic to wireworms (85).

Fungi Mortality from Metarhizium anisopliae and Metarhizium brunneum (Clavicipitaceae) has been re- ported for many elaterid species (78) (Figure 1k), and under laboratory conditions these fungi can drastically reduce larval populations. Screening of pathogenic strains has led to promising isolates, and laboratory and field testing is underway to control various Agriotes species (6, 78, 99). Beauveria bassiana (Cordycipitaceae) has been isolated from Conoderus spp., ,andHypnoidus bicolor and tested on several Canadian Prairies species (78). Commercial formulations of B. bassiana are under investigation for control of Agriotes spp. (47, 93). Other reported fungi found on wire- worms include Cordyceps spp. (Cordycipitaceae), Tolypocladium spp. (Ophiocordycipitaceae), and Zoophthora spp. (Entomophthoraceae) (78, 83, 104). Fungal pathogenicity is affected by wireworm

Access provided by University of Innsbruck on 01/07/15. For personal use only. species (78), wireworm state, and environmental conditions: Mortality of A. obscurus larvae from Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org Metarhizium infection increases with both temperature and biomass and depends on wireworm feeding state (77, 161, 163). The efficacy of entomopathogenic fungi in controlling wireworms (L. californicus, H. bicolor) also depended on the application method and can be superior to seed insecticidal treatments (117).

Nematodes Mermithid nematodes (Hexameris spp., Complexomermis spp.) were found to infect both larval (Figure 1j) and adult elaterids, sterilizing the latter (39, 151), with infection rates of up to 10% in A. obscurus collected from low-lying, wet fields. Physical deterrents to infection such as the thick cuticular, biforate spiracles, and the densely haired preoral cavity may explain the limited effectiveness of steinernematid and heterorhabditid nematodes against wireworms (44). However, susceptibility depends on both wireworm species and nematode strain (6, 153). For example,

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the agriotos strain of Steinernema carpocapsae, isolated from A. lineatus, is effective against several wireworm species (34). Field applications of Steinernema spp. and Heterorhabditis bacteriophora reduced damage to corn (Zea mays) (6), but applications of S. feltiae did not reduce potato (S. tuberosum) damage from Agriotes spp. (47).

Parasitoids and Predators Wireworms from several genera (Agriotes, Aeolus, Agrypnus, Conoderus, Limonius, Melanotus) are known to be attacked by proctotrupid (Paracodrus spp., Phaenoserphus spp., Proctotrupes spp.), bethylid (Pristocera spp.), and ichneumonid (Anomalon spp.) hymenopteran exo- and endoparasitoids (39, 61, 105, 115, 146) (Figure 1i). Dipteran parasitoids of click beetle larvae include tachinids (Ateloglossa cinerea parasitizing Melanotus spp.; 146) and unidentified phorids (78) (Figure 1h). Parasitism rates in field-collected wireworms tend to be low: ranging from 2% to 6% in Agriotes larvae collected in western Siberia (39); ranging from 3% to 20% in Melanotus spp. larvae collected in Massachusetts (146); approximately 4% in larvae in southern Florida (61); and less than 1% in A. obscurus collected in Lancashire and Cheshire, United Kingdom (105). Comparatively little is known about predation on click beetles, although there is evidence that elaterids fall prey to generalist predators and that elaterid predation rates depend on the availability of other (pest) prey (178). Laboratory feeding experiments have shown that a broad range of adult carabids can overwhelm and consume wireworms of genera such as Agriotes, Athous, Limonius,and Selatosomus (39, 151). Results of serological tests on field-collected larvae and adults of carabid and staphylinid beetles were positive for elaterid proteins, indicating predation on elaterids (52). However, it is likely that this precipitin test was not specific to elaterid proteins and that cross- reactions with other prey that these generalist predators regularly consume (e.g., lumbricids, collembolans) occurred and thus that predation on elaterids was overestimated. Soil-dwelling dipteran larvae attacking wireworms include asilids (Leptogaster cylindrical attacking A. obscurus; 39) and larvae of Therevidae (Cyclotelus spp., Ozodiceromya spp., Thereva spp.; 115, 151, 166). Tyroglyphid mites were frequently found on various wireworm species (39, 151, 188) but generally do not kill the host. The role of wireworms themselves may be underestimated, as many species are cannibalistic and/or predatory, and the latter may reduce populations of pests, including other wireworms (120). Commonly mentioned noninvertebrate predators of elaterids are frogs, toads, moles, and birds (42, 151), with corvids aggregating at places with high wireworm densities (39). Access provided by University of Innsbruck on 01/07/15. For personal use only.

Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org CULTURAL, PHYSICAL, AND CHEMICAL MANAGEMENT The availability of effective management tools and strategies to prevent economic injury to crops from wireworm feeding has had an interesting history over the last century. In the first half of the 1900s, predating the synthetic insecticide era, management options included various cultural (e.g., cultivation, crop rotation, mulching, time of planting and harvest); physical (e.g., repellents, companion planting); and insecticidal methods, the latter including fumigants (e.g., chloropicrin, cyanides, carbon disulfide), soil amendments (e.g., arsenicals, mercury compounds, pyrethrum, rotenone), and seed treatments (151). These control activities were integrated pest management (IPM) programs guided by sampling approaches, and more than one control technique was often deployed (114, 151). Research in the last half of the 1900s, on the other hand, became somewhat polarized toward the study and widespread use of the highly effective organochlorine (OC), organophosphate (OP), and carbamate (CA) insecticides, applied prophylactically to soil, fertilizers, or seeds for current-season wireworm control (111, 172). Of these, the OCs (e.g.,

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aldrin and heptachlor) were of particular importance in that their long persistence and ability to kill wireworms in the soil for up to 13 years likely account for wireworms becoming a pest of low worldwide importance during that period (68, 111, 172, 183). Furthermore, it is thought that the present upsurge in wireworm populations is due in part to the gradual decline of OC residues to nontoxic levels following the global deregistration of the most persistent OCs in the 1970s and 1980s (68, 172) and the highly effective seed treatment lindane (i.e., on cereals and forages) in the early 2000s (111, 119). By the end of the last century, control of wireworms was mostly dependent on a dwindling arsenal of less persistent OPs and CAs, which have generally been considered less consistent and effective than OCs (62, 110). The attrition of the OCs, OPs, and CAs leading up to the present century has once again steered contemporary research in many countries toward the development of IPM programs reminiscent of those developed in the early 1900s, albeit with the availability of modern IPM control and sampling technologies. A number of wireworm management approaches are reviewed elsewhere (9, 119), but here we focus on key articles describing existing or envisioned tactics that we feel offer the greatest generic promise of control.

Chemical Controls The development of new insecticides for wireworm control since 2000 has focused largely on the pyrethroids (i.e., tefluthrin and bifenthrin), neonicotinoids (i.e., imidacloprid, clothianidin, and thiamethoxam), and a phenyl pyrazole (fipronil) (9, 90, 111, 119, 172). These insecticides have demonstrated effectiveness in reducing damage by wireworms to corn (Z. mays) and wheat (Triticum aestivum) (174, 175, 182), potatoes (S. tuberosum) (90, 176), and other crops (9), and registrations on these crops have been approved in many countries worldwide. However, in contrast to studies of the OCs, OPs, and CAs, which are known to kill wireworms (41, 96, 174), there is positive evidence that pyrethroids (which cause wireworm repulsion) and neonicotinoids (which cause reversible intoxication), while providing crop protection, do not cause significant mortality in the field (162, 168, 174, 176) and can vary in effectiveness between species (165). However, fipronil, which has a mode of action similar to that of the OCs [γ-aminobutyric acid (GABA)-gated chloride channel inhibition], is lethal to all wireworms tested and provides efficacy superior to that of the formerly used lindane seed treatment, but at far lower dosages (177). There are environmental concerns surrounding the neonicotinoids (37) and fipronil that may restrict or even prohibit their availability in many countries for wireworm control in the future, and as of yet effective alternatives have not been identified. As effective chemical options for in-season control of wireworms dwindle, and populations Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org in fields increase, a likely consequence will be a focus on controlling the adult stage to prevent oviposition in preferred crops, such as cereals and other grasses in farmed or even nonfarmed habitats (48, 172, 173). Significant reductions in click beetle populations in fields with cereals or other grassy crops have been demonstrated in the Netherlands, where pheromone traps were used to time sprays of Agriotes spp. beetles with pyrethroids (i.e., λ-cyhalothrin and deltamethrin) (48). Although spraying adults will not control existing wireworm populations in the soil, reductions in oviposition over consecutive years, along with one or more of the alternative methods cited below, could eventually reduce the risk of damage in heavily infested areas (172).

