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Biology, Ecology, and Control
of Elaterid Beetles in
Agricultural Land∗
Michael Traugott,1,† Carly M. Benefer,2
Rod P. Blackshaw,2 Willem G. van Herk,3
and Robert S. Vernon3
1
Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck,
6020 Innsbruck, Austria; email: [email protected]
2
Plymouth University, Plymouth, Devon PL4 8AA, United Kingdom;
email: [email protected]
3
Pacific 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
October 17, 2014
wireworms, click beetles, Elateridae, pest management, agriculture
The Annual Review of Entomology is online at
ento.annualreviews.org
Abstract
This article’s doi:
10.1146/annurev-ento-010814-021035
∗
This paper was authored by employees of the
British Government as part of their official duties
and is therefore subject to Crown Copyright.
†
Corresponding author
Wireworms, the larvae of click beetles (Coleoptera: Elateridae), have had a
centuries-long role as major soil insect pests worldwide. With insecticidal
control options dwindling, research on click beetle biology and ecology is of
increasing importance in the development of new control tactics. Methodological improvements have deepened our understanding of how larvae and
adults spatially and temporarily utilize agricultural habitats and interact with
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 understanding 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 generation 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
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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, animals, 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 important 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 critically 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
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 Agriotes 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 Agriotes obscurus, Agriotes
sputator, and Agriotes 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 assessment. 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 considered 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
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
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e
h
c
i
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f
g
j
k
d
Figure 1
(a) Larva of Limonius 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, and Pseudanostirus species (49, 102) and 16S rDNA sequences
for Aeolus, Agriotes, Hypnoidus, Limonius, Melanotus, and Selatosomus species (13) are bar-coded. Such
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 bioluminescence (40, 91; see also the DELTA key of Elateriformia, http://delta-intkey.com/elateria/www/elat.htm, and the Tree of Life Web Project,
http://tolweb.org/Elateridae/9190, for further detailed information and references on click
beetle taxonomy). 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 American genera have recently been revised following new collections (3, 103), and there likely remain
other undescribed (and potential pest) species worldwide.
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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, and A. sputator. The focus on
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, Ctenicera, and Hypnoidus, 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).
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
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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
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
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Life Cycle Overview
Recently described elaterid life histories characterize Hapatesus hirtus (66), Conoderus rudis (130),
A. ustulatus (53, 54), and Agriotes sordidus (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 availability, 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 complicating 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,
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, and Conoderus 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 Limonius californicus 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
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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 (Agrypnus spp., Athous spp., Hemicrepidius spp.) species (158). This technique indicated that wireworms
exhibit intraspecific dietary preferences and that trophic plasticity can be considerable within phytophagous 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 proposed 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 wireworms 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◦ C in Agriotes species, 42, 55, 79), wireworms 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
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
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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 thereafter, 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 reported 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., Agriotes mancus, and Hypnoidus
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 wireworms include Cordyceps spp. (Cordycipitaceae), Tolypocladium spp. (Ophiocordycipitaceae), and
Zoophthora spp. (Entomophthoraceae) (78, 83, 104). Fungal pathogenicity is affected by wireworm
species (78), wireworm state, and environmental conditions: Mortality of A. obscurus larvae from
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
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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 Melanotus communis 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 crossreactions 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).
