insects

Review
A Review of Sampling and Monitoring Methods for
Beneficial Arthropods in Agroecosystems
Kenneth W. McCravy
Department of Biological Sciences, Western Illinois University, 1 University Circle, Macomb, IL 61455, USA;
[email protected]; Tel.: +1-309-298-2160




Received: 12 September 2018; Accepted: 19 November 2018; Published: 23 November 2018


Abstract: Beneficial arthropods provide many important ecosystem services. In agroecosystems,

pollination and control of crop pests provide benefits worth billions of dollars annually. Effective
sampling and monitoring of these beneficial arthropods is essential for ensuring their short- and
long-term viability and effectiveness. There are numerous methods available for sampling beneficial
arthropods in a variety of habitats, and these methods can vary in efficiency and effectiveness. In this
paper I review active and passive sampling methods for non-Apis bees and arthropod natural enemies
of agricultural pests, including methods for sampling flying insects, arthropods on vegetation and in
soil and litter environments, and estimation of predation and parasitism rates. Sample sizes, lethal
sampling, and the potential usefulness of bycatch are also discussed.

Keywords: sampling methodology; bee monitoring; beneficial arthropods; natural enemy monitoring;
vane traps; Malaise traps; bowl traps; pitfall traps; insect netting; epigeic arthropod sampling

1. Introduction
To sustainably use the Earth’s resources for our benefit, it is essential that we understand the
ecology of human-altered systems and the organisms that inhabit them. Agroecosystems include
agricultural activities plus living and nonliving components that interact with these activities in a
variety of ways. Beneficial arthropods, such as pollinators of crops and natural enemies of arthropod
pests and weeds, play important roles in the economic and ecological success of agroecosystems.
These arthropod-mediated ecosystem services (AMES) increase agroecosystem productivity and
sustainability by enhancing crop yields and reducing reliance on pesticides. The annual combined
value of pollination services by non-Apis bees and pest control provided by insect predators and
parasitoids has been estimated at $7.5 billion annually in the USA [1].
Land use practices can have adverse effects on these beneficial arthropods. Intensive agriculture
can negatively affect bee diversity and pollination, and there is evidence of causal connections between
decline of pollinators and decline of plants to which they are functionally linked [2]. Such adverse
effects can be mitigated if undisturbed pollinator habitat is available [3,4]. Likewise, agroecosystems
are often unfavorable environments for arthropod natural enemies of agricultural pests, but efforts
such as habitat enhancement to conserve these natural enemies can provide important control of these
pests [5]. For bees and natural enemies of insect pests, the ability to effectively assess and monitor their
abundance and diversity, and potential effects of land use practices on them, is of vital importance.
A variety of sampling methods is available, but these methods can be biased and vary widely in
performance [6–11]. Some may provide absolute estimates of abundance (density, or numbers per
unit area), but most provide relative estimates that are related to the sampling method being used
(e.g., numbers per trap per day, numbers per hour of aerial netting, etc.). In this paper I present a brief
overview of these beneficial arthropods and their importance, and some general concerns in regard
to sampling and monitoring of these organisms. I then review the major sampling and monitoring

Insects 2018, 9, 170; doi:10.3390/insects9040170 www.mdpi.com/journal/insects

 Insects
Insects 2018,
2018, 9,9,
170x FOR PEER REVIEW 2 2ofof
2726

importance, and some general concerns in regard to sampling and monitoring of these organisms. I
then review
methods the major
employed sampling
to assess theseand monitoring
organisms, and methods employed
the advantages andto assess these
limitations organisms,
of these and
methods.
Itthe advantages
is hoped that thisand limitations
paper of these
will provide methods.and
entomologists It crop
is hoped that specialists
protection this paperwith
willa provide
useful
entomologists
overview and crop
of sampling protection
methods specialists
available and with a useful overview
will encourage of sampling
awareness methods
and further available
research and
and will encourage
conservation of theseawareness
important and further research and conservation of these important arthropods.
arthropods.

2.2.Non-Apis
Non-ApisBees
Bees
The
Thetotal
totalvalue
valueofofpollination
pollinationservices
servicesworldwide
worldwidehas hasbeen
beenestimated
estimated atat$217$217billion
billion [12].
[12].
Approximately 78 to 94% of
Approximately 78 to 94% of flowering flowering plants, and most major agricultural crops, are
and most major agricultural crops, are pollinated by pollinated
by animals,
animals, withwith
beesbees being
being the predominant
the predominant pollinating
pollinating taxontaxon [1,4,13].
[1,4,13]. While managed
While managed honey bee honey
(Apis
bee
mellifera mellifera
(Apis L.) hives L.)
are hives
used inaremuch
usedofinthe
much of the
world, world, availability
availability of these hives of is
these hives
limited in is limited
many in
regions
many regions [14,15]. Honey bees are the most commonly used pollinators in
[14,15]. Honey bees are the most commonly used pollinators in large-scale commercial agriculture, large-scale commercial
agriculture,
but non-Apis butbees
non-Apis bees
(Figure 1) (Figure
are also1)important
are also important in crop pollination,
in crop pollination, especially especially
in more in more
complex
complex agroecosystems
agroecosystems and diverseand landscapes
diverse landscapes
[16]. In the [16].
USA,In non-Apis
the USA,beesnon-Apis beesalmost
comprise comprise 25%almost
of crop
25% of crop pollination,
pollination, at a value at a value estimated
estimated at $3.07
at $3.07 billion billion annually
annually [1]. High[1]. High diversity
diversity of bees canof bees can
enhance
enhance
pollinatorpollinator
functionalfunctional complimentarity
complimentarity and ensure
and ensure pollination
pollination function
function [17–19].
[17–19]. Pollination
Pollination can
can contribute to the nutritional value, shelf life, and quality of food crops
contribute to the nutritional value, shelf life, and quality of food crops as well [20,21]. as well [20,21].
Some
Somestudies
studies have
havedocumented
documented declines
declinesof non-Apis
of non-Apis beesbees
in specific geographic
in specific geographiclocations [22–24],
locations [22–
but
24],large-scale, long-term,
but large-scale, and statistically
long-term, robust monitoring
and statistically programs that
robust monitoring yield data
programs thaton population
yield data on
changes are badly
population changesneeded. To document
are badly needed. To future changesfuture
document in beechanges
diversity inand
bee evaluate
diversitytheand effectiveness
evaluate the
ofeffectiveness
mitigation efforts, reliable
of mitigation sampling
efforts, methods
reliable samplingare methods
required.are A required.
variety ofAmethods
variety ofare available
methods are
for sampling
available forbees, including
sampling passive trapping
bees, including passive and activeand
trapping netting.
active Much ofMuch
netting. our knowledge of the
of our knowledge
effectiveness of theseof
of the effectiveness methods has beenhas
these methods obtained in nonagricultural
been obtained environments.
in nonagricultural A review
environments. A of bee
review
sampling methodology
of bee sampling with a focus
methodology with aonfocus
tropical forests forests
on tropical and agroecosystems
and agroecosystems is available [25], as[25],
is available is
a as
frequently updated compendium of practical information on bee biology,
is a frequently updated compendium of practical information on bee biology, collection, collection, processing,
identification, and curation [26].
processing, identification, and curation [26].

(a) (b)

(c) (d)
Figure1.1.Some
Figure Some economically
economically important
important non-Apis
non-Apis bees: (a) (a) Blue
Blue orchard
orchard bee, Osmia lignaria
bee, Osmia lignariaSay,
Say, a
a common
commonorchard
orchardpollinator;
pollinator;(b)(b)southeastern
southeastern blueberry
blueberry bee,
bee, Habropoda
Habropoda laboriosa
laboriosa (Fabricius),
(Fabricius), an
an early
early spring
spring pollinator
pollinator of rabbit-eye
of rabbit-eye blueberry,
blueberry, Vaccinium
Vaccinium virgatum
virgatum Aiton;
Aiton; Peponapispruinosa
(c)(c)Peponapis pruinosaSay,
Say, a
a pollinator
pollinator of Cucurbitaspp.;
ofCucurbita spp.;and
and(d)(d)the
theorchid
orchidbeebee Eulaema
Eulaema mocsaryi
mocsaryi Friese,
Friese, a pollinator
a pollinator of Brazil
of Brazil nut,
nut, Bertholletia
Bertholletia excelsa
excelsa Humb.
Humb. & Bonpl.
& Bonpl. Attributions:
Attributions: (a) Robert
(a) Robert Engelhardt
Engelhardt [27];
[27]; (b) (b) Jerry
Jerry A. Payne,
A. Payne, USDA
USDA Agricultural
Agricultural Research
Research Service
Service [28];
[28]; (c) Jim(c)Cane,
Jim Cane,
USDA USDA Agricultural
Agricultural Research
Research Service
Service [29];(d)
[29]; and andM.
(d)
C.M. C. Cavalcante,
Cavalcante, F. F. Oliveira,
F. F. Oliveira, M. M. M.Maués,
M. Maués, and
and B. M.B.Freitas
M. Freitas
[30].[30].
Insects 2018, 9, 170 3 of 27