Cultural and Physical Methods Many cultural and physical methods for controlling wireworms and click beetles have been described at length in previous reviews that focus on (a) avoiding planting in infested fields;

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(b) establishing crop rotations that are unfavorable to oviposition and wireworm survivorship, along with associated cultural activities (e.g., weed control, fertilization, irrigation); (c) identifying optimal planting and harvest schedules; (d ) fallowing and cultivating at strategic times to kill the at various life stages; (e) protecting plantings with attractive companion crops; ( f ) increasing seeding rates and planting more tolerant cultivars; ( g) incorporating plants or extracts with allelochemical properties into soil for larval control; (h) field flooding; (i ) physical protection of crops; and ( j ) combinations of the above (5, 9, 56, 57, 90, 98, 111, 114, 119, 151, 169, 171, 172, 175). The efficacy of these methods is by no means generic, is often contradictory or inconsistent in the literature (5, 119, 151, 172), and must therefore be carefully tailored to the species complex and crops involved at regional or even field scales.

Semiochemical Methods A number of successful and unsuccessful attempts at reducing female oviposition via male mass trapping or using sex pheromones to cause mating confusion have been reported (116, 155, 172). The tactical and economic difficulties involved with these approaches when applied at the field scale have been pointed out (173), but many of these drawbacks are significantly reduced when such methods are directed at source wireworm populations concentrated in the nonfarmed grassy areas surrounding arable fields (17, 173). Because these areas typically cover only a fraction of the area of the arable fields they surround, they are potential and realistic target areas for click beetle reduction by semiochemical and other low-risk methods in chronic wireworm problem areas.

RESEARCH NEEDS The decline in the availability of insecticides for wireworm control leads to a short-term need for direct control options. For the longer-term sustainability of arable production, the research priorities should be directed toward reducing reliance on pesticides through the development of IPM. Molecular characterization of agrobiont elaterids needs to be expanded beyond the cur- rent limited range of species. This will permit researchers to address important topics such as (a) validation of morphologic wireworm keys and connecting larval with adult stages, (b) linking species to damage and characterizing their pest status, (c) tracking (larval) species composition and abundance over time, and (d ) applying population genetics to larval cohort composition. An im- portant task during future work will be to increase the level of our knowledge about non-Agriotes pest species to correspond with how much we already understand about the well-known species. The generation of species-specific data sets on elaterid communities will provide understanding Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org of click beetle ecology from the perspective of species’ traits and help to unravel how functional groups of elaterids respond to landscape features, cultivation practices, and insecticide usage. More detailed information is needed on the behavioral ecology of elaterids, specifically (a) how elaterids disperse; (b) the timing, frequency, and spatial scales of movement; (c) move- ment between uncropped and cropped areas; (d ) knowledge of biotic and abiotic factors driving dispersal, including the effect of management; (e) determining how males and females differ in their dispersal behavior; and ( f ) timing and location of mating and oviposition. Priority should be given to developing methods for the study of female behaviors. There is a need to extend the availability of sex pheromones to the full range of economically damaging species to better define their distributions. The development of lures for females is essential to ensure that our knowledge is not solely predicated upon studies on males. Such trap- ping systems are unlikely to deliver a useable surveillance method for IPM for most species, and there is a pressing need for a monitoring tool that will enable economically damaging wireworm

