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Review
Weed–Insect Interactions in Annual CroppingSystems
MaryE.Barbercheck1,3, and JohnWallace2
1Department of Entomology, Penn State University, University Park, PA 16802, 2Department of Plant Science, Penn State University,
University Park, PA 16802, and 3Corresponding author, e-mail: meb34@psu.edu
Subject Editor: GadiV.P.Reddy
Received 2 October 2020; Editorial decision 21 December 2020
Abstract
Agricultural production is increasingly viewed as more than a source of food, feed, fiber and fuel, but also as a
system of interdependent biotic and abiotic components that interact to produce ecosystem services and disser-
vices. Weeds and insects are commonly viewed as non-desirable components of agroecosystems that should
be managed. However, weeds can also provide benefits to cropping systems, such as providing resources and
habitat to pollinators and other beneficial arthropods. This review on weed–insect interactions in annual cropping
systems focuses on functional interactions within the context of regulating and supporting ecosystem services
and disservices. Regulating services are those that act as regulators of the environment, such as weed–insect
interactions that contribute to the regulating services of pollination and biological control, but also contribute to
the disservices of crop and cover crop seed predation, and maintenance of insect pests and insect-transmitted
phytopathogens. Supporting services include habitat and biodiversity that are necessary for the production and
maintenance of the other types of ecosystem services. Here we review the impacts of weed–insect interactions
as a component of biodiversity. We conclude by identifying some knowledge gaps that hinder our understanding
of trade-offs when seeking to improve net positive ecosystem services in annual cropping systems.
Graphical Abstract
Positive and negative interactions among insects and weeds. Credit: Nick Sloff.
Annals of the Entomological Society of America, 114(2), 2021, 276–291
doi: 10.1093/aesa/saab002
Advance Access Publication Date: 9 February 2021
Review
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277Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
Key words: annual agroecosystem, weed, insect, ecosystem service, agronomic crop
Agricultural production is increasingly viewed as a system of inter-
dependent biotic and abiotic components that interact to produce
ecosystem services and disservices (Millenium Ecosystem Assessment
2005). In general, ecosystem services are classied into four
types: provisioning, regulating, supporting, and cultural services.
Agroecosystems both provide and consume ecosystem services that
result in positive or negative impacts on human well-being (Zhang
etal. 2007, Shackleton etal. 2016). Some ecosystem services and dis-
services are clearly distinguishable. For example, ecosystem services
provided by agriculture include provisioning of food, feed, ber and
fuel, regulation of soil, water, and air quality, and biodiversity that
can contribute to regulation of pest organisms, such as insect pests
and weeds (Power 2010). Depending on management, agroeco-
systems can create numerous disservices, including loss of wildlife
habitat, creation of pest problems, nutrient runoff, sedimentation of
waterways, and pesticide intoxication of non-target species and con-
tamination of the environment.
Depending on context and grower goals, ecosystem services and
disservices can be produced by the same group of organisms. For
example, weeds are typically viewed as a non-desirable component
of agroecosystems that should be managed and their populations
limited because they can decrease crop yields, mechanically inter-
fere with harvest machinery, contaminate harvests and decrease
value of the harvested crop (Milanović etal. 2020). However, weeds
and their seeds can also provide supportive and regulating services
within crops. For example, weeds can provide ground cover that can
help to reduce soil erosion and N loss (Wortman 2016), much like
a winter cover crop, and support insect natural enemies (Diehl etal.
2012), pollinators (Gibson etal. 2006, Bretagnolle and Gaba 2015,
Blaix etal. 2018), birds (Thomas etal. 2001), and increase biodiver-
sity at the eld and landscape level (Marshall etal. 2003, Franke
etal. 2009, Storkey etal. 2014).
Earlier reviews have addressed the interactions between weeds
and insects in annual agroecosystems in various contexts. Norris
and Kogan (2000, 2005) reviewed the ecology of weed–insect inter-
actions and the consequences of these interactions for IPM (Norris
and Kogan 2000, 2005). Schroeder etal. (2005) examined the impact
of crop pests on weeds to examine the hypothesis that agricultural
elds are dominated by plant species that are tolerant or resistant to
the endemic insect complex. Capinera (2005) reviewed the relation-
ships between insect pests and weeds from an evolutionary perspec-
tive. Bàrberi etal. (2010) reviewed the inuence of spatial scale on
the functional relationships between weeds and arthropods in agro-
ecosystems. More recently, Harvey et al. (2010) and Sands (2018)
reviewed the interactions between invasive plants and plant-feeding
insects and consequences for conservation.
Regulating and Supporting Ecosystem
Services and Disservices
Scientists and the general public have become more aware of the value
of ecosystem services associated with weeds and insects and the crisis
of declining biodiversity, especially in agricultural habitats (Marshall
etal. 2003, Losey and Vaughan 2006, Yang and Gratton 2014, Blaix
etal. 2018, Sánchez-Bayo and Wyckhuys 2019, Smith etal. 2020).
Considering the net effects of a management system on trade-offs
between ecosystem services and disservices associated with groups
of organisms is crucial, especially under conditions of additional
stresses imposed by climate change. For the purposes of this review,
we will focus on functional weed–insect interactions in annual crop-
ping systems within the context of regulating and supporting services
(Millennium Ecosystem Assessment 2005). Regulating services are
those that act as regulators of the environment; here, we include
how weed–insect interactions affect pollination and biological con-
trol of insects and weeds. Regulating disservices associated with
weed–insect interactions include weed impacts on crop and cover
crop seed predation, and on promoting populations of insect pests
and prevalence of insect-transmitted phytopathogens. Supporting
services provide habitat and maintain biodiversity that are necessary
for the production and maintenance of the other ecosystem func-
tions, such as food provision, nutrient cycling, and microclimate
regulation (Millennium Ecosystem Assessment 2005). The demand
for provisioning services (i.e., yield) in agroecosystems often comes
at the expense of other ecosystem services, including those critical
to supporting services, such as pest regulation and crop pollination
(Foley etal. 2005, Bennett etal. 2009, Bretagnolle and Gaba 2015).
We conclude by identifying some knowledge gaps that hinder our
understanding of trade-offs when seeking to improve net positive
ecosystem services in annual cropping systems.
Insects and Weeds in Annual CroppingSystems
Both weeds and insects have been intensively and extensively studied
as pests with negative impacts on crop productivity and quality.
Plants are the foundation of the green food web as primary produ-
cers, and those considered to be weeds can comprise a considerable
part of the plant community in agroecosystems (Zou et al. 2016,
Neher and Barbercheck 2019). In annual agroecosystems, crop yield
loss from weed interference is a signicant contributor to farm prof-
itability. Recent syntheses of eld experiments suggest that in the
absence of weed control practices, grain corn and soybean yield loss
would exceed 50% (Soltani etal. 2016, 2017). In addition to the
direct impact of weeds on crop yields through competition for space,
nutrients, water, and light, weeds also indirectly affect crop produc-
tion via their inuence on insects, and by harboring phytopathogens
(Capinera 2005). However, plants also host the prey of omnivores
and carnivores. Therefore, the structure, composition, and manage-
ment of vegetation, including weeds, within cultivated elds and
eld margins greatly inuence biodiversity in agricultural land-
scapes. Weeds contribute to the biodiversity of agroecosystems and
have the potential to support the delivery of regulating ecosystem
services by increasing benecial arthropods involved in pollination
and biological control (Petit etal. 2011, Blaix etal. 2018, Storkey
and Neve 2018). The extent of the effects of weeds on agroecosystem
productivity is inuenced through functional traits such as biomass,
plant height, canopy and root size/architecture, leaf dry matter con-
tent, and reproductive phenology (de Bello etal. 2010, Lavorel etal.
2013). Attempts have been made to consider the management re-
quired to balance weed-associated ecosystem services and disservices
in agroecosystems (DiTommaso etal. 2016, Smith etal. 2020).