2.1. Bee Trapping Methods

The three most commonly used trapping methods for collecting bees for biodiversity studies are
bowl traps, vane traps, and Malaise traps. Bowl traps (Figure 2a) are by far the most popular trap
type for sampling bees. They are inexpensive, require little collector experience, and large numbers of
traps can be deployed and serviced in a time-efficient manner. Bowl traps are sometimes referred to
as “Moericke traps”, “bee bowls”, or “pan traps”, although the latter terminology can be confusing
because actual aluminum pans are sometimes used in trapping studies [31]. Bowl traps generally
consist of a colored plastic bowl or cup containing water or other liquid to serve as a killing agent,
with a small amount of fragrance-free dish detergent included to break surface tension. Traps are
generally deployed in the morning and samples collected in the late afternoon, or sometimes left out
for 24 h, but for longer-term sampling propylene glycol—a better preservative with lower evaporation
rates—can be used [32]. Bowl traps are generally placed on the ground, but are sometimes elevated to
match the height of most foraging bees. Bowl traps positioned one-third of the way up into the canopy
of a Michigan highbush blueberry (Vaccinium corymbosum L.) planting collected greater numbers of
bees than traps at lower or higher elevations [33].
Small bees such as halictids are often abundant in bowl traps [34,35], but the relative effectiveness
of bowl traps in collecting other small bee species is unclear. There is also substantial evidence for
taxon-specific bee attraction to certain colors, and a combination of blue, white, and yellow bowls
is frequently used to collect a wide diversity of bees [6,36]. Fluorescence may enhance bee captures,
and bee collections could also be affected by subtle variations in bowl and color characteristics among
manufacturers. Consistent use of bowl traps of standardized design and paint characteristics can
address this concern [26].
Traps are generally arranged systematically in a transect or grid with regular spacing to facilitate
easy location. Traps placed too closely together may compete for bees; evidence from a large-scale
study of bowl trap collections in a variety of ecoregions indicates that bee capture rates plateau at
intertrap distances of 3 to 5 m, with no further increase in captures at greater distances [34]. In general,
a 30-bowl transect appears to be adequate for assessing bee species richness, with little increase in
richness with greater numbers of bowls [37].
Vane traps (Figure 2b) consist of two colored plastic cross vanes (blue or yellow) with a collection
container underneath. Insects fall into the collection container after contacting a vane. Vane traps are
more expensive than bowl traps, bulkier to transport, and require a support structure for hanging. Vane
traps have been used less frequently than bowl traps in bee surveys, and there is a lack of studies on
optimal trap number and spacing. There is substantial evidence that vane traps collect relatively large
proportions of larger bees such as Bombus and eucerine bees [6,7,16,38–40], especially long-tongued
Bombus such as B. auricomus [16]. It has been suggested that blue vane trap light reflectance may
attract these bees by mimicking that of their preferred host plants [16,41]. Large numbers of these
large-bodied bees have been collected by blue vane traps in some studies [38,40], suggesting that these
traps can collect excessive numbers of these bees if not monitored closely. Because there is a single
source of vane traps, standardization is increased by avoiding differences in proprietary pigments
of different brands such as may occur with bowl traps [41]. However, long term monitoring projects
based on vane traps could be compromised if manufacture of these traps ends.
Bowl traps and vane traps have been used to assess bee abundance, diversity, and species
composition in agricultural systems. Blue, white, and yellow bowl traps, as well as blue and yellow
vane traps, were compared in Pennsylvania, USA apple orchards [41]. Highest species richness
estimates were found for blue vane and blue pan traps, and blue vane traps produced significantly
higher species accumulation rates than did all other traps. Vane traps were also deemed less labor
intensive to use because they only had to be collected weekly instead of daily, presumably because of
low rates of evaporation of preservative compared to bowl traps. Blue vane traps collected a high ratio
of common to rare bees compared to the other trap types, resulting in less efficient accumulation of
new species per bee collected, and suggesting that oversampling by blue vane traps may be a concern
Insects 2018, 9, 170 4 of 27

in this system [41]. However, oversampling is of less concern if the goal is to document the common
species in a community rather than compiling a comprehensive species list.
Bee communities of Michigan, USA commercial potato fields were sampled using blue vane
traps at canopy height and blue, white, and yellow bowl traps elevated 1 m and placed on circular
plastic platforms with one of each color trap [40]. Blue vane traps collected 30% more species than did
bowl traps. Blue vane traps also collected different species composition, with large-bodied Apidae
collected in relatively large numbers compared to bowl traps. However, it should be noted that in
this study the bowl traps on each platform were in close proximity to each other; in most studies
bowl traps are spaced apart in a transect. The pattern of trap deployment could affect bowl trap bee
collections. Blue vane traps may have high relative attractiveness in simple landscapes and collect
relatively large numbers of oligolectic bees, perhaps because of the greater relative attractiveness of
the UV reflectance of these traps in simple landscapes where resources are scarce [40,42,43]. Blue
vane traps were also used in combination with active netting to sample bees in sour cherry orchards
in Michigan and Pennsylvania as well as apple orchards in Pennsylvania [16]. The blue vane traps
collected an assemblage of bees distinct from that collected via active netting, and the trap collections
included primarily species that were not collected from orchard crop flowers. Several studies in a
variety of habitats have shown blue vane traps to be superior to yellow vane traps in collecting bee
abundance and species richness [6,7,41,44]. In locations where oversampling by blue vane traps is a
concern, the lower effectiveness of yellow vane traps could be an advantage, and replacement of some
blue vane traps with yellow vane traps or perhaps bowl traps might reduce excessive sample sizes.
Use of a combination of trap types and colors could also increase the proportion of the bee species
richness collected (see below).
While vane traps have been used to assess bee abundance and diversity in a variety of
environments, bowl traps are more commonly used and appear to be the method of choice for
monitoring bees at large geographic scales [45]. A protocol for monitoring insect pollinators and
detecting declines at such geographic scales using bowl traps has been proposed [46,47] and the merits
of this proposed program debated [48,49].
Bowl traps and vane traps are the most commonly used trapping methods in bee monitoring
and surveillance, but other trap types are available as well. Malaise traps (Figure 2c) are large
mesh fabric traps that are often used in collecting bees and other flying insects, which tend to move
upwards into the collection container upon contact with the trap [50]. There are several Malaise
trap designs, but the most widely used is the Townes-style Malaise trap with a black base and white
roof [51,52]. Malaise traps have frequently been used to sample various insect groups in a variety of
environments [6,53–57]. Only one of these studies focused on bees in an agricultural setting. This study
investigated bee diversity of southern Costa Rican coffee landscapes at 11 sites, including shaded coffee
farms, unshaded coffee farms, and nonagricultural sites, using Malaise traps [56]. Unshaded coffee
farms had higher bee abundance and species richness than the other two environments, and Malaise
traps collected substantial numbers of small-bodied bees, many of which had never been reported
as common in coffee farms. Although done in a very different environment, studies in Illinois, USA
restored tallgrass prairie [6] and deciduous forest [7] suggest that the results of the Costa Rica study
may be at least partially related to better relative performance of Malaise traps in open vs. shaded
environments. In the Illinois studies, Malaise traps collected by far the greatest bee abundance and
species richness of the four methods used in restored tallgrass prairie, but collected very few bees in
nearby deciduous forest, perhaps because of reduced phototactic behavior of bees in a closed canopy
environment. A significant association between Malaise trap collections and small-bodied bees has
also been found [58], supporting the observation that these traps are efficient in collecting small bees.
This could be advantageous in facilitating sampling of smaller, lesser known bees that are infrequently
collected in agroecosystems.
Because Malaise traps are probably more “passive” than bowl traps and vane traps, which
incorporate color to attract bees, it is possible that Malaise traps collect a more representative sample
Insects 2018, 9, 170 5 of 27