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populations to be identified. Attractive semiochemicals also create options for mass trapping and mating disruption. Future research should address the movement of wireworms in the soil profile in relation to parameters such as moisture, temperature, soil type, and food availability at the species level. Such information is available only for a minority of the economically important species and often refers to studies conducted in the first half of the twentieth century. As such, this awaits validation with contemporary work. Understanding which factors drive the vertical distribution of wireworms will allow development of predictive models (75, 100), guiding the timing of wireworm control measures mentioned above. Current knowledge of elaterid feeding ecology is rudimentary. Fortunately, a variety of pow- erful methods for analyzing trophic interactions are now at hand (156) to address (a) trophic level and trophic plasticity of economically important wireworm species across continental scales; (b) how environmental parameters such as soil conditions, plant community composition, and, in carnivorous wireworms, the availability of specific prey groups affect food choice; (c) how plant volatiles are utilized by larval and adult elaterids for finding and selecting host plants; and (d )the dietary needs and food choices of adults, especially females, in relation to longevity and fecundity. Such information will be important for new IPM tactics using push-pull approaches (32) and host plant resistance. The latter has been addressed for crops such as potato (e.g., 70), wheat (65), sugarcane (Saccharum spp.; 98), and sweet potato (Ipomoea batatas; 1), but more research is needed to identify the mechanisms of resistance (e.g., 70, 74) and to pinpoint those plant traits that are responsible for reduced wireworm susceptibility, guiding plant breeding efforts (107). Transgenic crops such as plants that express Bacillus thuringiensis Cry toxins (21) or allow for RNA interfer- ence (80) would provide a novel means to control agrobiont elaterids. A major challenge for these approaches will be their effectiveness against wireworm pest species complexes, which, at the same time, need to be pest specific to avoid nontarget effects. Biocontrol of elaterid beetles is also still in its infancy: Although inundative approaches such as the use of entomopathogenic nematodes and fungi have delivered promising results, there is scant published evidence that they will work outside controlled laboratory environments (but see 117). Hardly anything is known about how natural enemies, such as invertebrate predators, affect elaterid populations, and conservation biocontrol approaches have not been explored. The successful establishment of European and South American click beetles as pests in North America provides an opportunity to test the enemy release hypothesis, and the results may be relevant to future introductions of other nonnative click beetles. Climate change will have an impact on elaterid distribution and abundance on agricultural land, with the primary variables of importance being temperature and moisture, potentially affecting Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org (a) species distribution and abundance, (b) phenologies and population dynamics, (c) susceptibility of plants to wireworm damage, and (d ) efficacy of measures to control elaterids. For example, in- creased summer rainfall has been shown to enhance the abundance of A. lineatus larvae in grassland (137), whereas under summer drought, plant-mediated effects of wireworms on foliar herbivores depended on plant and insect identity (138, 139). Such impacts are likely to have differential effects on species ranges. Moreover, the impact of root-feeding wireworms on plants depends on plant nutrition and is affected by the density of both conspecifics and other root herbivores (46). These findings indicate that predicting the effects of a changing climate on agrobiont elaterid beetles will not be straightforward and that the responses are governed by the species’ biology and the ecological network they are embedded in. Improving our knowledge in these areas will thus be crucial for model-based predictions of climate change on agrobiont elaterids (148). The future success of elaterid control will rely on rational decision making with the knowledge of anticipated damage arising from an accurate determination of click beetle populations. There

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will be a reduced reliance on insecticides, pointing to the need to integrate click beetle management at the field and landscape levels based on detailed knowledge of click beetle biology and ecology.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

