Biological Control 75 (2014) 8–17

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Biological Control

journal homepage: www.elsevier .com/ locate/ybcon

Relationships between biodiversity and biological control inagroecosystems: Current status and future challenges

1049-9644/$ - see front matter � 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.biocontrol.2013.10.010

⇑ Corresponding author.E-mail address: dcrowder@wsu.edu (D.W. Crowder).

David W. Crowder a,⇑, Randa Jabbour b

a Department of Entomology, Washington State University, PO Box 646382, Pullman, WA, USAb Department of Plant Sciences, University of Wyoming, 1000 E. University Ave., Laramie, WY 82071, USA

h i g h l i g h t s

� Agricultural systems are intensifyingto keep up with growing humandemands.� Intensive agriculture can negatively

impact biodiversity and biologicalcontrol.� We review biodiversity and biological

control of arthropod and weedy pests.� We discuss similarities and

differences between biocontrol ofarthropods and weeds.� We suggest novel approaches for

examining biodiversity and biologicalcontrol.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Available online 1 November 2013

Keywords:Agricultural intensificationConservationEcosystem functioningEvennessRichness

a b s t r a c t

Agricultural systems around the world are faced with the challenge of providing for the demands of agrowing human population. To meet this demand, agricultural systems have intensified to produce morecrops per unit area at the expense of greater inputs. Agricultural intensification, while yielding morecrops, generally has detrimental impacts on biodiversity. However, intensified agricultural systems oftenhave fewer pests than more ‘‘environmentally-friendly’’ systems, which is believed to be primarily due toextensive pesticide use on intensive farms. In turn, to be competitive, less-intensive agricultural systemsmust rely on biological control of pests. Biological pest control is a complex ecosystem service that is gen-erally positively associated with biodiversity of natural enemy guilds. Yet, we still have a limited under-standing of the relationships between biodiversity and biological control in agroecosystems, and themechanisms underlying these relationships. Here, we review the effects of agricultural intensificationon the diversity of natural enemy communities attacking arthropod pests and weeds. We next discusshow biodiversity of these communities impacts pest control, and the mechanisms underlying theseeffects. We focus in particular on novel conceptual issues such as relationships between richness, even-ness, abundance, and pest control. Moreover, we discuss novel experimental approaches that can be usedto explore the relationships between biodiversity and biological control in agroecosystems. In particular,we highlight new experimental frontiers regarding evenness, realistic manipulations of biodiversity, andfunctional and genetic diversity. Management shifts that aim to conserve diversity while suppressingboth insect and weed pests will help growers to face future challenges. Moreover, a greater understand-ing of the interactions between diversity components, and the mechanisms underlying biodiversityeffects, would improve efforts to strengthen biological control in agroecosystems.

� 2013 Elsevier Inc. All rights reserved.

1. Introduction

Human population growth has led to the global expansion ofagriculture. The acreage of land used for crops increased by 466%

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from 1700 to the 1980s (Meyer and Turner, 1992). This growth,however, has slowed in recent decades as suitable areas for culti-vation become increasingly scarce (Matson et al., 1997). As growthof agricultural acreage has stagnated, agricultural systems aroundthe world have intensified. Agricultural intensification is a broadterm that encompasses many factors including, but not limitedto, increased use of pesticides and fertilizers (see Roubos et al.,2014), increases in farm size, decreases in crop diversity, increasesin crop density, and increased numbers of crops grown in a season.This has been due in large part to dramatic increases in crop yieldssince the 1960s, referred to as the ‘‘Green Revolution’’ (Pingali,2012), which has been spurred by technological and cultural ad-vances in crop breeding and management (Matson et al., 1997;Krebs et al., 1999; Benton et al., 2003).

While agriculture has kept pace with human populationgrowth, increases in crop yields has also slowed recently (FAO,2013). Moreover, agricultural intensification has negative localconsequences such as reduced biodiversity, increased soil erosion,pollution, and reduced socio-economic sustainability, each ofwhich has other impacts (Matson et al., 1997; Stoate et al., 2001;Kleijn et al., 2006). For example, reducing the number of species(reduced richness) (Hooper et al., 2005; Cardinale et al., 2006)and skewed relative abundance distributions (reduced speciesevenness) (Hillebrand et al., 2008; Crowder et al., 2010) generallyweaken biological control. These harmful consequences of agricul-tural intensification have led to an increased focus on methods toincrease the sustainability of agroecosystems (Tilman, 1999; Foleyet al., 2011).