of the overall bee fauna at a particular location, although color and fabric mesh size have been shown
to influence collections of some insect groups such as tabanids [59] and very small hymenopterans [54].
However, Malaise traps also collect many nontarget insects, which is a drawback unless this bycatch is
put to good scientific use. While large numbers of bees can be collected with Malaise traps and sample
collection time is low once traps are set up, the typically abundant bycatch means that time spent
sorting out the bees is relatively great.
Other disadvantages of Malaise traps are cost (200+ U.S. dollars per trap) and significant set-up
time, limiting the number of traps that can be deployed. This can be a problem 5because
Insects 2018, 9, x FOR PEER REVIEW of 26
there is
evidence that Malaise trap effective trapping area is localized, with large variation among traps, at least
and sample
in tallgrass prairie collection
wheretime is low
floral once traps
resources are bees
and set up,have
the typically
a patchyabundant bycatch means
distribution [57]. that
This problem is
time spent sorting out the bees is relatively great.
compounded because Malaise traps are also time-consuming to relocate after set up. However, in many
Other disadvantages of Malaise traps are cost (200+ U.S. dollars per trap) and significant set-up
agroecosystems
time, limiting beethe distributions
number of traps maythatbecanmore uniformThis
be deployed. with
canless
be avariation in beethere
problem because collections
is among
traps, meaning
evidence that fewer traps
Malaise would
trap effectivebetrapping
required. areaStudies of spatial
is localized, variation
with large variationin Malaise
among traps,trap
at collections
of bees least in tallgrass
are needed inprairie
thesewhere floral resources
environments. and bees
Smaller, have portable
more a patchy distribution
Malaise traps[57]. This problem
such as “SLAM” traps
is compounded because Malaise traps are also time-consuming to relocate after set up. However, in
(sea, land, and air Malaise traps) may provide an acceptable alternative to traditional Malaise traps;
many agroecosystems bee distributions may be more uniform with less variation in bee collections
researchamong
on the effectiveness
traps, meaning fewer of SLAM traps
traps would be for collection
required. Studiesofofbees is variation
spatial needed in asMalaise
well. trap
Comparisons
collections of bees of Malaise
are needed traps withenvironments.
in these bowl and vane traps
Smaller, morehave notMalaise
portable been done in agroecosystems,
traps such as
“SLAM” USA
but in Illinois, traps (sea, land, and
restored air Malaise
tallgrass traps)
prairie andmaydeciduous
provide an acceptable
forest thesealternative
methods to traditional
collected somewhat
Malaise traps; research on the effectiveness of SLAM traps for collection of bees is needed as well.
distinct bee species composition, and certain species (indicator species) were significantly associated
Comparisons of Malaise traps with bowl and vane traps have not been done in agroecosystems,
with particular trap
but in Illinois, USAtypes [6,7].
restored Furthermore,
tallgrass these trap
prairie and deciduous types
forest thesevaried
methods incollected
the functional
somewhattraits of bees
collected in this tallgrass prairie [58]. Ground-level pan traps collected statistically
distinct bee species composition, and certain species (indicator species) were significantly greater numbers of
associated
with particular trap types [6,7]. Furthermore, these trap types
solitary vs. social and above- vs. below-ground nesting bees than expected. Malaise varied in the functional traits of bees
traps collected
collected in this tallgrass prairie [58]. Ground-level pan traps collected statistically greater numbers
greater numbers of polylectic vs. oligolectic bees as well as bees of shorter body length, and vane traps
of solitary vs. social and above- vs. below-ground nesting bees than expected. Malaise traps collected
collected greater
greater numbers
numbers of longer
of polylectic body length
vs. oligolectic bees
bees as wellthan expected.
as bees of shorterComparisons
body length, and of vane
the performance
of thesetraps
traps in agroecosystems,
collected greater numbers offrom longerboth
bodya length
species beesand
thantrait diversity
expected. standpoint,
Comparisons of the could yield
performance
important information of thesenot traps
only in on
agroecosystems,
variation infrom trapboth a species andbut
performance traitalso
diversity
on the standpoint,
ecology and natural
could yield important information not only on variation in trap performance but also on the ecology
history of bees in environments of varying complexity.
and natural history of bees in environments of varying complexity.

(a) (b)

(c) (d)

Figure Figure 2. Common

2. Common samplingmethods
sampling methods forfornon-Apis bees:bees:
non-Apis (a) Blue
(a)bowl
Blue trap, Moericke
bowl trap,trap, or pan trap, or pan
Moericke
trap; (b) Blue vane trap; (c) Townes-style Malaise trap; and (d) aerial (left) and sweep nets. Attribution:
trap; (b) Blue vane trap; (c) Townes-style Malaise trap; and (d) aerial (left) and sweep nets. Attribution:
(c) Ceuthophilus [60].
(c) Ceuthophilus [60].
2.2. Active Netting of Bees
2.2. Active Netting of Bees
In addition to trapping, bees are also commonly sampled using insect nets. Insect netting
In generally
addition to two
takes trapping, bees netting
forms: targeted are also commonly
of bees sampled
using an aerial using
net (Figure insect
2d, left), and nets. Insect netting
sweeping
of vegetation using a sweep net (Figure 2d, right). Targeted netting allows the researcher
generally takes two forms: targeted netting of bees using an aerial net (Figure 2d, left), and sweeping of to
preferentially collect particular species, and to associate an individual bee with the particular flower
Insects 2018, 9, 170 6 of 27

vegetation using a sweep net (Figure 2d, right). Targeted netting allows the researcher to preferentially
collect particular species, and to associate an individual bee with the particular flower it visits. Aerial
nets are generally constructed of a lightweight mesh fabric, whereas sweep nets are constructed of
sturdy cloth that allows the collector to sweep the net through vegetation, collecting insects that are on
the vegetation [61]. While less focused than targeted netting, sweep netting can provide information
on the bee fauna associated with a particular area of vegetation. In both types of netting, samples
can be standardized by timing the sampling period or by measuring the distance or area covered.
Active netting of bees is inexpensive, but relatively labor-intensive, and variation in collector abilities
can make comparisons among samples difficult. Targeted netting, if done thoroughly enough, can
provide a relatively complete sample of the bee fauna present, or can supplement bee samples collected
by other methods. For instance, relative to bowl traps, targeted netting can yield high numbers
of fast or high-flying bees such as Colletes, Megachile, and Melissodes [62]. However, depending on
collector experience and skills, smaller and more cryptic bees may be under-represented in targeted
netting samples.
Targeted netting in combination with bait stations is a well-known method of sampling orchid
bees (Apidae: Euglossini), a dominant bee taxon of Neotropical forests that includes pollinators of
economically important crops such as rubber trees, Hevea brasiliensis Müll. Arg., and Brazil nuts,
Bertholletia excelsa Humb. & Bonpl. (Figure 1d) [30,63–65]. Male orchid bees visit orchids and other
flowers to collect aromatic chemicals that appear to be important in species recognition and mate
choice [66]. These compounds make it possible to sample orchid bees by netting them as they approach
a bait station. Orchid bee bait stations generally consist of an absorbent material such as cotton
suspended from a string and baited with a chemical attractant. Generally, several bait stations are set
up a few meters apart, with each station being baited with a different attractant. There are dozens
of these chemical attractants [66]; some are relatively expensive, and may not be available in some
countries, necessitating international shipping which adds to the expense. Some of the more commonly
used attractants include benzyl acetate, cineole, eugenol, methyl salicylate, and vanillin. Orchid bee
attractants vary greatly in the abundance and species composition of bees attracted [66,67]. These
attractants are also used in conjunction with traps to collect orchid bees. However there is evidence
that baited traps collect lower abundance and species richness than does sampling with baits and
active netting, with trap collections biased toward larger orchid bee species in the genera Eulaema and
Eufriesea [68]. A review of these and other methodological issues related to orchid bee sampling is
available [69].
Sweep netting generally involves continuously sweeping vegetation with the net for a specific
time period, while walking a measured transect, or covering a specified area. This allows the collector
to capture relatively small or inconspicuous bees that may not be collected readily by targeted netting.
Sweep netting is a commonly used method of sampling bees in tropical locations [25], but appears to
be less frequently used in temperate regions. In temperate agroecosystems, sweep netting has been
used in conjunction with bowl traps to assess non-Apis bee abundance and diversity in canola fields
in Alberta, Canada [70–72], grasslands of agriculturally dominated landscapes in Iowa, USA [73],
and lowbush blueberry fields in Maine, USA [74]. In the studies of bees associated with canola fields,
over 20 times as many bees were collected in bowl traps as by sweep netting [72], but difficulty in
assessing relative sampling effort makes comparisons between methods problematic.
Approximately 5% of all bee and wasp species are “trap-nesting” species, that is, they establish
nest sites in tunnels in dead wood or grass stems [75]. These include species in the genera Megachile,
Osmia, Hylaeus, Trypoxylon, and Ancistrocerus, among others. These species can be sampled using
“trap-nests” constructed of wood or other materials. Trap-nests have been used in a variety of ecological
and life history studies, including a recent study of the phenology of plant flowering and solitary bee
and wasp emergence in Rocky Mountain, USA meadows [76]. Trap-nests appear to be an uncommon
approach in agroecosystems, but have been used to assess nesting frequency of trap-nesting species
in fallow and wildflower plots in agriculturally dominated areas in North-Central Florida, USA [77].
Insects 2018, 9, 170 7 of 27