Plants, including weeds, provide many resources to insects in
agroecosystems, e.g., food, shelter, and sites for overwintering and
reproduction. Plant-feeding insects are an important cause of crop
yield losses worldwide (Oerke 2006, Dhaliwal etal. 2015, Savary
etal. 2019) and these losses are predicted to increase in response to
climate change (Capinera 2005, Deutsch etal. 2018). Plant-feeding
arthropods are typically grouped into types based on diet breadth (Ali
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278 Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
and Agrawal 2012). Those whose diet breadth is limited to only one
or a few closely related plant taxa are considered highly specialized,
or monophagous, whereas those that feed on several plant species
in more than one plant family are considered generalists, or pol-
yphagous. Some species, whose diet breadth is usually restricted to
several species within a plant family are considered oligophagous.
The taxonomic and phenological similarity between weeds and a
crop therefore becomes an important element in predicting potential
for damage to crops by weed-feeding insects (Capinera 2005, rev. in
MacLaren etal. 2020). Those plant-feeding insects that can feed on
multiple plant species in a particular family are likely to be adapted
to attack both crops and weeds in the same family. For example,
in feeding preference assays, larval stalk borer (Papaipema nebris
(Guenee) [Lepidoptera: Noctuidae]) a pest of corn, preferred cool-
season perennial grasses compared with broadleaf weeds (Highland
and Roberts 1987). Capinera (2005) suggested that practices that
break the taxonomic link between weeds and crop plants can reduce
the movement of specialist and oligophagous insects from weeds to
crop plants.
Weed and Insect Communities Shift in Response to
DisturbanceRegimes
Annual cropping systems are characterized by their high level of dis-
turbance (Crews etal. 2016), and pest management is one of the
primary sources of chemical and physical disturbances in annual
cropping systems (Tooker etal. 2020). Weed management in com-
modity crop production typically employs a crop protection mindset
and is characterized by multiple herbicide applications containing
multiple modes-of-action. In response to overwhelming mortality
pressure from broad-spectrum herbicides, diversity of arable weed
communities in intensively managed systems is declining (Potts etal.
2010b, Petit et al. 2011, 2015; Meyer et al. 2013). Extensive use
of broad-spectrum weed control tactics often results in signicant
population increases of a limited number of weed species adapted to
weed control and disturbance regimes (Cardina etal. 2002, Murphy
etal. 2006). For example, no-till management changes the compos-
ition of the weed community, promoting annual grasses and per-
ennial weeds with deeper plant roots (rev. in Rollin et al. 2016).
Similarly, frequent and intensive disturbance from tillage and culti-
vation favor the dominance of a few competitive species. Herbicide-
resistant weed species are an extreme case of evolved adaptation
followed by rapid population increase. In addition to direct impacts
of herbicide- and tillage-based weed management on crop product-
ivity, additional economic and environmental costs can arise from
these management practices, such as increased risk of non-target ef-
fects associated with herbicides (Zaller and Brühl 2019), and for soil
degradation where extensive cultivation is used to suppress weeds
(Logan etal. 1991).
The marked decline in weed and insect diversity has contributed
to the decline in the functional biodiversity of ora in agroecosys-
tems, which has important implications for trophic interactions
and ecosystem services (Marshall etal. 2003, Losey and Vaughan
2006, Yang and Gratton 2014, Blaix et al. 2018, Sánchez-Bayo
and Wyckhuys 2019, Smith et al. 2020). Many of the weed spe-
cies that are known to support farmland birds or insects (Storkey
2013, 2014; Eraud etal. 2015), e.g., lambsquarters, Chenopodium
album L. (Amaranthaceae), black bindweed, Fallopia convolvulus
(L.) Á. Löve (Polygonaceae), prostrate knotweed, Polygonum
aviculare L. (Polygonaceae), lady’s thumb, Polygonum persicaria
L.(Polygonaceae), wild mustard, Sinapis arvensis L.(Brassicaceae),
and common chickweed, Stellaria media (L.) Vill. (Caryophyllaceae)
have decreased signicantly over the last few decades (Fried etal.
2008, 2009a,b, 2012). Storkey etal. (2012) attribute the decline of
weed abundance and diversity in arable elds to increased intensity
of management, including increased crop plant density, decreased
crop diversity, increased fertilizer and herbicide use, and more ef-
cient seed cleaning.
Regulating Services of Weed–Insect Interactions:
Pollinators and Pollination
Regulating services regulate processes in the environment, e.g., pol-
lination and control of plant-feeding arthropods in agroecosystems.
One of the most important ways that insect–plant interactions posi-
tively affect provisioning services (e.g., yield) in agroecosystems is
through pollination (Petit et al. 2011, 2015; Hanley et al. 2015;
Sutter et al. 2017; Blaix etal. 2018). Populations of pollinators,
including wild bees, honey bees, and bumble bees are declining in
agricultural landscapes (Van Engelsdorp etal. 2008; Winfree etal.
2008; Ellis etal. 2010; Potts etal. 2010a,c; Cameron et al. 2011;
Gonzalez-Varo etal. 2013). Pollination by insects is vital for the ma-
jority of cultivated and wild plants (Ollerton etal. 2011). Klein et
al. (2006) estimated that 70% of 57 crops grown worldwide de-
pend on insect pollination, and pollination services to crops has been
valued at 153 billion euros annually worldwide (Gallai etal. 2009),
and more than 18 billion dollars in the United States (Mäder etal.
2011). Numerous studies have demonstrated the benets of weeds in
supporting pollinators and crop pollination (rev. in Bretagnolle and
Gaba 2015, Blaix etal. 2018). Flowering weeds can support pollin-
ator populations and pollination through the provision of pollen and
nectar to bees and other insect pollinators. Outside of bloom periods
of mass-owering crops, pollinators must rely on other resources,
such as wildowers and weeds, which are not usually as abundant
and dense as crops in intensively managed systems. Many owering
plant species, most of which are weeds, in natural and semi-natural
habitats are important food resources for pollinators (Requier etal.
2015, Sutter et al. 2017). In the period between mass-owering of
oilseed crops in cereal systems, honey bees forage almost exclusively
on weeds (Morandin and Winston 2006, Requier etal. 2015).
There is a strong correlation between plant diversity and bee
diversity (Biesmeijer etal. 2006, Hopwood 2008, Holzschuh etal.
2010) and weeds can supply and diversify nectar in agricultural
landscapes dominated by agronomic crops, which often offer low
amounts of nectar compared with other habitats (Baude etal. 2016).
Greater and more diverse food resources associated with weeds
positively affect pollinator diversity (Carvalheiro etal. 2011, Pettis
etal. 2013), and diverse pollinator communities improve pollination
services (Klein etal. 2006, Hoehn etal. 2008). In addition to sup-
porting crop production, enhanced pollinator communities support
other ecosystem services such as honey production, weed regulation,
and improved survival of wild ora (Bretagnolle and Gaba 2015).
Regulating Disservices of Weed–Insect Interactions:
Pollinators and Pollination
Conservation of natural and semi-natural eld-edge habitats and
in-eld refuge strips in agricultural landscapes can support man-
aged and wild pollinator populations by providing food resources
(Garibaldi et al. 2011, Requier et al. 2015, Kovács-Hostyánszki
et al. 2017). However, management strategies to conserve insect
pollinators in agroecosystems can result in trade-offs. One trade-off
associated with weeds as a resource for pollinators is competitive
interactions between managed and wild bees. Managed and wild bees
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279Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
interact in trophic networks in complex ways and these interacting
networks affect crop pollination, depending on weed communities.
For example, weed abundance and proximity to crops can affect
the abundance of wild bees, which may compete with honey bees
for weed pollen and nectar (Carvalheiro etal. 2011). If crops rely
on insect pollination and wild bees displace honey bees from weeds
and onto crops, then crop production may be increased. However, if
owering crops are not available to honey bees that have been dis-
placed from weeds, local resources for honey bees may be reduced.