Biological control is a key ecosystem service that is necessaryfor sustainable crop production (Bianchi et al., 2006; Losey andVaughan, 2006). Natural enemies such as predators, parasitoids,and pathogens play a central role in limiting damage from nativeand exotic pests (Hawkins et al., 1999; Losey and Vaughan,2006). Conservative estimates suggest that the economic valueprovided by insect natural enemies controlling pests attacking cropplants exceeds $4.5 billion annually in the United States (Losey andVaughan, 2006). If weedy pests, or pests attacking humans andlivestock (not crops) were considered the estimate of pest controlprovided by insects would likely be much greater. Moreover, amultitude of species act as natural enemies of insect or weedypests such as birds, bats, fungi, nematodes, and rodents (Kirket al., 1996; Miller and Surlykke, 2001; Navntoft et al., 2009; Ra-mirez and Snyder, 2009; Williams et al., 2009; Jabbour et al.,2011). Thus, if these species were considered the economic valueof biological control would be far greater than $4.5 billion annually.

To improve and conserve biological control, it is essential tounderstand the relationships between agricultural intensification,biodiversity, and pest suppression. We addresses this complex is-sue by first reviewing the effects of agricultural intensification onthe biodiversity of natural enemies, and the role of natural enemiesin agricultural food webs. We next discuss conceptual modelsrelating biodiversity to natural pest control. Third, we reviewmethodologies for examining the relationship between biodiver-sity and biological control in agroecosystems. We conclude by dis-cussing areas of research emphasis that, if addressed, wouldimprove our understanding of how biodiversity and biological con-trol operate in agroecosystems.

2. Effects of agricultural intensification on biodiversity

2.1. Non-pest species

Agricultural intensification impacts both pest and non-pest spe-cies in agricultural communities. Indeed, much of the evidence ofthe impacts of agricultural intensification on ecologicalcommunities comes from conservation-related studies on non-pest

species. Some of the longest-term studies of agricultural intensifi-cation and biodiversity have focused on bird populations in Europe,which have declined dramatically over the last half-century(Benton et al., 2003). Donald et al. (2001) showed that birdpopulations in the UK declined with increases in cereal and milkyields along with fertilizer and tractor usage. Cereal yields aloneexplained 31% of the variability in declining bird populations,suggesting that intensification of a single crop type can impactdiversity (Donald et al., 2001).

There is evidence, however, that agri-environment schemes en-acted by many European countries to encourage wildlife have ledto resurgence of some bird species (Benton et al., 2003). Agri-envi-ronment schemes provide monetary incentives for farmers to man-age a portion of their land to promote conservation of biodiversityand reduced impacts on the environment (Benton et al., 2003;Kleijn et al., 2006). By incorporating or conserving natural habitatin agricultural ecosystems to preserve native species, theseschemes are designed to buffer against potentially damagingeffects from agricultural intensification on biodiversity. Kleijnet al., 2006 compared the abundance and richness of plants, birds,and arthropods at 202 paired locations across five Europeancounties. Each location contained one site managed with anagri-environment scheme and one conventional site. The agri-environment schemes had some positive impacts on abundanceand diversity of these groups in each country, while conventionalmanagement did not benefit any group (Kleijn et al., 2006). Theauthors speculated that benefits were due to reduced inputs anddisturbances in agri-environment fields. However, the species thatbenefitted most from agri-environment schemes did not includemany species of extinction concern. This suggests that conservingnative habitat may not benefit rare species, or that species ofextinction concern declined in abundance due to factors other thanagricultural intensification.

Crowder et al. (2010, 2012) showed that organic farming sys-tems had marginal positive impacts on richness and significant po-sitive impacts on evenness and abundance compared withconventional systems. These benefits occurred across crop typesand were consistent across several organismal groups includingarthropods, birds, non-bird vertebrates, plants, and soil organisms.The benefits of organic farming were greatest for the rarest speciesin conventional systems (Crowder et al., 2012). Other reviews(Bengtsson et al., 2005; Hole et al., 2005) have shown similar posi-tive impacts of organic farming on richness and abundance oforganisms. In each case, these results are likely due to reducedinsecticide use in organic farming systems and/or increased habitatdiversity. For example, granivorous beetle diversity has beenshown to be positively associated with habitat complexity onfarms (Vanbergen et al., 2010; Trichard et al., 2013), and negativelyassociated with use of pesticides (Trichard et al., 2013).