Trap-nests were also used to examine effects of landscape complexity on trap-nesting Hymenoptera and
their parasites in a region dominated by intensively managed agriculture in northwestern Germany [78].
In addition to detection of trap-nesting species, interesting life history data, such as seasonality,
duration of life stages, and nest parasites can be collected using this method. The construction of
trap-nests can be labor intensive, although premade “bee houses” are commercially available and
could be useful
Insects for
2018,research.
9, x FOR PEERMold
REVIEW formation can be a problem in trap-nests, especially if an 7 ofimpervious
26

material such as glass tubing is used. Naturally occurring plant materials such as bamboo are good
The construction of trap-nests can be labor intensive, although premade “bee houses” are
for constructing trap-nests,
commercially but
available the
and variable
could diameter
be useful is aMold
for research. disadvantage.
formation can Straight-grained
be a problem in trap- pieces of
seasoned white
nests, pine haveif been
especially found tomaterial
an impervious work well forglass
such as constructing trap-nests
tubing is used. Naturally[75]. Further
occurring plant studies on
materials
the usefulness of this such as bamboo
method are good beneficial
in sampling for constructing trap-nests, but
Hymenoptera in the variable diameter
agroecosystems areisneeded.
a
disadvantage. Straight-grained pieces of seasoned white pine have been found to work well for
constructing trap-nests [75]. Further studies on the usefulness of this method in sampling beneficial
3. Natural Enemies/Pest Management
Hymenoptera in agroecosystems are needed.
The value of natural control of native agricultural pests by beneficial insects (Figure 3) has been
3. Natural Enemies/Pest Management
estimated at $4.49 billion [1]. However, agroecosystems often provide an unfavorable environment
The value of natural control of native agricultural pests by beneficial insects (Figure 3) has been
for the survival and reproduction of these beneficial organisms. Conservation biological control,
estimated at $4.49 billion [1]. However, agroecosystems often provide an unfavorable environment
the manipulation of the and
for the survival environment
reproductionto of conserve these
these beneficial beneficial
organisms. natural enemies
Conservation and enhance
biological control, the their
effectiveness, is an increasingly
manipulation important
of the environment component
to conserve theseof agricultural
beneficial naturalpest management
enemies and enhance[5]. In order to
their
effectiveness,
evaluate the is an increasingly
status of these importantand
natural enemies component of agriculturalof
the effectiveness pest management [5].
conservation In order reliable
measures,
to evaluate the status of these natural enemies and the effectiveness of conservation measures, reliable
sampling methods are needed. In this section I review methodological approaches to sampling and
sampling methods are needed. In this section I review methodological approaches to sampling and
monitoringmonitoring
these beneficial arthropods
these beneficial in agroecosystems.
arthropods in agroecosystems.

(a)
(b)

(d)
(c)
Figure natural
Figure 3. Some 3. Some natural
enemies enemies potentially
potentially important in
important ininsect
insectpest control:
pest (a) a carabid
control: beetle, beetle,
(a) a carabid
Poecilus cupreus (L.); (b) the predatory wheel bug, Arilus cristatus (L.) consuming a Japanese beetle,
Poecilus cupreus (L.); (b) the predatory wheel bug, Arilus cristatus (L.) consuming a Japanese beetle,
Popillia japonica Newman; (c) a campoplegine ichneumonid; (d) the hunting wasp Ammophila sabulosa
Popillia japonica Newman;
(L.) carrying (c) a campoplegine
a caterpillar. ichneumonid;
Attributions: (a) James Lindsey (d) the hunting
at Ecology wasp Ammophila
of Commanster sabulosa (L.)
[79]; (b) Andy
carrying a McLemore,
caterpillar. [80];Attributions: (a)and
(c) H. Dumas, [81]; James Lindsey
(d) Patrick at Ecology
Reijnders, [82]. of Commanster [79]; (b) Andy
McLemore, [80]; (c) H. Dumas, [81]; and (d) Patrick Reijnders, [82].
3.1. Sampling Natural Enemies in Epigeic Environments
3.1. Sampling Natural Enemies in Epigeic Environments
3.1.1. Pitfall Traps
3.1.1. Pitfall Traps
The most important groups of beneficial epigeic natural enemies include carabid beetles,
(Coleoptera: Carabidae) (Figure 3a), rove beetles (Coleoptera: Staphylinidae), wolf spiders (Araneae:
The most important
Lycosidae) and othergroups of spiders,
wandering beneficial epigeic (Myriopoda:
and centipedes natural enemies include
Chilopoda). Of thesecarabid
groups, beetles,
(Coleoptera: Carabidae)
carabids are the(Figure 3a), rove studied
most thoroughly beetlesand(Coleoptera: Staphylinidae),
well understood. Carabids and wolf spiders
other epigeic(Araneae:
Lycosidae) arthropods
and otherare most commonly
wandering sampled
spiders, and using pitfall traps
centipedes (Figure 4a) [83–85].
(Myriopoda: This trap type
Chilopoda). Of is the groups,
these
carabids are the most thoroughly studied and well understood. Carabids and other epigeic arthropods
are most commonly sampled using pitfall traps (Figure 4a) [83–85]. This trap type is the method of
Insects 2018, 9, 170 8 of 27

choice for carabid abundance and diversity sampling within the National Ecological Observatory
Network (NEON), a continental-scale program to increase our knowledge of the ecological impacts
of climate change, land-use patterns, and invasive species on biodiversity and ecosystem processes
in the USA [86]. Pitfall traps have been used to collect and quantify epigeic arthropods since at least
the early 1900s [87,88]. Pitfall traps consist of an open-top container buried in the ground with the
rim flush with or slightly below the substrate surface. Animals falling into the container are trapped.
There are many modifications of the basic pitfall trap design, including a funnel to prevent escape,
a cover to block rain and debris from falling into the trap, baits to target particular taxa, and drift fences
and barriers to increase captures and infer direction of movement [89,90]. Pitfall traps are sometimes
used dry to collect live specimens, but predatory species feeding on each other is often a problem [91],
so more often the trap is partially filled with a preservative to kill and maintain the trapped arthropods.
A variety of preservatives have been used, including water, brine, formalin (which is highly toxic and
generally no longer used), ethylene glycol, propylene glycol, acetic acid, alcohol, kerosene, and chloral
hydrate [85]. Because the numbers of specimens captured is dependent on their activity levels as well
as their abundance [92], pitfall trap samples are best described in terms of “activity-abundance” or
“activity-density” [84].
Most studies using pitfall traps in agroecosystems have focused on carabids. Many of these have
been done in the agriculturally important Midwestern USA [93]. One focus has been on effects of
cropping practices on beneficial arthropods. For example, pitfall traps and quadrat sampling have been
used to examine the effects of organic transition systems on carabids and other arthropods in Illinois,
USA agricultural fields [94,95]. Pitfall trapping indicated that activity levels of beneficial arthropods
were reduced in the low intensity system, but quadrat sampling showed that this environment
had the greatest density of these arthropods, suggesting that the more stable environment of the
low intensity system resulted in less arthropod movement. Predation rates on sentinel wax moth
(Galleria mellonella L.) larvae and seed removal were greatest in the low intensity system as well,
suggesting that low intensity agricultural practices were advantageous to beneficial arthropods. These
results demonstrate that a combination of sampling methods can often provide more information
and greater insight than does a single method. Pitfall traps have also been used to monitor carabid
abundances in conventional vs. reduced-risk insecticide management practices in Michigan, USA
highbush blueberry plantations [96], to assess potential effects of transgenic corn on carabid abundance
in Iowa, USA [97], and to evaluate the potential of carabids to serve as indicators of adverse
environmental effects of genetically modified crops in Europe [98].
In addition to assessments of beneficial arthropods in relation to conditions within the crop
environment, there have been several landscape-scale investigations of effects of anthropogenic land
use patterns on arthropods, based on pitfall trap sampling. Pitfall traps were used to show that
carabid community variation is associated with extent of disturbance in sites ranging from highly
disturbed pasture to cocoa (Theobroma cacao L.) plantations to successional forest and undisturbed
native forest in the Brazilian Amazon [99]. This study also identified several carabid indicator species
and suggested that carabid communities can be used to evaluate the status of Neotropical ecosystems.
Pitfall traps were also employed to compare responses of epigeic spiders and carabids to differences
in cultivated and semi-natural environments in China [100]. Results of this study indicated that the
high plant diversity and vegetation structure of semi-natural habitats significantly enhanced spider
abundance, whereas these factors were a poor predictor of carabid abundance and species richness.
Plant diversity affected the species composition of both groups. These studies illustrate the utility
of pitfall traps for investigating associations between habitat characteristics and beneficial epigeic
arthropods. However, the potential for habitat-specific effects on collections of arthropods in pitfall
traps should be considered, and if possible a combination of sampling methods should be used.
Like most trapping methods, pitfall traps are subject to certain biases, and collections can be
affected by a variety of factors. In a study of the spider community of winter wheat, species composition
and sex ratios obtained using pitfall traps differed from that obtained via density sampling using a
Insects 2018, 9, 170 9 of 27