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164. van Herk WG, Vernon RS. 2014. Click beetles and wireworms (Coleoptera: Elateridae) of 164. Lists elaterid Alberta, Saskatchewan, and Manitoba. In of Canadian Grasslands,Vol.4:Biodiversity species of the Canadian and Systematics Part 2, ed. DJ Giberson, HA Carcamo,´ pp. 87–117. Ottawa, Canada: Biol. Surv. Prairies and describes Can. life histories of several 165. van Herk WG, Vernon RS, Clodius M, Harding C, Tolman JH. 2007. Mortality of five wireworm species key species. (Coleoptera: Elateridae), following topical application of clothianidin and chlorpyrifos. J. Entomol. Soc. B. C. 104:55–63 166. van Herk WG, Vernon RS, Cronin EML, Gaimari SD. 2014. Predation of Thereva nobilitata (Fabricius) (Diptera: Therevidae) on Agriotes obscurus L. (Coleoptera: Elateridae). J. Appl. Entomol. In press. doi: 10.1111/jen.12162 167. van Herk WG, Vernon RS, Harding C, Roitberg BD, Gries G. 2010. Possible aversion learning in the Pacific Coast wireworm. Phys. Entomol. 35:19–28 168. van Herk WG, Vernon RS, McGinnis S. 2013. Response of the dusky wireworm, Agriotes obscurus (Coleoptera: Elateridae), to residual levels of bifenthrin in field soil. J. Pest Sci. 86:125–36 169. Vernon RS. 2005. Aggregation and mortality of Agriotes obscurus (Coleoptera: Elateridae) at insecticide- treated trap crops of wheat. J. Econ. Entomol. 98:1999–2005 170. Vernon RS, Kabaluk T, Behringer A. 2000. Movement of Agriotes obscurus (Coleoptera: Elateridae) in strawberry (Rosaceae) plantings with wheat (Graminae) as a trap crop. Can. Entomol. 132:231–41 171. Vernon RS, van Herk WG. 2013. Physical exclusion of adult click beetles from wheat with an exclusion trench. J. Pest Sci. 86:77–83 172. Vernon RS, van Herk WG. 2013. Wireworms as pests of potato. In Insect Pests of Potato: Global 172. Extensive review of Perspectives on Biology and Management, ed. P Giordanengo, C Vincent, A Alyokhin, pp. 103–64. ecology and Amsterdam: Academic management of 173. Vernon RS, van Herk WG, Blackshaw RP, Shimizu Y, Clodius M. 2014. Mark–recapture of Agriotes wireworm pests of obscurus and Agriotes lineatus with dense arrays of pheromone traps in an undisturbed grassland population potatoes in the Holarctic. reservoir. Agric. For. Entomol. 16:217–26 174. Vernon RS, van Herk WG, Clodius M, Harding C. 2009. Wireworm management I: stand protection versus wireworm mortality with wheat seed treatments. J. Econ. Entomol. 102:2126–36 175. Vernon RS, van Herk WG, Clodius M, Harding C. 2013. Crop protection and mortality of Agriotes obscurus wireworms with blended insecticidal wheat seed treatments. J. Pest Sci. 86:137–50 176. Vernon RS, van Herk WG, Clodius M, Harding C. 2013. Further studies on wireworm management in Canada: damage protection versus wireworm mortality in potatoes. J. Econ. Entomol. 106:786–99 177. Vernon RS, van Herk WG, Tolman JH, Ortiz Saavedra H, Clodius M, Gage B. 2008. Transitional sublethal and lethal effects of insecticides after dermal exposures to five economic species of wireworms (Coleoptera: Elateridae). J. Econ. Entomol. 101:365–74 178. von Berg K, Thies C, Tscharntke T, Scheu S. 2009. Cereal aphid control by generalist predators in pres- ence of belowground alternative prey: complementary predation as affected by prey density. Pedobiologia 53:41–48 Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org 179. Vuts J, Tolasch T, Furlan L, Balintn´ eCsonka´ E,´ Felfoldi¨ T, et al. 2012. Agriotes proximus and A. lineatus (Coleoptera: Elateridae): a comparative study on the pheromone composition and cytochrome c oxidase subunit I gene sequence. Chemoecology 22:23–28 180. Wackers¨ FL, Bezemer TM. 2003. Root herbivory induces an above-ground indirect defence. Ecol. Lett. 6:9–12 181. Wallinger C, Staudacher K, Schallhart N, Mitterrutzner E, Steiner E-M, et al. 2014. How generalist herbivores exploit belowground plant diversity in temperate grasslands. Mol. Ecol. 23:3826–37 182. Wilde G, Roozeboom K, Claasen M, Janssen K, Witt M. 2004. Seed treatment for control of early-season pests of corn and its effect on yield. J. Agric. Urban Entomol. 21:75–85 183. Wilkinson ATS, Finlayson DG, Morley HV. 1964. Toxic residues in soil 9 years after treatment with aldrin and heptachlor. Science 143:681–83 184. Williams L, Schotzko DJ, McCaffrey JP. 1992. Geostatistical description of the spatial distribution of Limonius californicus (Coleoptera, Elateridae) wireworms in the northwestern United States with com- ments on sampling. Environ. Entomol. 21:983–95