Insect pollinators can promote the reproduction and persistence
of some weed species, even those that are predominantly self- or
wind-pollinated (Marshall et al. 2003, Sutherland 2004, Nicholls
and Altieri 2012, rev. in Rollin et al. 2016). The persistence of
most weed species in annual cropping systems is largely driven by
insect pollination, and in some intensively managed agricultural
landscapes, weeds can account for the majority of pollen resources
(Requier etal. 2015). Weed seed production can be improved with
pollination even in self-compatible species (Morales and Galetto
2003). Therefore, the support of weed populations may be a positive
service to pollinators but a disservice to farmers whose yields may
be negatively impacted by weeds. Aweed-management strategy is
required that provides sufciently abundant weeds to support pollin-
ators but not so abundant that crop yield is lost to weed competition.
Regulating Services of Weed–Insect Interactions:
Support of NaturalEnemies
Weeds contribute to the biodiversity of agroecosystems, and as
such have the potential to support the delivery of regulating eco-
system services in agroecosystems by increasing benecial arthro-
pods involved in biological control (Norris and Kogan 2000, 2005;
Gurr etal. 2016, 2017; Holland etal. 2016; Amoabeng etal. 2020;
Kleiman etal. 2020; Shields etal. 2019). The regulating ecosystem
service of biological control of pest insects contributes considerably
to agricultural productivity (Naranjo etal. 2015) and the value of
this service has been conservatively estimated at $4.5 billion an-
nually (Losey and Vaughan 2006). Many authors have reviewed
the importance of landscape complexity and vegetational diver-
sity for enhancing populations of benecial arthropods in agri-
cultural landscapes (e.g., Landis etal. 2000, 2005; Andow 1991;
Tscharntke et al. 2008; Letourneau etal. 2011). Heterogeneous
landscapes with a diversity of habitat types generally increase bio-
diversity and ecosystem services and functions (Tscharntke etal.
2008, Chaplin-Kramer etal. 2011), although the benets of diver-
sication practices on local communities can be strongly mediated
by regional species pools (Gering and Crist 2002). In simplied
agricultural landscapes, weedy or non-crop habitats can provide re-
sources such as oral nectar and pollen to meet or complement the
nutritional requirements of natural enemies, and alternate prey, as
well as refuge, nesting, and overwintering sites (Landis etal. 2000,
2005). For example, in corn, parasitism of Helicoverpa armigera
Hübner (Lepidoptera: Noctuidae) eggs by Trichogramma chilonis
Ishii (Hymenoptera: Trichogrammatidae) was positively correlated
to the proportion of non-crop habitat diversity at 0.5 and 1.0 km
radius scales (Liu etal. 2016).
Research on conservation biological control of arthropod pests
suggests that the positive effect of plant diversity, to which weeds
contribute, on biological control is supported by theories describing
multiple mechanisms. These include the enemies hypothesis, which
predicts that natural enemies will be augmented in diversied agro-
ecosystems and thereby control herbivores more effectively (Risch
1981, Blubaugh etal. 2021); the resource concentration hypothesis
which posits that that the apparency of a crop to an arthropod
pest is reduced by reducing the concentration of host plants (Root
1973); by diversion of pest species away from crops (Capinera
2005); or by creating an associational resistance to pest infestation
(Ninkovic etal. 2009). However, the effect of the enhancement of
natural enemy populations on actual pest control and crop yield is
not always measured (Letourneau and Bothwell 2008, Holland etal.
2016, Sutter etal. 2017, Blaix etal. 2018, Kleiman etal. 2020).
Blaix etal. (2018) reviewed the contribution of weeds to insect
pest regulation through multiple mechanisms and identied that
the most common way that weeds benet the reduction of insect
pest populations is by providing natural enemies of pests resources
in or around cultivated elds, supporting the natural enemies hy-
pothesis (Risch 1981). Several laboratory and greenhouse experi-
ments have measured the time that benecial arthropods spend
foraging on owers or have analyzed their preference for owers
of particular species (Blaix et al. 2018). For example, Belz etal.
(2013) found that the parasitoid, Microplitis mediator Haliday
(Hymenoptera: Braconidae) preferred candytuft, Iberis amara
L.(Brassicaceae) and cornower, Cyanus segetum Hill (Asteraceae)
over buckwheat, Fagopyrum esculentum Moench (Polygonaceae),
and Queen Anne’s lace, Ammi majus L.(Apiaceae). The pink lady
beetle, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae),
preferred to deposit eggs on velvetleaf, Abutilon theophrasti Medik.
(Malvaceae), compared with eight other broad-leaved annual weeds,
including species in the plant families Amaranthaceae, Asteraceae,
Euphorbiaceae, Malvaceae, and Solanaceae (Grifn and Yeargan
2002). Araj et al. (2019) investigated the effects of oral resources
from two common brassicaceous weed species, shepherd’s purse,
Capsella bursa-pastoris (L.) Medik. and white rocket, Diplotaxis
erucoides (L.) DC., on Eretmocerus mundus Mercet (Hymenoptera:
Aphelinidae), a parasitoid of the silverleaf whitey, Bemisia tabaci
Gennadius (Hemiptera: Aleyrodidae). Adults of E.mundus that were
provided owers of shepherd’s purse and white rocket survived 2.8
and 3.1 times longer, respectively, than those in a water-only con-
trol. Parasitoid longevity, egg load, fecundity and parasitism rate
of B. tabaci were also greater when they were provided with weed
owers compared to the control.
Control of arthropod pests by natural enemies can vary con-
siderably and the relative importance of non-crop habitat for sup-
porting biological control can also vary depending on the crop, pest,
natural enemies, management, and landscape structure (Tscharntke
et al. 2016). In-eld weeds and weedy eld margins that provide
oral resources have been associated with increased abundance and
diversity of benecial insects and reductions in pest numbers. In a
meta-analysis of 60 studies that included 29 comparisons of elds
with either high or low in-eld plant diversity, in-eld plant diver-
sity strongly increased arthropod abundance and richness, but had
weaker effects on evenness (Lichtenberg etal. 2017). The positive
effects of in-eld plant diversication were greatest for pollinators
and predators and was not signicant for herbivores. The authors
concluded that management that increases in-eld plant diversity
can promote key ecosystem service providers without increasing pest
herbivore densities (Lichtenberg etal. 2017). Albajes etal. (2009) re-
ported that natural enemy diversity increased up to 213% in weedy
compared with weed-free plots. Populations of a key pest of rice,
the rice brown planthopper, Nilaparvata lugens (Stål) (Hemiptera:
Delphacidae), were signicantly lower in a nectar-producing plant
intervention treatment than in the control treatment without nectar-
producing plants (Gurr etal. 2016). Smith etal. (2020) investigated
the functional link between weeds and invertebrates and the poten-
tial for these to provide ecosystem services such as pest control in
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280 Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
wheat, Triticum aestivum L.(Poaceae). In that study, the weed spe-
cies most frequently shown to predict the invertebrate community
included several weeds typical of temperate agroecosystems from
several plant families, including the Amaranthaceae, Asteraceae,
Boraginaceae, Brassicaceae, Caryophyllaceae, Lamiaceae,
Papaveraceae, Plantaginaceae, Poaceae, and Primulaceae. Smith etal.
(2020) concluded that even in an intensively grown cereal system, ar-
able weeds can play an important role in maintaining and restoring
invertebrate populations and suggested that 10% weed cover is
needed to support invertebrates that provide ecosystem services.
Regulating Services of Weed–Insect Interactions:
Granivory
Weed Seed Predation
Weed management is a challenge in agroecosystems due, in part, to
the weed seedbank, which maintains the persistence of annual spe-
cies within the weed community (Fox etal. 2013). Limiting the num-
bers of viable seeds in the seedbank through cultural practices is a
critical component of sustainable weed management. Consequently,
the role of granivorous animals in weed seed consumption, a regu-
lating ecosystem service, is of interest due to their prominence in
agroecosystems (rev. in Kulkarni 2015, Sarabi 2019). Weed seeds are
an important food resource for some arthropod species in annual
agroecosystems, most commonly carabid beetle species (Petit etal.
2011, 2015), crickets (Carmona etal. 1999, Westerman etal. 2003,
White etal. 2007), and ants (Pearson etal. 2014, Penn and Crist
2018). Insect weed seed predators can contribute to the reduction
of weed populations by consuming seeds before seed dispersal (pre-
dispersal predation) or after the seeds have been shed and are on
the soil surface (post-dispersal). Most of the research on weed seed
predation in temperate annual agroecosystems has focused on post-
dispersal weed seed predation.