D-Vac suction sampler (see next section). These discrepancies could be due to species-specific variation
in activity patterns, searching for mates or food, and species-specific differences in ability to escape
from the pitfall traps [101]. Challenges associated with pitfall trapping have been studied in detail for
carabids
Insects[9,102].
2018, 9, x As
FORpreviously
PEER REVIEWmentioned, arthropod activity level affects the probability of capture.
9 of 26
This may be related to another bias associated with pitfall traps—the tendency for over-representation
differences in ability to escape from the pitfall traps [101]. Challenges associated with pitfall trapping
of large-bodied species, as shown by a study in which carabid composition of pitfall trap samples was
have been studied in detail for carabids [9,102]. As previously mentioned, arthropod activity level
compared with that collected via extraction from litter using Berlese–Tullgren funnels (Figure 4b) [9].
affects the probability of capture. This may be related to another bias associated with pitfall traps—
This is
theprobably
tendencyrelated to locomotive abilities.
for over-representation Largerspecies,
of large-bodied speciesasgenerally
shown bymove a study greater distances
in which carabid than
smaller species, whereas smaller species such as Notiophilus spp., often evade
composition of pitfall trap samples was compared with that collected via extraction from litter using capture upon reaching
the lip
Berlese–Tullgren funnels (Figure 4b) [9]. This is probably related to locomotive abilities. Largerfrom
of the trap [9,102,103]. Different carabid species also have differing abilities to escape
trapsspecies
[104]. generally
Pitfall trap movecollections also vary
greater distances in relation
than to diel whereas
smaller species, activity smaller
patternsspecies
of carabids,
such as with
Notiophilus
diurnal carabids spp., often
being evade capture uponinreaching
under-represented the lip perhaps
pitfall traps, of the trapbecause
[9,102,103].
theyDifferent
can seecarabid
and avoid
species
the traps also have
[102,103]. differingdiel
However, abilities to escape
activity from traps
of particular [104]. species
carabid Pitfall trap
can collections also vary
vary in relation in
to habitat,
relation to diel activity patterns of carabids, with diurnal carabids being under-represented
with greater or lesser diurnal activity in agricultural fields than in nearby uncultivated habitat [105]. in pitfall
traps, perhaps because they can see and avoid the traps [102,103]. However, diel activity of particular
Amount and structure of vegetation can also affect carabid collections. For instance, pitfall traps
carabid species can vary in relation to habitat, with greater or lesser diurnal activity in agricultural
with vegetation removed from the surrounding area generally collect more carabids than do traps
fields than in nearby uncultivated habitat [105]. Amount and structure of vegetation can also affect
without a cleared
carabid area, although
collections. For instance,different
pitfallcarabid
traps withspecies vary in
vegetation their response
removed from thetosurrounding
different vegetation
area
structure [102]. Characteristics related to the pitfall traps themselves
generally collect more carabids than do traps without a cleared area, although different can also affect carabidcarabid
collections.
Round trapsvary
species without covers
in their tendtotodifferent
response collect greater
vegetationabundance of carabids
structure [102]. than dorelated
Characteristics covered to traps
the or
rectangular traps,
pitfall traps althoughcan
themselves there
also isaffect
somecarabid
speciescollections.
and habitat-related
Round traps variation
without [9]. Type
covers tendoftopreservative
collect
greater abundance
can influence abundance of carabids
and species than composition
do covered traps or rectangular
of collections traps,[106,107],
as well although so there is some in
consistency
comparative studies using pitfall traps is important. On the other hand, variation in species
species and habitat-related variation [9]. Type of preservative can influence abundance and pitfall trap
composition
collections relatedoftocollections as wellcan
trap variation [106,107],
be putso toconsistency
good advantagein comparative
in species studies using studies
inventory pitfall traps
because
is important. On the other hand, variation in pitfall trap collections related to trap variation can be
the traps may collect greater combined species richness [106]. A review of factors that may affect
put to good advantage in species inventory studies because the traps may collect greater combined
arthropod collections by pitfall traps is available [106].
species richness [106]. A review of factors that may affect arthropod collections by pitfall traps is
There
available is evidence
[106]. that pitfall trap samples can be related to densities of carabids [108]. Fenced
pitfall traps Therewere evaluated
is evidence for use
that pitfall trap insamples
estimatingcan bedensities
related toof epigeicof predatory
densities beetles,
carabids [108]. Fencedusing
mark-release-recapture.
pitfall traps were evaluated For seven
for use of 10 speciesdensities
in estimating studiedofrecapture rates were
epigeic predatory greater
beetles, than 70%,
using mark-
suggesting that these traps are suitable for estimating densities if trap density is sufficient [109].
release-recapture. For seven of 10 species studied recapture rates were greater than 70%, suggesting
thatstudies
Further these traps
are are suitable
needed to for estimating
evaluate densities if trapofdensity
the effectiveness pitfallistraps
sufficient [109]. Further studies
in agroecosystems and how
are needed
sampling to evaluate
is affected the effectiveness
by arthropod behavior, of pitfall
activitytraps in agroecosystems
levels, and environmental and how samplingsuch
variables is as
affected by arthropod behavior, activity levels, and environmental
vegetation structure. Studies incorporating a second sampling method that measures arthropod variables such as vegetation
structure. Studies incorporating a second sampling method that measures arthropod densities, such
densities, such as quadrat sampling and extraction of arthropods [9,95], would allow comparison
as quadrat sampling and extraction of arthropods [9,95], would allow comparison of pitfall trap
of pitfall trap samples with density estimates of epigeic arthropods. Some of these approaches to
samples with density estimates of epigeic arthropods. Some of these approaches to measuring epigeic
measuring
arthropod epigeic arthropod
densities densities
are discussed arenext
in the discussed
section.in the next section.

(b)
(a)
Figure
Figure 4. Two
4. Two common
common sampling
sampling methodsfor
methods forepigeic
epigeic arthropods:
arthropods:(a)(a)
Pitfall trap
Pitfall or Barber
trap trap trap
or Barber and and
(b) homemade
(b) homemade Berlese–Tullgren
Berlese–Tullgren funnels.Attribution:
funnels. Attribution: (a)
(a) Mnolf
Mnolf[110].
[110].

3.1.2. Other Methods of Sampling Epigeic Arthropods

Insects 2018, 9, 170 10 of 27

3.1.2. Other Methods of Sampling Epigeic Arthropods

While pitfall traps are by far the most commonly used method of sampling epigeic arthropods,
other methods are available as well, some of which can provide estimates of arthropod density. Other
methods for sampling epigeic arthropods include suction samplers, emergence traps, soil flooding,
microhabitat removal and arthropod extraction, and cryptozoan boards.
Suction samplers are frequently used to collect arthropods from vegetation, but can also be used
to collect epigeic arthropods. These samplers use suction provided by a motorized fan to collect
arthropods into a collection net. The most widely used suction sampler is the Dietrick vacuum insect
net, or “D-vac” [111,112]. When used to sample a specified surface area, they can provide a measure
of arthropod density [101], but sampling within enclosures that are sealed to the ground is needed
to avoid collecting specimens from outside the measured sampling area [113]. In terms of sampling
of beneficial arthropods, cursorial spiders have been sampled in Central European farmland and
perennial habitats using suction sampling [114]. Sampling efficiency may be taxon-specific, and large,
heavy predators are often undersampled [115]. Wet sampling locations, such as when dew is present,
can reduce collections because specimens stick to the nozzle, hose, and collection net [116].
Emergence traps generally consist of a cloth or metal enclosure that covers a known area of
soil/litter or other environment. When the animal exits as it moves from one part of its habitat to
another, perhaps during a specific stage of its life, the animal is trapped in a collection container [115].
Emergence traps are also known as eclectors, or photoeclectors if the trap exploits positive phototaxis
of emerging organisms [112], as most emergence traps do. Emergence traps can provide a measure of
density since they collect from a discrete area, and are also advantageous in that specimens collected
are from the location of interest rather than potential migrants. Typically an emergence trap will
include a pitfall trap within it to collect invertebrates that tend to stay on the ground rather than
moving up to the collection container, and in this discussion “emergence trap” is considered to contain
a pitfall trap as part of the apparatus.
Emergence traps have been used in agricultural studies, although less frequently than pitfall traps.
Emergence traps, along with pitfall traps (separate from the emergence traps), were used in a study that
showed oilseed rape to be a beneficial crop environment for at least two dominant species of carabids,
Poecilus cupreus (L.) and Brachinus sclopeta (Fabricius), in western France [117]. The two sampling
methods allowed the authors to investigate spring activity-density as well as overwintering location of
these carabids. Emergence traps and pitfall traps were also used to assess the effects of agricultural
land use on carabid community trait composition in southwestern Sweden [118]. Emerging carabids in
high intensity land-use fields had lower body length, whereas crop fields produced greater proportions
of carabids with good flight ability and carnivorous diets than did grasslands. Species composition
differed significantly between sampling methods, and there was a significant land-use type by sampling
method interaction. Macro-emergence traps (modified Malaise traps) have been used successfully to
sample arthropod natural enemy communities overwintering in semi-natural habitats in agricultural
landscapes of southwestern France [119]. A variety of arthropod taxa were collected, including Araneae,
Hemiptera, Neuroptera, Carabidae, Coccinellidae, Syrphidae, Staphylinidae, and various parasitoids.
Emergence traps appear to have a great deal of potential for studies of agroecosystem invertebrates.
They are somewhat complimentary with pitfall traps in that they provide direct density estimates of
an enclosed area whereas pitfall trap collections to a great extent reflect activity levels of the organisms.
Therefore, use of these two trap types in the same habitat, and comparison of the invertebrate assemblages
collected with the two methods, can provide important information on the biology of these animals [112].
One potential drawback of emergence traps is that they can influence the microclimate of the enclosed
area and so may influence the phenology or behavior of the invertebrates. These effects can be specific
to trap construction [115]. For instance, metal-screened emergence traps collected twice as many pink
bollworms, Pectinophora gossypiella (Saunders) as did plastic-screened ones [120].
Soil flooding involves saturating a defined area of soil with water, which forces the arthropods
to the surface where they can be collected. This method was originally used to collect carabids and
Insects 2018, 9, 170 11 of 27