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185. Willis RB, Abney MR, Kennedy GG. 2010. Survey of wireworms (Coleoptera: Elateridae) in North Carolina sweet potato fields and seasonal abundance of Conoderus vespertinus. J. Econ. Entomol. 103:1268– 76 186. Yamamura K, Kishita M, Arakaki N, Kawamura F, Sadoyama Y. 2003. Estimation of the dispersal distance by mark-recapture experiments using traps: correction of bias caused by the artificial removal by traps. Popul. Ecol. 45:149–55 187. Yoshida M, Yoshii M. 1959. Researches on the wireworm Melanotus caudex Lewis: XIV. On the bacteria living in the body of the wireworm. Jpn. J. Appl. Entomol. Zool. 3:190–94 188. Zacharuk RY. 1962. Distribution, habits, and development of Ctenicera destructor (Brown) in western Canada, with notes on the related species C. aeripennis (Kby.) (Coleoptera: Elateridae). Can. J. Zool. 40:539–52 189. Zacharuk RY. 1962. Seasonal behavior of larvae of Ctenicera spp. and other wireworms (Coleoptera: Elateridae), in relation to temperature, moisture, food and gravity. Can. J. Zool. 40:697–718 190. Zacharuk RY. 1973. Penetration of the cuticular layers of elaterid larvae (Coleoptera) by the fungus Metarhizium anisopliae, and notes on a bacterial invasion. J. Invertebr. Pathol. 21:101–6 191. Zuur AF, Blackshaw RP, Vernon RS, Thiebaud F, Ieno EN. 2012. Analysis of zero inflated click-beetle data. In Zero Inflated Models and Generalized Mixed Models with R, ed. AF Zuur, AA Saveliev, EN Ieno, pp. 257–76. Newburgh, UK: Highl. Stat. Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org

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Annual Review of Entomology Contents Volume 60, 2015

Breaking Good: A Chemist Wanders into Entomology John H. Law pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Multiorganismal Insects: Diversity and Function of Resident Microorganisms Angela E. Douglas ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp17 Crop Domestication and Its Impact on Naturally Selected Trophic Interactions Yolanda H. Chen, Rieta Gols, and Betty Benrey ppppppppppppppppppppppppppppppppppppppppppppp35 Insect Heat Shock Proteins During Stress and Diapause Allison M. King and Thomas H. MacRae pppppppppppppppppppppppppppppppppppppppppppppppppppp59 Termites as Targets and Models for Biotechnology Michael E. Scharf ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp77 Small Is Beautiful: Features of the Smallest Insects and Limits to Miniaturization Alexey A. Polilov ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp103 Insects in Fluctuating Thermal Environments Herv´e Colinet, Brent J. Sinclair, Philippe Vernon, and David Renault ppppppppppppppppp123 Developmental Mechanisms of Body Size and Wing-Body Scaling in Insects