Several studies have shown that individual management prac-
tices such as tillage, crop type, fertilizer, and pesticide inputs can
have substantial impacts on weed seed predation (rev. in Menalled
etal. 2008). The timing, frequency and intensity of tillage practices
can have a signicant effect on seed predation rates due to their
impact on the location of weed seeds in the soil prole. Soil con-
servation practices that reduce tillage (conservation or zero tillage)
favor greater weed seed predation due, in part, to the high avail-
ability of seeds at the soil surface or at shallow soil depths (Kulkarni
etal. 2015). In tilled systems, seed predation on the soil surface de-
pends on the time lag between seed shed and incorporation in soil
(Westerman etal. 2003). Even though many natural and manage-
ment factors affect weed seed predation, it has been widely dem-
onstrated to be one of ‘many little hammers’ that can contribute to
weed suppression in annual agroecosystems (Liebman and Gallandt
1997, Gallandt 2006, Sarabi 2019).
Pre-dispersal Weed Seed Predation
Although biological control of weeds using pre-dispersal weed seed
predators has been undertaken in many countries, deployment of
this approach has been curtailed over the past decades in the United
States because of concerns about non-target impacts such as adap-
tation of insects to attack crops and other valuable plant species,
and the resulting requirements for stringent testing of candidate
biological control agents before release (Van Driesche etal. 2010,
Schwarzländer etal. 2018a,b, Hinz etal. 2020). Most pre-dispersal
seed predators occur in the Diptera, Lepidoptera, Coleoptera, and
Hymenoptera and are specialists on one plant species, genus, or
family (Van Driesche etal. 2010). Much of the literature on pre-
dispersal weed seed predation by insects is focused on biological
control of invasive aquatic or rangeland and pasture weeds (Van
Driesche etal. 2010; Schwarzländer et al. 2018a,b; Day and Witt
2019; Hinz etal. 2020).
Natural control of weeds through pre-dispersal weed seed pre-
dation in annual agroecosystems can be signicant but variable,
differing between and within years and crop management (rev. in
Sarabi 2019). Examples of pre-dispersal predation by specialist in-
sects common to annual cropping systems in the United States that
provide natural control include velvetleaf, lambsquarters, pigweeds,
and Canada thistle (Kremer and Spencer 1989, Landis etal. 2005).
DeSousa et al. (2003) reported larval Coleophora lineapulvella
Chambers (Lepidoptera: Coleophoridae) feeding on the maturing
seeds of redroot pigweed, Amaranthus retroexus L.This insect also
feeds on the seeds of smooth pigweed (A.hybridus L.) and powell
amaranth (A.powellii S.Wats.) (Weaver and McWilliams 1980).
Post-Dispersal Weed Seed Predation
Granivorous and omnivorous arthropods, especially crickets and
ground beetles (Coleoptera: Carabidae), can be important post-
dispersal weed seed predators (Honěk etal. 2007; Bohan etal. 2011;
Lundgren etal. 2013; Kulkarni etal. 2015, 2017). Several omniv-
orous or predominantly granivorous carabid species (Coleoptera:
Carabidae) can be important weed seed predators in temperate
zones (Thomas et al. 2001, Kulkarni et al. 2015). Field crickets
(Orthoptera: Gryllidae) consume the seeds of several common weed
species, for example, common ragweed (Ambrosia artemisiifolia L.,
Asteraceae), redroot pigweed, and crabgrass (Digitaria spp. Haller)
(Carmona etal. 1999; Westerman etal. 2003; White etal. 2007).
Ants can play an important role in seed feeding, especially in semi-
arid and arid regions (rev. in Penn and Crist 2018).
Post-dispersal weed seed predation can occur on and below the
soil surface, and predation by granivorous and omnivorous inver-
tebrates can substantially reduce the surface weed seed numbers
(Westerman etal. 2003, 2008). For example, Mauchline etal. (2005)
found greater than 70% predation of common chickweed (Stellaria
media (L.) Vill., Caryophyllaceae), prostrate knotweed (Polygonum
aviculare L., Polygonaceae), common lambsquarters (Chenopodium
album L., Amaranthaceae), and wild mustard (Sinapis arvensis
L., Brassicaceae) over a 2-wk period coincident with natural seed
rain. Several studies have examined the feeding preference of spe-
cic weed seed predators. For example, White etal. (2007) deter-
mined feeding preferences of three common species of ground
beetles: Amara aenea DeGeer, Anisodactylus sanctaecrucis F., and
Harpalus pensylvanicus DeGeer (Coleoptera: Carabidae) and the
northern eld cricket, Gryllus pennsylvanicus DeGeer (Orthoptera:
Gryllidae) and the effect of seed predation on weed emergence.
Anisodactylus sanctaecrucis, H.pensylvanicus, and female and male
G.pennsylvanicus consumed more seeds of redroot pigweed com-
pared with seeds of giant foxtail (Setaria faberi R.A.W.Herrm.);
granivory by A.aenea did not differ between these two weed spe-
cies. All the tested insects consumed fewer velvetleaf (Abutilon
theophrasti Medik, Malvaceae) seeds compared with redroot pig-
weed and giant foxtail seeds (White etal. 2007).
The magnitude of weed seedbank loss due to weed seed predation
is likely highly variable. In a greenhouse study, White etal. (2007)
determined that the carabid, A.sanctaecrucis, decreased total weed
emergence by 15%, and the eld cricket, G.pennsylvanicus, females
and males decreased weed emergence by 16 and 5%, respectively.
Emergence of redroot pigweed, but not velvetleaf or giant foxtail,
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281Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
decreased when A.sanctaecrucis and male G. pennsylvanicus were
present, whereas the emergence of all three weed species decreased
in the presence of the female G.pennsylvanicus. In eld experiments
to estimate relative contribution of vertebrate and invertebrate weed
seed predation, White etal. (2007) found that invertebrate access
reduced emergence of velvetleaf seeds by 4 to 6% and giant foxtail
seeds by 4 to 13%. Westerman etal. (2003) examined the temporal
patterns of loss of the seed of the common chickweed, lambsquarters,
and wild oat, Avena fatua L.(Poaceae) from predation in organic
cereal elds in the Netherlands. Total weed seed production varied
considerably among elds and ranged from 800 to 16,000 seeds per
m2 per year. Calculated losses from seed predation ranged from 32
to 70% when assuming continuous exposure of seeds to predators
in the period from seed shed until crop harvest. The authors suggest
that seed predation in organic cereal elds is an important factor
shaping the population dynamics of arable weeds, and that the time
of weed seed exposure and vulnerability of weed seeds to seed pre-
dation is mainly affected by variation in the timing of seed shed and
seed burial by tillage (Westerman etal. 2003). Seed burial depths
of 0.5 or 1.0 cm reduced redroot pigweed and giant foxtail seed
consumption by A.aenea and A.sanctaecrucis but not by the larger
carabid beetle, H.pensylvanicus (White etal. 2007).
Soil and residue management can affect levels of weed seed preda-
tion, even when seeds are on the soil surface. Menalled etal. (2007)
assayed invertebrate seed predation rates of fall panicum (Panicum
dichotomiorum Michx., Poaceae) and common lambsquarters and
found that activity-densities of seed-predating carabid species and
seed predation were greater in a no-till compared to conventionally-
tilled and organic systems. The carabid community structure was
distinct among the three systems and there was a strong correlation
between seed removal rates and the total number of carabid seed
predators captured in each system. Ward et al. (2011) assessed the
activity-density of two granivorous ground beetles, A. aenea and
H. pensylvanicus, in management systems that ranged in disturb-
ance frequency, crop type and aboveground biomass production.
Ground beetle activity-density was higher in systems with greater
aboveground biomass and plant diversity (i.e., summer annual cover
crops) and lower in cultivated soybean systems without covercrops.