staphylinids in riparian habitats [121] and provides an estimate of density. An area of soil is isolated
with a 0.1 m2 enclosure, vegetation is examined and removed, and 2 L of water is poured into the
enclosure. Arthropods are removed, and later an additional 2 liters are added and arthropods are again
removed [112]. Studies in a variety of crop environments have shown that small carabids, staphylinids,
and Araneae can be collected via soil flooding [122–124]. In a study using three methods to sample
beneficial arthropods of agricultural fields in Austria, small carabids were predominant in soil flooding
and emergence trap samples, whereas the larger P. cupreus was predominant in pitfall traps, probably
reflecting its greater mobility [124]. However, soil flooding can be ineffective under certain soil
conditions. Blockage of the soil surface by silty mud can inhibit the emergence of arthropods, and in
dry clay soils with large cracks or other highly perforated soils, impractical amounts of water can be
required to sufficiently flood the soil [112].
Microhabitat removal and arthropod extraction involves removal of a known area of litter or
soil for later extraction of arthropods, providing an estimate of density. A variety of methods have
been used. Samples can be hand-sorted and searched for arthropods manually, or can be placed in an
apparatus for extraction [112]. The most widely used of these is the Berlese–Tullgren funnel (Figure 4b),
in which the sample is placed in a container with a mesh screen to support the sample and a funnel
that leads to a collection container below. A light bulb or other heat source is located above the sample;
the arthropods within the sample are forced downward into the collection container by the heat and
desiccating soil [115]. Many modifications and improvements have been made on the original design.
When placed in the extractor, the soil core should be inverted and kept intact; otherwise, the natural
passageways will be disrupted and the arthropods’ “escape routes” will be eliminated [125]. It has also
been noted that significant losses can occur through arthropods becoming trapped in the condensation
that forms on the sides of the container from the moisture contained in the soil core; space should be
left between the core and the sides of the container to prevent this [126].
Berlese–Tullgren funnels have been used to collect spiders from samples taken from maize, ryegrass,
and pasture [127], and beneficial predatory arthropods (spiders, carabids, and staphylinids) from samples
taken from overwintering sites within cereal fields [128]. However, the effectiveness of this method can
vary with habitat. Berlese–Tullgren funnels were found to be an ineffective method for sampling epigeic
arthropods in the sandy soils of Florida, USA bush bean plots, because of the low amount of surface
litter and large amounts of sand that fall from the sample into the collection jar [129].
Cryptozoan boards, sometimes referred to as “drop boards”, can be used to collect cryptozoans,
the “hidden animals” that shelter and hide underneath stones and logs [115,130]. These are generally
wooden boards of 0.1 m2 each that are placed on the ground. When collecting samples, the boundaries
of the board should be marked to avoid sampling outside of the covered area. The board should
be lifted and specimens collected quickly, since many of these animals move rapidly and quickly
find hiding places. An aspirator for sucking up the specimens is helpful [130]. A potentially useful
alternate method is to place a 0.1 m2 enclosure around the board (slightly greater area than the board),
with the edges pressed into the soil. Then the board is removed and specimens collected, with the
enclosure preventing escape. The specimens can be collected on site, or the litter and soil can be
collected and placed in a bag for later sorting in the lab, or perhaps extraction using Berlese–Tullgren
funnels. Another possibility might be to use a suction sampler (see above) to collect the material under
the board, although the high humidity of the microhabitat might cause clumping of the litter and so
preliminary breaking up and loosening of the material may be necessary.
Predatory macroarthropods found among the cryptozoa include carabids, centipedes,
staphylinids, dermapterans, and Araneae. The microhabitats these animals are adapted to are generally
dark, with fairly stable temperature and humidity compared to the surrounding environment [131].
These animals vary in the degree to which they are bound to this environment, and predators appear
to be less restricted to the cryptozoan microhabitat than other organisms [132]. Because it may take
some time for the microenvironment underneath a cryptozoan board to develop into an optimal one
for cryptozoan colonization, the length of time the cryptozoan boards are left in place may affect
Insects 2018, 9, 170 12 of 27

collections, and this may vary in a taxon-specific manner. Abundance and taxonomic composition of
invertebrates collected via cryptozoan boards can also vary with board size, color, and surface features
of the ground [133].
Cryptozoan boards have been used relatively infrequently in agroecosystems. In Zimbabwe,
millipedes are important in the processes of decomposition and nutrient cycling [134]; the seasonal
activity patterns of these animals has been examined in agricultural pasture and other habitats using
cryptozoan boards [135]. Cryptozoan boards were also used to sample soil surface arthropods in the
aforementioned study in Florida, USA bush bean plots. Cryptozoan boards collected less taxonomic
diversity than did pitfall traps but more than Berlese–Tullgren funnels overall. Compared to pitfall
traps, cryptozoan boards collected fewer staphylinids, spiders, parasitoid wasps, and various other
taxa; more crickets, Dermaptera, and elaterids; and similar numbers of formicids and carabids [129].
Cryptozoan boards are generally less productive than pitfall traps on a per unit time or effort basis [136].

3.2. Sampling Natural Enemies on Vegetation

3.2.1. Direct Counts

In some cases, beneficial arthropods can be sampled using direct counts of individuals on
vegetation. This method is best used on relatively inactive arthropods; accurate counts are difficult to
obtain for active, fast-moving, or easily disturbed arthropods. In fields with regularly spaced crops,
natural enemies associated with the crop may be visually counted and densities per plant or per
unit area calculated. But in more structurally complex agroecosystems, a measure of density can be
obtained using quadrats or specific plant structures as the sampling unit. Spiders of grassland and
cereal crop vegetation have been sampled using direct counts within 1 m2 quadrats [137]. Eggs and
larvae of syrphid and coccinellid predators of aphids were counted on winter wheat shoots and in
quadrats. The latter study combined those two data sets to obtain predator density estimates for the
entire habitat [138]. Some predators may have highly clumped distributions related to prey density and
other environmental factors. Coccinellids, for instance, are affected by temperature and aphid density.
When these factors were included into a predictive model of coccinellid densities in wheat fields,
R2 values of 0.63 to 0.94, depending on species, were found between coccinellid visual counts and
population densities [139]. Direct visual counting of arthropods is relatively labor-intensive, and this
can be a major disadvantage, depending on the difficulty of seeing and counting the arthropods in
question and the complexity of the environment in which they live. Sixty to 90 person-minutes per plot
were required to search for and remove spiders from 0.5 m2 plots of grassland with a mean vegetation
height of 15 cm [140].
More active arthropods can be counted after removal from vegetation using a suction sampler,
described previously for epigeic arthropods. This method has been used to quantitatively sample the
spider fauna of USA Great Plains winter wheat within enclosed 1 m2 sample plots [141].