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Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org H. Frederik Nijhout and Viviane Callier 141 Evolutionary Biology of Harvestmen (Arachnida, Opiliones) Gonzalo Giribet and Prashant P. Sharma ppppppppppppppppppppppppppppppppppppppppppppppppp157 Chorion Genes: A Landscape of Their Evolution, Structure, and Regulation Argyris Papantonis, Luc Swevers, and Kostas Iatrou pppppppppppppppppppppppppppppppppppppp177 Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and Their Use in Biological Control Apostolos Kapranas and Alejandro Tena ppppppppppppppppppppppppppppppppppppppppppppppppppp195

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Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical Ecology, Phenotypic Plasticity, and Food Webs Martin Heil pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp213 Insect Response to Plant Defensive Protease Inhibitors Keyan Zhu-Salzman and Rensen Zeng pppppppppppppppppppppppppppppppppppppppppppppppppppp233 Origin, Development, and Evolution of Butterfly Eyespots Ant´onia Monteiro pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp253 Whitefly Parasitoids: Distribution, Life History, Bionomics, and Utilization Tong-Xian Liu, Philip A. Stansly, and Dan Gerling ppppppppppppppppppppppppppppppppppppp273 Recent Advances in the Integrative Nutrition of Arthropods Stephen J. Simpson, Fiona J. Clissold, Mathieu Lihoreau, Fleur Ponton, Shawn M. Wilder, and David Raubenheimer pppppppppppppppppppppppppppppppppppppppppp293 Biology, Ecology, and Control of Elaterid Beetles in Agricultural Land Michael Traugott, Carly M. Benefer, Rod P. Blackshaw, Willem G. van Herk, and Robert S. Vernon ppppppppppppppppppppppppppppppppppppppppppp313 Anopheles punctulatus Group: Evolution, Distribution, and Control Nigel W. Beebe, Tanya Russell, Thomas R. Burkot, and Robert D. Cooper pppppppppppppp335 Adenotrophic Viviparity in Tsetse Flies: Potential for Population Control and as an Insect Model for Lactation Joshua B. Benoit, Geoffrey M. Attardo, Aaron A. Baumann, Veronika Michalkova, and Serap Aksoy ppppppppppppppppppppppppppppppppppppppppppppppppp351 Bionomics of Temperate and Tropical Culicoides Midges: Knowledge Gaps and Consequences for Transmission of Culicoides-Borne Viruses B.V. Purse, S. Carpenter, G.J. Venter, G. Bellis, and B.A. Mullens pppppppppppppppppppp373 Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations, Interactions, and Ecological Implications Alfred G. Wheeler Jr. and Billy A. Krimmel pppppppppppppppppppppppppppppppppppppppppppppp393 Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org Honey Bee Toxicology Reed M. Johnson ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp415 DNA Methylation in Social Insects: How Epigenetics Can Control Behavior and Longevity Hua Yan, Roberto Bonasio, Daniel F. Simola, J¨urgen Liebig, Shelley L. Berger, and Danny Reinberg ppppppppppppppppppppppppppppppppppppppppppppppppp435 Exaggerated Trait Growth in Insects Laura Lavine, Hiroki Gotoh, Colin S. Brent, Ian Dworkin, and Douglas J. Emlen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp453

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Physiology of Environmental Adaptations and Resource Acquisition in Cockroaches Donald E. Mullins ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp473 Plant Responses to Insect Egg Deposition Monika Hilker and Nina E. Fatouros pppppppppppppppppppppppppppppppppppppppppppppppppppppp493 Root-Feeding Insects and Their Interactions with Organisms in the Rhizosphere Scott N. Johnson and Sergio Rasmann ppppppppppppppppppppppppppppppppppppppppppppppppppppp517 Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research Directions Nannan Liu pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp537 Vector Ecology of Equine Piroplasmosis Glen A. Scoles and Massaro W. Ueti ppppppppppppppppppppppppppppppppppppppppppppppppppppppp561 Trail Pheromones: An Integrative View of Their Role in Social Insect Colony Organization Tomer J. Czaczkes, Christoph Gr¨uter, and Francis L.W. Ratnieks pppppppppppppppppppppp581 Sirex Woodwasp: A Model for Evolving Management Paradigms of Invasive Forest Pests Bernard Slippers, Brett P. Hurley, and Michael J. Wingfield pppppppppppppppppppppppppppp601 Economic Value of Biological Control in Integrated Pest Management of Managed Plant Systems Steven E. Naranjo, Peter C. Ellsworth, and George B. Frisvold ppppppppppppppppppppppppp621