Multiple eld studies suggest that granivorous ground beetles
aggregate in response to weed seed distributions (Honěk and Jarošík
2000, Trichard etal. 2014, Kulkarni 2017), and carabid abundance
has been associated with aboveground seed density (Frank et al.
2011). Kulkarni (2017) and Blubaugh and Kaplan (2015) observed
a signicant spatial overlap between activity-density of carabids
and patches of high weed density, with spatial association strength-
ening as crop development advanced, suggesting that weedy patches
in cropped areas contribute to biodiversity by conserving popula-
tions of carabids and weed seed predation. Ward etal. (2014) found
that activity-density of H. pensylvanicus in late summer (June to
October) peaked at the onset of giant foxtail (Setaria faberi Herrm.,
Poaceae) seed shed, highlighting the need for incorporation of man-
agement practices to support ground beetle populations to maximize
predation potential for summer annual weeds that shed seed later in
the growing season. In a eld study to compare weed seed predation
by insects, Blubaugh etal. (2016) examined the effects of vegetative
cover on weed seed predation by carabid ground beetles on common
lambsquarters seeds. The omnivorous carabids, A. sanctaecrucis
and H.pensylvanicus aggregated in weed seed patches. While both
carabid species tracked and consumed weed seeds, A.sanctaecrucis
foraged equally in both bare and vegetative cover treatment plots,
whereas H.pensylvanicus was more active in habitat with vegetative
cover compared with plots without vegetative cover. Blubaugh etal.
(2016) suggested that niche complementarity that results from con-
trasting habitat selection among seed predators reduces the likeli-
hood of predator interference and may result in more even seedbank
depletion across heterogeneous habitat types, resulting in enhanced
weed seed predation in annual agroecosystems.
While many studies have recorded the removal and consumption
of applied weed seeds or from weed seed ‘cafeterias’ by insects, rela-
tively few studies of weed seed predation include data on predation
of naturally dispersed weed seed or the actual decrease of weed pres-
sure due to seed predation under commercial growing conditions.
Evans and Gleeson (2016) measured the impact of seed predation
by ants on naturally dispersed seeds of prickly saltwort, Salsola aus-
tralis R.Br. (Amaranthaceae), in wheat and found that the removal of
ants by insecticides resulted in a doubling of S.australis plants meas-
ured 2 mo after removal of ants, demonstrating that ant predation
of naturally dispersed weed seeds limited abundance of weeds in a
commercial grain system.
Regulating Disservices of Weed–Insect Interactions:
Granivory of Crop and CoverCrops
While granivory can provide regulating services through pre-and
post-dispersal consumption of weed seeds, it can also be the source
of disservices if desired seeds, such as crop or cover crop seed, are
consumed. Agricultural practices and environmental conditions that
support populations of weed seed predators may simultaneously
benet granivorous insects that could act as crop pests (Zhang etal.
2007, Tscharntke etal. 2016). Pre-dispersal granivory can reduce
crop yield and quality, especially where the seed is the harvestable
product, e.g., grain crops. For example, larval soybean podworm,
Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), chews through
the pod to feed on developing seeds and also feeds on leaves and
owers. Several species of stink bugs (Hemiptera: Pentatomidae) can
damage and reduce yield in soybeans and other seed crops by using
their mouthparts to suck the contents from developing owers, pods,
and seeds and are major pests of oilseed crops (Koch etal. 2017).
Tschumi etal. (2018) studied the contribution of omnivorous and
granivorous invertebrates and vertebrates to regulating ecosystem
services and disservices in cereal elds and found that post-dispersal
seed predation was dominated by vertebrates, while vertebrates and
invertebrates contributed equally to predation of animal prey; how-
ever, benecial invertebrates and crop seeds were often consumed
to a similar or even greater extent than pest invertebrates or weed
seeds. The authors raised concerns that management for predation-
related ecosystem services may create equal or greater levels of
disservices, and that predation-related services will not necessarily
translate into net benets for agricultural production in some cases
(Tschumi etal. 2018).
Predation on seeds can reduce populations of planted crops, re-
sulting in reduced yields. Losses from granivorous soil-associated
insects, such as wireworms (Coleoptera: Elateridae), certain ground
beetles (Coleoptera: Carabidae, particularly Harpalini and Zabrini),
seedcorn maggots (Delia platura (Meigen), Diptera:Anthomyiidae),
thief (Solenopsis molesta Buren) and re ants (Solenopsis spp.
Westwood) (Hymenoptera: Formicidae) and crickets (Orthoptera:
Gryllidae: Nemobiinae and Gryllinae) through consumption
of planted seeds can be considerable (Lundgren et al. 2007).
Youngerman etal. (2020) conducted laboratory seed preference
trials with four common omnivorous predators that included the
Pennsylvania dingy ground beetle (H.pensylvanicus De Geer), the
common black ground beetle (Pterostichus melanarius (Illiger)),
Allard’s ground cricket (Allonemobius allardi (Alexander &
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282 Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
Thomas)) and the fall eld cricket (G.pennsylvanicus Burmeister)
and ten commonly used cover crop species, including barley
(Hordeum vulgare L.), annual ryegrass (Lolium multiorum
Lam.), pearl millet (Pennisetum glaucum (L.) R.Br.), forage radish
(Raphanus sativus L.), cereal rye (Secale cereale L.), white mustard
(Sinapis alba L.), crimson clover (Trifolium incarnatum L.), red
clover (Trifolium pratense L.), triticale (×Triticosecale Wittmack)
and hairy vetch (Vicia villosa Roth). Three weed species were also
included to test relative preference between weed and cover crop
seed, and included velvetleaf (A. theophrasti), common ragweed
(A.artemisiifolia L.) and giant foxtail (S.faberi). All four seed pred-
ators readily consumed cover crop seeds but cover crops with hard
seed coats and seed hulls such as hairy vetch and barley were less
preferred (Youngerman etal.2020).
Seed predators may act as dispersal agents of seeds if they possess
caching behavior or move viable seeds to suitable sites for germin-
ation. These seed dispersal behaviors can affect the spatial distri-
bution of weeds by concentrating seeds that were scattered from
the mother plant (Detrain and Tasse 2000, Vander Wall etal. 2005,
Schupp etal. 2019). Seeds can also be distributed vertically in the
soil by insect burrowing activities (Sarabi 2019). Ant seed dispersal
(myrmecochory) may reduce seed predation and increase germin-
ation if seeds are disposed of in ant refuse dumps or seed caches
(Penn and Crist 2018).
Regulating Disservices of Weed–Insect Interactions:
Weeds and Arthropod-Transmitted Phytopathogens
Weeds can interact with insects to inuence phytopathogen move-
ment in agroecosystems (Duffus 1971, Wisler and Norris 2005,
Eigenbrode et al. 2018). Weeds can serve as an overwintering
or in-season reservoir for phytopathogens that are trans-
mitted from outside or within the crop eld to crop plants by
insects. Some weeds may serve as an obligate alternate host for
phytopathogens that require them as part of the phytopathogen
life cycle. Many phytopathogens, mainly viruses (Blanc et al.
2011), and to a lesser extent fungi and bacteria (Perilla-Henao
and Casteel 2016), are transmitted by insects with sucking-
piercing or rasping mouthparts, such as leafhoppers (Hemiptera:
Cicadellidae), planthoppers (Hemiptera: Fulgoromorpha), white-
ies (Hemiptera: Aleyrodidae), aphids (Hemiptera: Aphidoidea),
psyllids (Hemiptera: Psylloidea), and thrips (Thysanoptera:
Thripidae) (Alexander et al. 2014). Insect vectors may be col-
onizers (i.e., those that feed or reproduce on a plant species) or
non-colonizers (i.e., those that do not feed and reproduce on a
plant species). Aphid-transmitted viruses are often transmis-
sible by a large suite of species, including non-colonizers (Zitter
2001). Within-eld or surrounding land cover can mediate virus
epidemiology by providing habitat for the insect vector. For ex-
ample, nonpersistent, aphid-transmitted viruses often have large
host-plant ranges and reservoirs of both the vector and virus can
persist in the surrounding landscape or within elds, affecting the
probability of virus infection within crop systems (Zitter 2001).