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
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 insects 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
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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 current 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 important 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
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) movement 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 trapping 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 powerful 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 interference (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
(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, increased 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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Annual Review of
Entomology
Volume 60, 2015
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Breaking Good: A Chemist Wanders into Entomology
John H. Law p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Multiorganismal Insects: Diversity and Function of
Resident Microorganisms
Angela E. Douglas p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p17
Crop Domestication and Its Impact on Naturally Selected
Trophic Interactions
Yolanda H. Chen, Rieta Gols, and Betty Benrey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p35
Insect Heat Shock Proteins During Stress and Diapause
Allison M. King and Thomas H. MacRae p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59
Termites as Targets and Models for Biotechnology
Michael E. Scharf p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p77
Small Is Beautiful: Features of the Smallest Insects and
Limits to Miniaturization
Alexey A. Polilov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 103
Insects in Fluctuating Thermal Environments
Hervé Colinet, Brent J. Sinclair, Philippe Vernon, and David Renault p p p p p p p p p p p p p p p p p 123
Developmental Mechanisms of Body Size and Wing-Body
Scaling in Insects
H. Frederik Nijhout and Viviane Callier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 141
Evolutionary Biology of Harvestmen (Arachnida, Opiliones)
Gonzalo Giribet and Prashant P. Sharma p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157
Chorion Genes: A Landscape of Their Evolution, Structure,
and Regulation
Argyris Papantonis, Luc Swevers, and Kostas Iatrou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Encyrtid Parasitoids of Soft Scale Insects: Biology, Behavior, and Their
Use in Biological Control
Apostolos Kapranas and Alejandro Tena p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 195
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Extrafloral Nectar at the Plant-Insect Interface: A Spotlight on Chemical
Ecology, Phenotypic Plasticity, and Food Webs
Martin Heil p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 213
Insect Response to Plant Defensive Protease Inhibitors
Keyan Zhu-Salzman and Rensen Zeng p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 233
Origin, Development, and Evolution of Butterfly Eyespots
Antónia Monteiro p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 253
Whitefly Parasitoids: Distribution, Life History,
Bionomics, and Utilization
Tong-Xian Liu, Philip A. Stansly, and Dan Gerling p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 273
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Recent Advances in the Integrative Nutrition of Arthropods
Stephen J. Simpson, Fiona J. Clissold, Mathieu Lihoreau, Fleur Ponton,
Shawn M. Wilder, and David Raubenheimer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 293
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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 313
Anopheles punctulatus Group: Evolution, Distribution, and Control
Nigel W. Beebe, Tanya Russell, Thomas R. Burkot, and Robert D. Cooper p p p p p p p p p p p p p p 335
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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
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 p p p p p p p p p p p p p p p p p p p p 373
Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations,
Interactions, and Ecological Implications
Alfred G. Wheeler Jr. and Billy A. Krimmel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 393
Honey Bee Toxicology
Reed M. Johnson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415
DNA Methylation in Social Insects: How Epigenetics Can Control
Behavior and Longevity
Hua Yan, Roberto Bonasio, Daniel F. Simola, Jürgen Liebig,
Shelley L. Berger, and Danny Reinberg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 435
Exaggerated Trait Growth in Insects
Laura Lavine, Hiroki Gotoh, Colin S. Brent, Ian Dworkin,
and Douglas J. Emlen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 453
viii
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Physiology of Environmental Adaptations and Resource Acquisition
in Cockroaches
Donald E. Mullins p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 473
Plant Responses to Insect Egg Deposition
Monika Hilker and Nina E. Fatouros p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 493
Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org
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Root-Feeding Insects and Their Interactions with Organisms
in the Rhizosphere
Scott N. Johnson and Sergio Rasmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517
Insecticide Resistance in Mosquitoes: Impact, Mechanisms, and Research
Directions
Nannan Liu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 537
Vector Ecology of Equine Piroplasmosis
Glen A. Scoles and Massaro W. Ueti p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
Trail Pheromones: An Integrative View of Their Role in Social Insect
Colony Organization
Tomer J. Czaczkes, Christoph Grüter, and Francis L.W. Ratnieks p p p p p p p p p p p p p p p p p p p p p p 581
Sirex Woodwasp: A Model for Evolving Management Paradigms of
Invasive Forest Pests
Bernard Slippers, Brett P. Hurley, and Michael J. Wingfield p p p p p p p p p p p p p p p p p p p p p p p p p p p p 601
Economic Value of Biological Control in Integrated Pest Management of
Managed Plant Systems
Steven E. Naranjo, Peter C. Ellsworth, and George B. Frisvold p p p p p p p p p p p p p p p p p p p p p p p p p 621
Indexes
Cumulative Index of Contributing Authors, Volumes 51–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p 647
Cumulative Index of Article Titles, Volumes 51–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 652
Errata
An online log of corrections to Annual Review of Entomology articles may be found at
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Annu. Rev. Entomol. 2015.60:313-334. Downloaded from www.annualreviews.org
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