Indexes

Cumulative Index of Contributing Authors, Volumes 51–60 ppppppppppppppppppppppppppp647 Cumulative Index of Article Titles, Volumes 51–60 ppppppppppppppppppppppppppppppppppppp652 Access provided by University of Innsbruck on 01/07/15. For personal use only. Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org Errata

An online log of corrections to Annual Review of Entomology articles may be found at http://www.annualreviews.org/errata/ento

Contents ix Annual Reviews It’s about time. Your time. It’s time well spent.

New From Annual Reviews: Annual Review of Statistics and Its Application Volume 1 • Online January 2014 • http://statistics.annualreviews.org Editor: Stephen E. Fienberg, Carnegie Mellon University Associate Editors: Nancy Reid, University of Toronto Stephen M. Stigler, University of Chicago The Annual Review of Statistics and Its Application aims to inform statisticians and quantitative methodologists, as well as all scientists and users of statistics about major methodological advances and the computational tools that allow for their implementation. It will include developments in the field of statistics, including theoretical statistical underpinnings of new methodology, as well as developments in specific application domains such as biostatistics and bioinformatics, economics, machine learning, psychology, sociology, and aspects of the physical sciences. Complimentary online access to the first volume will be available until January 2015.

table of contents: • What Is Statistics? Stephen E. Fienberg • High-Dimensional Statistics with a View Toward Applications • A Systematic Statistical Approach to Evaluating Evidence in Biology, Peter Bühlmann, Markus Kalisch, Lukas Meier from Observational Studies, David Madigan, Paul E. Stang, • Next-Generation Statistical Genetics: Modeling, Penalization, Jesse A. Berlin, Martijn Schuemie, J. Marc Overhage, and Optimization in High-Dimensional Data, Kenneth Lange, Marc A. Suchard, Bill Dumouchel, Abraham G. Hartzema, Jeanette C. Papp, Janet S. Sinsheimer, Eric M. Sobel Patrick B. Ryan • Breaking Bad: Two Decades of Life-Course Data Analysis • The Role of Statistics in the Discovery of a Higgs Boson, in Criminology, Developmental Psychology, and Beyond, David A. van Dyk Elena A. Erosheva, Ross L. Matsueda, Donatello Telesca • Brain Imaging Analysis, F. DuBois Bowman • Event History Analysis, Niels Keiding • Statistics and Climate, Peter Guttorp • Statistical Evaluation of Forensic DNA Profile Evidence, • Climate Simulators and Climate Projections, Christopher D. Steele, David J. Balding Jonathan Rougier, Michael Goldstein • Using League Table Rankings in Public Policy Formation: • Probabilistic Forecasting, Tilmann Gneiting, Statistical Issues, Harvey Goldstein Matthias Katzfuss • Statistical Ecology, Ruth King Access provided by University of Innsbruck on 01/07/15. For personal use only.

Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org • Bayesian Computational Tools, Christian P. Robert • Estimating the Number of Species in Microbial Diversity • Bayesian Computation Via Markov Chain Monte Carlo, Studies, John Bunge, Amy Willis, Fiona Walsh Radu V. Craiu, Jeffrey S. Rosenthal • Dynamic Treatment Regimes, Bibhas Chakraborty, • Build, Compute, Critique, Repeat: Data Analysis with Latent Susan A. Murphy Variable Models, David M. Blei • Statistics and Related Topics in Single-Molecule Biophysics, • Structured Regularizers for High-Dimensional Problems: Hong Qian, S.C. Kou Statistical and Computational Issues, Martin J. Wainwright • Statistics and Quantitative Risk Management for Banking and Insurance, Paul Embrechts, Marius Hofert

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