Groves et al. (2002) monitored thrips populations and Tomato
Spotted Wilt Virus (TSWV) on 28 common perennial, biennial, and
annual weed species over two non-crop seasons at eld locations
across North Carolina. Spiny sowthistle, (Sonchus asper (L.) Hill,
Herb. Brit., Asteraceae), chickweed, and dandelion (Taraxacum
ofcinale (L.) Weber ex F.H. Wigg, Asteraceae) consistently sup-
ported the largest populations of immature TSWV vector spe-
cies, the most abundant being the tobacco thrips, Frankliniella
fusca Hinds (Thysanoptera:Thripidae). TSWV infection was
documented in 49% of common perennial (14%), biennial (6%),
and annual (29%) weed species across 18 plant families. The au-
thors found that perennial weed species, including black-seeded
plantain (Plantago rugelii Decne., Plantaginaceae) and curly dock
(Rumex crispus L, Polygonaceae) remained TSWV-infected for 2
yr in a eld experiment, and suggested that perennial weed species
may serve as long-lasting inoculum acquisition sources of TSWV
for spread to susceptible crops (Groves etal. 2002).
The abundance of agricultural pests and the damage they cause
to crops are inuenced by combinations of management decisions
made at the within-eld scale (e.g., tillage regime, pesticide inputs)
and extra-eld characteristics (e.g., land use, habitat heterogeneity)
that are usually beyond the control of individual farmers. Insect-
transmitted crop viruses are mediated by both within-eld weeds
(e.g., Duffus 1971, Ali and Agrawal 2012, Srinivasan et al. 2014,
Smith etal. 2016) and in the surrounding area (e.g., Carrière etal.
2014, Clain etal. 2017). Angellella etal. (2016) compared the pre-
dictive ability of surrounding landscapes at different scales with that
of within-eld weed cover on aphid vector alightment and virus
infection within elds and found that for vectors of nonpersistent,
stylet-borne viruses, extra-eld landscape composition had a greater
inuence on vector alightment than did in-eld weed cover. Based
on their results, the authors questioned whether in-eld weed man-
agement is an effective method of crop virus prevention in some sys-
tems and suggested that management approaches should focus on
optimal crop placement relative to surrounding land use (Angellella
etal. 2016).
Supporting Services of Weed–Insect Interactions:
Biodiversity
Supporting services provide habitat and maintain biodiversity that
are necessary for the production and maintenance of the other
types of ecosystem services. Even though weeds are often harmful
for crop production they are also an important component of bio-
diversity in agricultural landscapes, and can serve as a resource for
arthropods and other organisms (Marshall etal. 2003, Petit et al.
2011, Woodcock etal. 2016, Blaix 2018). Many studies have found
positive relationships between plant diversity and the diversity of
consumer assemblages (rev. in Ng 2018). The diversity of weeds in
arable elds has been shown to increase with the complexity of the
landscape (Gabriel etal. 2005), which in turn can affect insect abun-
dance and diversity. In a study across three ecosystems, Tylianakis
etal. (2008) found that the relationship between diversity and an
ecosystem function became stronger in habitats with spatially het-
erogeneous distributions of an essential resource. The authors sug-
gested a heterogeneous environment reduces competition between
species through niche partitioning, allowing diverse assemblages that
perform their ecosystem functions at elevated rates (Tylianakis etal.
2008).
In agroecosystems, weeds can comprise a considerable propor-
tion of total plant species richness, a commonly used vegetation at-
tribute that represents the diversity of available resources (Perner
etal. 2005). Plant species richness has been linked to the diversity of
food resources, shelter and oviposition sites for arthropods (Landis
etal. 2005, Perner etal. 2005). Much research has focused on how
to increase biodiversity and ecosystem services in agricultural sys-
tems through management of eld margins and non-crop habitat
(Diehl et al. 2012, Tschumi et al. 2016) to counteract declines in
biodiversity within the cropped area of elds (Ewald etal. 2015).
Habitat heterogeneity is also temporally variable in agroecosystems.
Temporal (e.g., seasonal) and spatial habitat effects on insect–plant
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283Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
relationships can result through several mechanisms, including dif-
ferent plant host use at different stages of insect life cycles, changes
in plant phenology and succession, and varying environmental con-
ditions through time (Landis etal. 2000, 2005; Rouabah etal. 2015).
Increased biodiversity from weeds in annual cropping systems
can inuence the diversity and abundance of arthropods either dir-
ectly, through resource-mediated processes, e.g., provision of prey,
nectar, pollen, shelter or reproduction sites, or indirectly through
structure-mediated processes, i.e., modication of the physical en-
vironment. These mechanisms are not mutually exclusive and are
linked to site-specic factors such as abiotic conditions, disturbance,
and productivity (Perner etal. 2005). For example, Ng etal. (2018)
quantied the relationships between attributes of the ground-layer
plant community (structure, species richness, species composition)
and the diversity and species composition of beetles in three habitat
types (remnant woodland patches, farmland, and their edges), during
peak crop growth in spring and post-harvest in summer. The authors
found that plant species composition better-predicted beetle species
community composition than did vegetation structure; plant species
richness and vegetation structure both signicantly affected overall
beetle activity-density; and the inuence of these vegetation attri-
butes varied depending on habitat and time for all trophic groups
(Ng etal. 2018).
Habitat Structural Complexity and VegetativeCover
In agroecosystems, weeds can diversify habitat structure, dened as
the composition and arrangement of the physical material at a lo-
cation and measured as the absolute abundance of individual struc-
tural components per unit area (Woodcock etal. 2007). Habitat
structure is a driver of many patterns and processes by providing
resources (e.g., shelter, nesting sites) and mediating resource-based
dynamics in food webs (e.g., predation and competition) (Tews
et al. 2004). Theory (Loreau et al. 2003) and empirical evidence
(Tscharntke etal. 2008, 2012) indicate that habitat heterogeneity
can enhance the effects of biodiversity on ecosystem functioning and
stability by promoting coexistence through resource partitioning
among species (Cardinale etal. 2000). Weeds in both within-eld
and non-crop habitats contribute to habitat structure and cover in
agricultural landscapes (Saska etal. 2007). Vegetative cover supports
higher densities and evenness of natural enemies and inuences bio-
logical control by predators of insects and weeds (Letourneau etal.
2011; Diehl etal. 2012; Blubaugh etal. 2021, 2016; Ng etal. 2018).
Structural heterogeneity and vegetative cover provided by weeds
can modify the microclimate, such as ground temperature, and may
buffer the system against disturbances, e.g., unfavorable weather
conditions such as heavy rain or excessive heat and pesticide sprays
(Gontijo 2019).
Structural habitat heterogeneity and ecotones generally pro-
vide favorable habitats for arthropod predators (Landis etal. 2000,
Langellotto and Denno 2004), and contribute to their retention by
providing shelter and refuge from inter- and intra-guild predation,
resulting in higher predator densities (Janssen et al. 2007, Bohan
2011, Diehl etal. 2012, Kratina etal. 2012). Habitat structure also
inuences how organisms move through a habitat, in turn affecting
prey availability to predators and competitive and predatory inter-
actions among predators (Landis etal. 2005, Ng et al. 2018). Ng
(2018) suggested that weedy patches could provide structural refuge
(e.g., oviposition or estivation sites) for predatory beetles during
the summer. Greater predator abundance and diversity can lead
to greater biological control of insect pests (Sunderland and Samu
2003, Letourneau etal. 2011).
Complex habitats with non-crop plants such as weeds can also
host a greater diversity of herbivores, supporting a greater diver-
sity of natural enemies (Andow 1991). Vegetative cover provided by
weeds can also enhance arthropod numbers. Among the most con-
sistent factors that distinguished carabid beetle species assemblages
among years and treatments in a study comparing levels of disturb-
ance and cover crop type in an organic cropping system were soil
disturbance and weed density (Jabbour etal. 2016, Pisani Gareau
et al. 2020). In a meta-analysis of seven long-term eld studies in
Britain, Smith et al. (2020) found arthropod predator abundance
was related to total weed cover in wheat, Triticum aestivumL.