3.2.2. Sweep Netting

Sweep-netting (Figure 2d, right) is a commonly used method of sampling arthropods on
vegetation [115], and can collect a variety of beneficial arthropods including spiders as well as predatory
hemipterans (Figure 3b), beetles, and neuropterans. Sweep-netting was used in the above study
estimating coccinellid densities in wheat fields [139]. Regression models relating sweep net collections
to absolute densities of coccinellids produced R2 values ranging from 0.51 to 0.90, depending on
species. Effects of different crop types and production systems on densities of staphylinids have been
examined using sweep-netting and four other methods in Punjab Province, Pakistan, but comparisons
among sampling methods were not done [142].
Sweep-netting has important advantages, including low equipment cost and potentially large
yield of specimens per unit effort. By standardizing efforts based on number of sweeps, area sampled,
or duration of sampling, repeatable and comparative results can be obtained. A formula allowing
Insects 2018, 9, 170 13 of 27

reporting of sweep-netting samples as insects collected per unit volume of vegetation has been
developed [143] and applied to coccinellid sampling [144].
If sweep net samples obtained by different people are included in a comparative study, then efforts
should be undertaken to ensure that the samples are standardized and comparable. There are other
potential biases and sources of error associated with sweep-netting. Arthropods that tend to fall off
the vegetation or fly away as the netter approaches will be undersampled [130]. Vegetation structure
and the taxon being sampled can also affect sweep net collections. If the species being sampled is
distributed throughout the vertical range of the plants, then smaller proportions of the species will
likely be sampled from taller plants relative to shorter plants [115], and even closely related species
can differ in their susceptibility to collection by sweep net [145].

3.2.3. Suction Samplers

As mentioned previously in the section on sampling epigeic arthropods, these devices use suction
provided by a motor to collect arthropods. They are frequently used to sample arthropods from
vegetation. These devices have been used extensively in sampling of grassland invertebrates, but are also
useful in agroecosystems, including alfalfa [146], cereals [147,148], and winter wheat [149]. Efficiency of
vacuum samplers is taxon-specific, can vary with year, season, site, and vegetation structure, and can
be affected by a variety of environmental factors [147,148,150,151]. High abundance and diversity of
spiders (4700 individuals and 91 species) were sampled in Central European farmland and perennial
habitats using suction sampling [114]. Per unit effort, suction sampling collected greater abundance and
species richness of arthropods than did sweep-netting in California coastal sage scrub habitat [152].

3.2.4. Shaking and Beating Vegetation

Arthropods can be sampled from vegetation by shaking or using a stick to beat plants or
plant structures, and collecting the arthropods that fall from the vegetation in a collection tray or
cloth [115]. The insects can be rapidly collected with an aspirator, or into a tray containing a killing
solution/preservative such as ethyl alcohol. Large arthropods that are easily dislodged, such as many
pentatomids, may yield absolute estimates, but of course insects that tend to fly away when disturbed
will be poorly sampled [115,130,153]. Predatory arthropods have been successfully sampled from
apple trees by removing branches over a cloth, and then cutting into smaller sections and putting these
into a revolving rectangular shaker and dislodging the insects [154]. Beating has been used to sample
coccinellids on trees and shrubs in a study of the impacts of the invasive coccinellid Harmonia axyridis
(Pallas) on native coccinellids [155]. Shaking or beating may substitute for sweep netting when shrubs
and small trees are being sampled, or in dense, thorny habitats that are not suitable for sweeping.
It has been pointed out that beating could damage some plants (and therefore disrupt the habitat being
sampled), and for this reason shaking may be preferable [156].

3.3. Sampling Predatory and Parasitic Wasps and Flies

3.3.1. Trapping Methods

Since many predatory and parasitic wasps and flies (Figure 3c,d) are active fliers and often
abundant on vegetation as they search for hosts, prey, or plant-based food sources, some of the
previously mentioned methods, such as netting and suction sampling, can be useful for these insects
as well. Trapping methods for these insects include pan traps (Figure 2a) (also called Moericke traps,
or, in the bee literature, bowl traps), Malaise traps (Figure 2c), and sticky traps. These traps have
been used in studies of parasitoids in in a variety of habitats including agroecosystems and other
cultivated habitats. For instance, Liotryphon crassiseta (Thomson), an ichneumonid parasitoid of the
red-belted clearwing moth, Synanthedon myopaeformis (Borkhausen), was monitored using yellow
pan traps in apple orchards of western Poland [157]. Malaise traps were used to compare relative
abundance of parasitoids in herbicide-treated and untreated loblolly pine (Pinus taeda L.) plantations in
Insects 2018, 9, 170 14 of 27

the coastal plain of Georgia, USA [158]. The effectiveness of different sticky trap colors was compared
in a study of aphelinid parasitoids of San Jose scale in apple orchards in North Carolina, USA. Trap
color had a significant effect on relative abundances of species collected. Among colored traps, traps
combined with San Jose scale sex pheromone collected significantly more Encarsia perniciosi (Tower)
than did unbaited traps, suggesting that this pheromone acts as a kairomone for this parasitoid. Black
baited traps collected significantly more E. perniciosi than did baited yellow or white traps, suggesting
an olfactory–visual interaction in host location by this species [159]. Yellow sticky traps have also
been used to monitor abundances of Cardiaspina psillids and adult parasitoids during an outbreak in
Eucalyptus woodland in Western Sydney, Australia [160].
Several studies have compared different methods of sampling parasitic hymenoptera in a
variety of habitats. Two Malaise traps and four pan traps (color not given) were used to collect
parasitic Hymenoptera in a transect in organic rice fields and a nearby protected area in the Brazilian
Atlantic Forest biome [161]. Malaise traps collected the greatest numbers of parasitoids (58% of total),
and collected 1.7 to 1.9 times the estimated species richness as did the pan traps. In rice ecosystems of
Tamil Nadu, India, sweep-netting, yellow pan traps at ground level, and yellow pan traps elevated to
the rice canopy were compared in effectiveness of sampling chalcicid and pteromalid parasitoids [162].
Sweep-netting and ground-level yellow pan traps collected the most parasitoids overall and the most
pteromalids, whereas sweep-netting collected the most chalcidids. Elevated yellow pan traps were
clearly the least effective method overall, but comparison of pan trap and sweep-netting collection effort
is difficult. Sweep-netting, yellow pan trap, and Malaise trap collections of parasitic Hymenoptera
were compared at southern India urban sites disturbed by human activities and cattle grazing. Among
platygastrids, which were identified to genus level, Malaise traps had the highest capture rate overall,
but results varied among genera [163]. For all parasitic Hymenoptera collected, each trap was effective
for particular taxa, and it was concluded that a combination of these trap types would be best for
comprehensive collections [164]. Malaise traps, yellow pan traps, and flight intercept traps were also
compared in secondary tropical deciduous forest on the Caribbean island of Dominica [165]. Yellow
pan traps collected the greatest numbers, but relatively low diversity because of the dominance of
a few species of diapriids. Malaise traps collected the greatest richness (based on morphospecies)
and diversity, while flight intercept traps collected relatively low abundance and richness. Again,
comparison of collection effort among different methods is problematic.
Aculeate wasps are also potentially important biological control agents in agroecosystems [166–168],
and several of the above trapping methods have been used to sample these wasps in a variety
of habitats. Malaise traps and sweep nets have been used to collect the crabronid Bembecinus
quinquespinosus (Say) in a study of male mating and mate location [169], and Malaise traps, sweep nets,
and pan traps were used in faunistic surveys of sphecid and crabronid wasps in Iran [170,171].
The Diptera includes many potentially important natural enemies of agricultural pests.
Tachinids (Diptera: Tachinidae) have shown potential for biological control of some agroecosystem
pests [172–175], and can be collected using a variety of methods. Tachinid specimens in the diverse
subfamily Exoristinae have been recorded as collected in North Korea using sweep net and yellow pan
traps [176]. Tachinids comprised 23% of overall parasitoid captures in Malaise traps in Georgia, USA
coastal plain loblolly pine plantations, and the tachinid Lixophaga mediocris was the most abundant
parasitoid of the loblolly pine pest Nantucket pine tip moth, Rhyacionia frustrana (Scudder), collected
by this method (72% of total) [158]. Many species of syrphid flies (Diptera: Syrphidae) are also
beneficial, the larvae as natural enemies and adults as pollinators. Syrphids were studied as landscape
indicators in agroecosystems in Italy using Malaise traps and yellow sticky traps [177]. Malaise traps
collected the greatest numbers, but some species were collected only by sticky traps, some of the latter
in large numbers. Robber flies (Diptera: Asilidae) are voracious predators that can be sampled via
targeted netting and Malaise traps [178–180]. In Illinois, USA restored tallgrass prairie and adjacent
deciduous forest, Malaise traps collected 26 species and 0.35 robber flies/trap/day; approximately
Insects 2018, 9, 170 15 of 27

85% of estimated minimum asymptotic species richness was collected [178,179]. Studies on sampling
and impacts of predatory flies and aculeate wasps in agroecosystems are needed.