Overall, the effects of habitat complexity and vegetative cover are
locally specic and can range from having a very great effect to no
effect at all on weed seed predation (Birthisel etal. 2014, Winqvist
etal. 2011). Blubaugh etal. (2016) examined the effects of vegeta-
tive cover provided by cover crops on predation of weed seeds by
omnivorous arthropods and found that vegetative cover increased
per-capita weed seed predation by 73% compared with bare plots.
Early-season weed seed presence increased beetle activity-density by
77%, and the authors suggested that within-eld habitat manage-
ment such as cover crops improve biological control, not only by
promoting increased activity of omnivores, but also by facilitating
their function as weed seed predators, demonstrating the utility of
cover crops to promote weed seed predation by increasing seed
predator activity-density, as well as increasing per-capita predation
frequency (Blubaugh etal. 2016).
Resource-MediatedEffects
Vegetative cover supports higher densities of natural enemies through
provision of alternate food sources, including plant-based resources,
such as pollen, nectar, and seeds, and weed-attracted or -associ-
ated herbivore and detritivore prey (Lövei and Sunderland 1996,
Birkhofer etal. 2008, Bohan 2011, Diehl etal. 2012, Holland etal.
2016, Ng et al. 2018). The presence of insects on weeds may sup-
port populations of benecial insects that can spill over onto crops
and help suppress pests. Omnivory is common among generalist
predators in agroecosystems, and weeds can contribute to a broad
diet that supports the persistence of omnivores despite seasonal dis-
turbances and food scarcity (Eubanks and Denno 1999). In addition
to arthropod prey, generalist arthropod predators and omnivores
consume a wide range of plant-based foods, although some omniv-
orous and granivorous predator species have preferences for seeds
of particular weed species (Lundgren et al. 2013, Honěk etal. 2007,
Sasakawa 2010, Sarabi etal. 2019). Diehl etal. (2012) examined
the effects of arable weeds in an organically-managed wheat eld
and found that the presence of arable weeds fosters carabid activity-
density and species richness via resource-mediated effects, such as a
higher availability of weed-borne resources (e.g., seeds and pollen),
as well as arthropodprey.
The adult stage of many predators and parasitoids feed on
nectar from owers or from extraoral nectaries and it is well docu-
mented that natural enemies can survive longer and produce more
viable offspring when they are provided with plant-based food re-
sources than in the absence of those resources (rev. in Gurr etal.
2016, 2017). The presence of weeds, especially those with accessible
nectar from owers or extraoral nectaries enhances the survival
of benecial insects that can assist in biological control of pests.
For example, many predatory insects with piercing-sucking mouth-
parts, such as the insidious ower bugs and minute pirate bugs
(Hemiptera:Anthocoridae) are facultative predators, feeding prefer-
entially on insects but also imbibing plant sap and nectar. In addition
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284 Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
to the benets of weeds on natural enemies of pest insects, weeds af-
fect the activities of pollinators. Pollinators collect nectar and pollen,
and often are not abundant in the absence of weeds (Requier etal.
2015, Rollin etal. 2016).
Supporting Disservices of Weed–Insect Interactions:
Biodiversity
Even though weeds contribute to ecosystem services supported
by biodiversity and structural complexity in cropping systems, as
the primary pest in annual agroecosystems, weeds are the focus
of intensive and extensive management to reduce their numbers
and their negative impacts on provision of ecosystem services
(rev. in Vaz et al. 2017, Chauhan 2020). The most frequently
documented negative impact of weeds in agroecosystems is com-
petition for resources with other plant species (Maxwell 2018)
and the support of phytopathogens and crop pests (Norris and
Kogan 2005). In a study of weed-invertebrate relationships across
seven studies of winter-sown wheat spanning 18 yr, Smith etal.
(2020) found that herbivores showed a stronger positive relation-
ship with weed cover than did predators. The authors suggested
that this result was expected because herbivores rely on the re-
sources provided by weeds whereas the response of predatory spe-
cies is likely to be mediated by their prey. Increased fecundity of
pests has been observed when weeds were present, due to nectar
obtained by the adults, which has led to the question by some of
the utility of leaving weeds as a source of nectar for benecial in-
sects (Shields etal. 2019). Ng (2018) suggested that the mixed re-
sponses of herbivores and predators to plant species composition
or vegetation structure include that a high proportion of herbiv-
orous beetles may be attracted to plant species that are largely
limited to habitat edges, e.g., Blue cranesbill (Erodium crinitum,
Geraniaceae), tumbleweed (Salsola australis, Amaranthaceae) and
wild mustard (Sisymbrium sp., Brassicaceae). Herbivores may al-
locate more time to foraging in complex habitats because they
provide protection from predators through consumptive and non-
consumptive effects (Langellotto and Denno 2004, Blubaugh etal.
2017, Hermann and Landis 2017).
There can be negative effects associated with insect feeding on
weeds if the insect does not restrict its feeding to weeds. In their re-
view, Norris and Kogan (2005) supplied several specic examples of
weeds serving as hosts for pest arthropods. Oligophagous and pol-
yphagous herbivores can move from weeds to crop plants, potentially
causing crop damage. For example, neonate European corn borer,
Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), is a polypha-
gous pest of corn in the United States. In feeding preference assays,
neonate European corn borer readily accepted foliage of several
common weed species found in corn elds, including Pennsylvania
smartweed (Polygonum pennsylvanicum (L.)), swamp smart-
weed (Polygonum amphibium L.), velvetleaf (Abutilon theophrasti
Medicus), cocklebur (Xanthium strumarium L.) and yellow foxtail
(Setaria glauca (L.)) (Tate etal. 2006). Specialist herbivores that feed
on weeds that are closely related to crops represent a particular risk
for attacking those crops (Capinera 2005), and insect species that
prefer weeds may damage crops readily in the absence of attractive
weeds. For example, the Colorado potato beetle, Leptinotarsa
decemlineata (Say), an economic pest of potato, prefers to oviposit
on hairy nightshade (Solanum sarrachoides Sendtner) rather than on
potato (S.tuberosum (L.)), and eggs are less abundant on potato in
the presence of nightshade (Horton and Capinera 1990). In the ab-
sence of solanaceous weeds, Colorado potato beetle readily oviposits
and develops on potato foliage, often causing extensivedamage.
Complex landscapes with numerous eld edges provide stable
habitats, such as unplowed refuges or natural vegetation bordering
or dividing cultivated areas. Interactions between relatively stable
areas and highly disturbed annual crop elds can inuence within-
eld diversity and abundance of natural enemies. However, non-crop
and edge habitats can also provide resources for arthropod pests
that can move into crops (Tscharntke etal. 2012, 2016). Therefore,
balancing the functional contributions of weeds in eld edges and
non-crop habitats while minimizing disservices requires consider-
ation of spatial arrangements. For example, Colbach etal. (2018)
used a simulation model to determine optimal approaches to maxi-
mize crop productivity and weeds in a soybean/maize/wheat/maize
rotation. The authors found that a land-sparing scenario (landscape
management) designed to maximize crop production by maximizing
biodiversity (25% of the landscape devoted to non-crop area) or
grass strips (10% of the landscape) were best, resulting in high crop
production and medium biodiversity at the landscape scale. Land-
sharing scenarios attempting to maximize both productivity and bio-
diversity within the same eld always produced less biodiversity and
less production (Colbach etal. 2018).
Generalist predators and specialized parasitoids may respond
to plant diversity and habitat structure differently and some studies
have demonstrated that habitat complexity negatively impacts nat-
ural enemy abundance and efciency. For example, Tscharntke
etal. (2008) demonstrated that although generalist natural enemy
diversity was preserved in complex landscapes, specialized natural
enemies were not, because of specic habitat or resource needs.
Structurally complex agricultural habitats negatively impacted the
hunting behavior or limited the ability of predators, such as lady bee-
tles, to visually search for prey (Legrand and Barbosa 2003). Weed
diversity had little impact on predation by generalist predators in
eld corn (Wilson etal. 2004) but reduced specialized natural enemy
populations in canola (Brassica napus L., Brassica rapa L.) (Broatch
etal. 2010). Although vegetative cover can support higher densities
of natural enemies by providing a favorable microclimate and pro-
visions of non-pest food (Diehl etal. 2012), alternate foods may dis-
tract natural enemies from focal pest suppression (Frank etal. 2011).