3.3.2. Assessing Parasitism and Predation

Unlike most predation events in which little or no sign of the prey remains, infection by parasitoids
can often be detected and estimates of parasitism rates derived. Immature stages of many pest insects
can be collected and placed in rearing chambers; the relative proportions of parasitoid and pest
adults that emerge can be used to calculate an estimate of parasitism rates [158,181–183], sometimes
referred to as “apparent parasitism” [184]. Parasitism rates may also be estimated by dissection of
the hosts [185,186]. The first method (rearing) may be complicated by failure of some parasites and
hosts to emerge. This may necessitate dissection of these individuals, particularly if these emergence
failures could potentially affect the parasitism estimate (either parasitoid or host relatively more
likely to successfully emerge and be counted, or different species of parasitoids vary in emergence
success). Parasitism rate estimates can also be complicated by life histories of some parasitoid taxa.
Hyperparasitism can cause the impacts of primary parasitoids to be underestimated, whereas multiple
emerges of parasitoids from a single host (associated with gregarious parasitoids or polyembryony)
can lead to overestimation of parasitism rates if not taken into account. Identification of parasitoids
based on dissections may be difficult depending on the condition or the life stage of the parasitoid.
Parasitism by Trichogramma egg parasitoids can be detected based on the blackening of the
vitelline membrane of the parasitized egg [187], and this marker has been used to estimate parasitism
rates of a variety of lepidopteran pests, including the Nantucket pine tip moth, R. frustrana [188],
tomato leaf miner, Tuta absoluta (Meyrick) [189], imported cabbageworm, Pieris rapae (L.) [190],
and diamondback moth, Plutella xylostella (L.) [191]. This blackening takes two or more days to
occur [187], so very recently parasitized eggs will probably not be detected using this method.
Assessments of parasitism based strictly on proportion of black eggs will not provide information
on species-level parasitism by Trichogramma unless there is good information on which species are
present in the environment. A subsample of parasitized eggs may be used for rearing of adult
Trichogramma for species-level identifications to obtain information on species present and their relative
abundances [188]. Species-level identifications of Trichogramma are difficult and generally require
examination of male genitalia, meaning mounting on slides and examination by a specialist will be
necessary for reliable identifications.
Predation on crop pests can be difficult to detect, let alone estimate, but research on predation
on crop pests has made great strides in recent years. Predation has been studied in a variety of
ways, including video recording [192], use of sentinel prey [193], and use of markers and analysis of
predators for prey remains, including molecular methods for analysis of predator gut contents [194].
Artificial caterpillars made of modeling clay have been used to assess predation in insecticide treated
vs. untreated cotton plots in Uganda [195], and in vetch and barley cover crops in Italy [196].
This method allows identification of predators reliably at course taxonomic levels (bird, mammal,
and arthropod) [197]. Approaches for assessing natural enemy impacts in agroecosystems have been
reviewed recently [198,199].

4. Conclusions and Further Considerations

Beneficial arthropods comprise a wide diversity of taxa and life histories, and the methods available
to sample them are accordingly diverse as well. Any sampling method will have inherent advantages and
limitations (Table 1), and it is essential that researchers be aware of these so that results can be properly
interpreted. Different sampling methods for the same taxonomic group will often yield different results.
This means that consistency in methodology is essential for results to be comparable. It also means results
of different sampling methods may be complimentary to an extent, and that use of multiple trapping
methods may give more complete results than use of a single method. This is particularly important in
studies focusing on diversity. Unfortunately, in the vast majority of cases we do not have information
Insects 2018, 9, 170 16 of 27

on the “true” faunal composition which could serve as a point of reference with which to compare our
sampling methods. However, multiple sampling methods should increase completeness to the extent
that the results of the different methods are nonoverlapping. More research is needed on development
of novel sampling methods for beneficial arthropods and comparisons of the different methods.
Since most invertebrate monitoring programs rely heavily on lethal sampling, potential effects of
monitoring on beneficial arthropod abundance and diversity are a concern. Only a few studies have
specifically addressed effects of lethal sampling, and most of these focus on vertebrates, including
shrews [200], lizards [201], and small mammals [202]. Among beneficial arthropods, potential impacts
of lethal sampling on bees have been examined [203]. These studies have consistently found no
evidence for long-term negative impacts on these communities. Even so, researchers should try to
avoid sacrificing excessive numbers of specimens. In studies addressing beneficial arthropod diversity,
a predetermined point beyond which sampling is unnecessary can be established based on estimates of
species richness [179,204,205], although for many arthropod taxa a major challenge is the on-the-spot
specimen identifications that would be required.
It is also important to note that many sampling methods will produce incidental captures, or
“bycatch”. While this bycatch may be unimportant for the study at hand, it could contain specimens
of concern for pest management, or of research or conservation interest. For instance, pitfall trap
studies have yielded important information via incidental bee captures in coastal sage scrub habitats
of southern California [206] and in the Palouse Prairie of eastern Washington and northwestern Idaho,
USA [207]. Conversely, Malaise traps with a collection container at the base have been successfully used
in conjunction with pitfall traps to sample carabids in seasonally flooded hardwood forest canopy gaps;
use of pitfall traps alone would have resulted in a 38% reduction in species richness [208]. As these
researchers note, flight is an important dispersal mechanism in many carabid species, and macropterous
species are often predominant in disturbed habitats [209–212]. This suggests that Malaise traps or
perhaps less expensive flight interception traps could be useful in augmenting pitfall trap collections
of carabids in agroecosystems. Malaise traps can also be used to effectively sample spiders, as shown
in a study of spider diversity in peatland and wet grassland across Ireland [213]. In this study, Malaise
trap collections were to a great degree complimentary with pitfall trap collections. As these authors
observe, Malaise traps may not be suitable as a sole method of sampling spiders, but traps in use to
collect insects may also provide valuable data on the spider fauna. While the above studies were done
in nonagricultural environments, they underscore the potential for bycatch or nontarget captures to
contribute important and perhaps unexpected information. Bycatch not intended to be used can be
made available to appropriate specialists to avoid waste [214].
It should also be noted that correct identification of arthropod specimens is often much more
challenging and time-consuming than the sampling itself. Help from appropriate specialists is often
needed, and it is wise to explicitly budget for identification services. Furthermore, collected specimens
will require care and management. It is wise to construct a plan for specimen identification, data entry
and organization, and collection management before sampling begins.
As habitat destruction, climate change, and other anthropogenically-driven changes continue to
unfold, intensive agricultural practices will face new challenges. If climate change leads to increased
insect pest populations and changes in pest geographic ranges, it will be difficult to resist the temptation
to respond with even greater reliance on insecticides. However, such a response would likely contribute
to the already high rate of biodiversity loss, including loss of beneficial arthropod diversity. An
increased role for native pollinators and natural enemies in agroecosystems would be one strategy for
decreasing reliance on insecticides. However our knowledge of these beneficial arthropods is only as
good as the reliability of our sampling. Reliable sampling and monitoring methods for these beneficial
arthropods will be essential for assessing the effects of environmental disturbances and effectiveness
of conservation efforts. Hopefully this paper provides information that will prove useful in choosing
appropriate methods for assessing beneficial arthropod health and effectiveness in agricultural systems.
Insects 2018, 9, 170 17 of 27

Table 1. Beneficial arthropod sampling methods included in this paper, focus, type of estimate, relative cost and labor, and comments on advantages and limitations of
each method.

Method Focus Absolute or Relative Estimate Cost Labor Comments

Bowl traps Bees, wasps, flies Relative Low Low
Blue vane traps Bees, wasps, flies Relative High Low Bulky to transport
Potential oversampling of large bees
Trap-nests Trap-nesting bees and wasps Relative Low High High selectivity
Targeted netting w/baits Orchid bees Relative High High High selectivity
Collector abilities can vary
Malaise traps Flying insects Relative High Low High and diverse yield
Significant setup time
Potential damage due to wind or vandalism
Targeted netting Flying insects; insects on vegetation Relative Low High High selectivity
Collector abilities can vary
Sweep-netting Arthropods on vegetation Relative or absolute Low High High and diverse yield
See a past paper [143] for absolute estimates
Direct counts on vegetation Arthropods on vegetation Relative or absolute Low High High selectivity
Significant training may be required
Shaking/beating vegetation Arthropods on vegetation Relative or absolute Low High May damage plants
Suction samplers Plant and litter arthropods Relative or absolute High High High and diverse yield
Pitfall traps Epigeic arthropods Relative Low Low Significant setup time
High and diverse yield
Sensitive to rainfall
Potential animal disturbance
Emergence traps Epigeic arthropods Absolute High High May affect microclimate
Sampling excludes migrants
Soil flooding Epigeic arthropods Absolute Low High
Microhabitat removal and extraction Epigeic arthropods Absolute Low High
Cryptozoan boards Epigeic arthropods Relative Low High Placement duration may affect yield
Sticky traps Parasitic Hymenoptera Relative Low Low Baits increase expense
Estimates of parasitism Parasitoids Relative Low High High selectivity
Direct measure of natural enemy effects
Estimates of predation Predators Relative Variable High Direct measure of predation
Insects 2018, 9, 170 18 of 27

Funding: This research received no external funding.

Acknowledgments: I would like to thank the several anonymous reviewers whose comments helped improve
the manuscript. I also thank Western Illinois University for administrative support of this project.
Conflicts of Interest: The author declares no conflicts of interest.

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