If weed species are preferred over an adjacent crop, the weeds may
act as a barrier or a trap crop (Andow 1991). Benecial effects of
weeds on arthropod communities must be weighed against potential
negative effects on crop quality and yield.
Summary and Identification of KnowledgeGaps
Weeds, insects and their interactions can have positive or negative
effects on ecosystem services and the functioning of agroecosystems.
Weeds can support regulating services (biological control, pollin-
ation) and supporting services (e.g., biodiversity) that can improve
agricultural production and restore biodiversity in agroecosystems.
In some situations, weed–insect interactions supply disservices (e.g.,
increase in weed fecundity and abundance, crop and cover crop seed
consumption, maintenance of phytopathogen and insect pest popu-
lations). Our challenge is to design and manage cropping systems
and agricultural landscapes that can deliver services that support
crop productivity without causing damaging populations of weed
and insect pests that lead to loss of crop yield and/or quality. Meeting
this challenge will require a paradigm shift in current pest manage-
ment practices within production systems that rely extensively on
herbicides and tillage to control weeds and pre-emptive applications
of broad-spectrum insecticides to control insect pests. In a recent re-
view, MacLaren etal. (2020) suggest that a renewed and persistent
focus on managing weeds at the agroecosystem level to regulate,
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285Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
rather than eradicate, weed populations is needed to conserve eco-
system services provided by weeds while preventing disservices such
as crop yield loss. The simplication of agricultural systems remains
a signicant barrier to realizing more ecosystem services than disser-
vices from weed–insect interactions. However, the growing emphasis
on soil health building practices that couple diverse crop rotations,
use of cover crops to promote continuous living cover, and reduced
tillage practices offer opportunities for promoting more sustainable
forms of pest regulation.
Within this context, additional research is needed to develop
strategies for maintaining weed and insect diversity at levels capable
of delivering meaningful levels of ecosystem services. At landscape
scales, greater understanding of how land use intensity and com-
plexity inuence weed–insect interactions could inform the devel-
opment of pest management practices. At eld scales, concentrated
efforts to design and manage eld-edge habitats is needed to attract
benecial insects for conservation biological control of insects and
weeds, and for pollination services.
Improved management of eld margins and adjacent non-crop
habitat to increase positive weed–insect functional interactions or
decrease the expression of disservices likely offers greater potential
to conserve weed and insect diversity than within-eld manage-
ment practices. However, renewed interest in intercropping practices
(Brooker etal. 2015, Bybee-Finley and Ryan 2018), where multiple
crops species (e.g., multiple cash crops, or cash and cover crops)
are grown at the same time and place offer signicant opportun-
ities for manipulating weed–insect functional interactions. At a crop-
ping system scale, several crop and soil management practices (e.g.,
crop species and varieties, types and timing of disturbance) may be
manipulated to regulate weed–insect interactions. Crop production
practices that break the taxonomic association between the crop and
the weeds that are co-located, for example, through crop rotations
that diversify timing of disturbances, make it less likely that insects
will move from weed to crop plants, that damaging population
densities of insects will develop in the eld, and that insect vectors
that transmit plant diseases will be harbored in the eld (Cardina
etal. 2002, Gallandt 2006).
Research focusing on cash- and cover- crop residue manage-
ment should seek to understand how surface and incorporated
residue management strategies inuence microhabitats for weed
and insect predators. Though use of economic thresholds to govern
herbicide applications for weed control is generally viewed as im-
practical due to the growth and persistence of weed seedbanks
generated by weeds left uncontrolled, other weed-management
strategies should be considered to foster greater functional weed
diversity at eld scales. Identication of management strategies
that select for weeds that are less competitive per capita, thereby
producing negligible effects on crop yields, but provide ecosystem
services (e.g., pollination support of natural enemies) should be
explored. Weed-management systems that employ multiple low-
intensity and asynchronous selection pressures (i.e., many little
hammers) on weed communities are more likely to promote func-
tional weed diversity compared to weed management systems that
rely exclusively on intensive selection pressure associated with
broad-spectrum herbicides.
One relatively unexplored area is the chemical ecology of
weed–insect interactions. There is evidence that weeds chemically
interact with other weeds and crop plants and affect plant–insect
interactions. For example, root herbivory on spotted knapweed,
C. maculosa, increased exudation of the avanol (±)-catechin, an
allelopathic agent that negatively affects other plant species (Thelen
et al. 2005). However, herbivory by a phloem-feeding aphid re-
duced the allelopathic activity of goatweed, Ageratum conyzoides
L. (Asteraceae) (Kong et al. 2002). Barley (Hordeum vulgare L.,
Poaceae) plants exposed to root exudates from couch grass, Elytrigia
repens (L.) Desv. ex Nevski (Poaceae), and volatiles from bull thistle,
Cirsium vulgare (Savi) Ten. (Asteraceae) became less acceptable
to pest aphids of cereals (Glinwood et al. 2004, 2011). Exposure
to volatiles from lambsquarters, C. album, reduced aphid settling
on barley in the laboratory and in the eld (Ninkovic etal. 2009).
Research to further elucidate the impact of the chemical ecology of
weed–insect interactions on damage from insects and other pests
and on crop productivity could inform design of weed-management
strategies to promote ecosystem services and avoid promoting insect
pest populations.
Because the same weed species can produce both ecosystem
services and disservices, research is also needed to assess manage-
ment options for ambiguous weed–insect interactions. For example,
pollinator declines over the last decades have resulted in loss of pol-
lination services that can result in negative ecological and economic
impacts on wild plant diversity, wider ecosystem stability, crop pro-
duction, food security and human welfare (Potts etal. 2010a,b,c).
However, pollination of weeds can potentially lead to their greater
fecundity and abundance, resulting in greater management costs and
loss of crop productivity. Annual agroecosystems employ owering
cover crops to provide a broad suite of ecosystem services, but
that can also become weeds. For example, buckwheat, Fagopyrum
esculentum Moench, is a short-duration crop and cover crop that
readily drops seed before harvest, often resulting in volunteer buck-
wheat plants in the following crop (Lyon etal. 2019). Buckwheat
can act as a potent allergen, and some importers of U.S.wheat have
a near-zero tolerance for buckwheat in grain shipments (Machado
etal. 2020). Honey bees are frequently the most abundant pollin-
ators of buckwheat (Bjorkman 1995) and consumer demand for
monooral honeys has increased in recent years because of their
avor and pharmacological properties. High-quality honey produced
from buckwheat nectar commands a price premium (Machado etal.
2020). Therefore, land managers may need to consider the relative
impact of management on crop productivity, and pollinator conser-
vation and exploitation on short- and long-term protability in their
particular context.
Overall, research that provides tools and frameworks (e.g.,
Dille etal. 2002, Schipanski etal. 2014, 2017; Finney etal. 2017;
Rodriguez etal. 2018) that allow farmers and managers to estimate
risk within their local and regional context and exploit ecosystem
services provided by weed–insect interactions while minimizing
disservices could improve the sustainability of annual cropping
systems. For example, DiTommaso etal. (2016) introduced a weed-
management decision framework that accounts for benets from
common milkweed, Asclepias syriaca L., in maize, and demonstrates
how in-crop weeds can indirectly increase crop yields by harboring
alternate insect hosts that support natural enemies of the European
corn borer, Ostrinia nubilalis (Hübner). At the same time, this frame-
work evaluates the role of milkweed in providing resources to the
monarch buttery, Danaus plexippus L., a charismatic insect whose
sole larval food is milkweed. Analytical frameworks such as those
that use a holistic approach and integrate the management of mul-
tiple crop pests and benecial organisms can potentially improve
decision-making that balances ecosystem services and disserves in
annual agroecosystems.
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286 Annals of the Entomological Society of America, 2021, Vol. 114, No. 2
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