2.2. Arthropod pests

Root (1973) suggested that dense, homogenous plant commu-nities facilitated higher herbivore populations. His ‘‘resource-con-centration hypothesis’’ posits that specialist pests can locateplant stands, and feed more efficiently, when a single non-diversecrop is present. Thus, intensification may actually be responsiblefor pest outbreaks so common in monocultures. However, thishypothesis does not hold true for all cases, suggesting that re-source-concentration effects are organism dependent (Grez andGonzalez, 1995). Secondary pest outbreaks, where early-seasoninsecticide applications kill natural enemies and result in late-sea-son outbreaks of pests, have also received attention as a negativeimpact of agricultural intensification. For example, Gross andRosenheim (2011) showed that 20% of late-season pesticide costswere attributable to early-season pesticide applications for control

Fig. 1. A hypothetical agricultural food web, where arrows indicate energy flow.Biological control of weeds and insect prey involve several of the same animalgroups, including potential intraguild predation amongst birds, mammals, andinsect omnivores and predators.

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of lygus bugs. This is perhaps not surprising as pesticides can dis-rupt natural enemy populations at broad scales (Roubos et al.,2014) and might disrupt periods of temporal overlap betweenpests and their natural enemies (Welch and Harwood, 2014).

Comparison of organic and conventional farming systems alsosuggest mixed effects of intensification on pests. For example,aphids tend to be more abundant in conventional farms due tohigher-quality crops that grow faster, while mites and true bugstend to be more common in organic farms (Hole et al., 2005).Across multiple pest groups, Bengtsson et al. (2005) found no sig-nificant effect of organic farming on abundance or species richness.This result is perhaps surprising given that conventional farmstend to use significantly more pesticides compared with organicfarms, which should limit pest populations (Bengtsson et al.,2005; Hole et al., 2005). This perhaps suggests that for many pestherbivores that increased effectiveness of natural enemies in or-ganic farming systems might allow for pest control equivalent, ornearly equivalent, to control achieved with pesticides (Crowderet al., 2010, 2012).

2.3. Weeds

Weed communities are consistently more abundant and rich inless-intensive agricultural systems. For example, organic farmsgenerally harbor 2.3–2.8 times more abundant weed seed densitiesand 1.3–1.6 times more weed species compared with conventionalfarms (Roschewitz et al., 2005; Gabriel et al., 2006; Hawes et al.,2010; José-María and Sans, 2011). Frequent herbicide use in inten-sive agroecosystems likely drives reduced weed diversity andabundance. In addition, weed communities often vary based oninorganic fertilizer use and crop rotations (Hawes et al., 2010).Hawes et al. (2010) showed that fertilizer use and rotations ex-plained as much variation in weed abundance/ diversity as farmtype across 109 conventional, integrated, and organic farms. Syn-thetic fertilizer use was negatively associated with weed abun-dance, an unsurprising result given that farms using syntheticfertilizers also likely use synthetic herbicides. However, organicmanures are known as likely sources of weed seed (Mt. Pleasantand Schlather, 1994), a risk that farmers and scientists acknowl-edge readily in discussions of weed introduction and weed spread(Jabbour et al., 2013).

Weed communities on farms are also influenced by the sur-rounding landscape (see also Chisholm et al., 2014). For example,weed vegetation and seedbank diversity in German wheat fieldswas positively associated with landscape complexity around farms(Roschewitz et al., 2005). Interestingly, in this study, weed diver-sity was similar in organic and conventional fields when land-scapes were complex, but weed diversity was higher in organicfields in simple landscapes. In contrast, effects of landscape com-plexity on weed seedbanks in Mediterranean dryland systemswere limited and only detected in field edges, not field centers(José-María and Sans, 2011). These results suggest that in some,but not all systems, management of landscape complexity mightbe a strategy for less-intensive farmers to manage weeds.

2.4. Other pests

There is evidence that agricultural intensification influencespathogens (Wolfe et al., 2007). For example, measles, mumps,smallpox, and influenza likely originated with domesticated ani-mals (Wolfe et al., 2007). Agriculture leads to crowding of popula-tions, which promotes pathogen spread (Wolfe et al., 2007).Similarly, high vector densities in intensive systems promote thespread of crop pathogens. While not a focus of this review due tolimited studies, effects of biodiversity on biological control ofpathogens should be examined further.

2.5. Overview

The studies discussed here show that agricultural intensifica-tion has complex effects on pests and beneficial species. In general,more intensive systems decrease the abundance and biodiversityof beneficial species such as natural enemies. At the same time,intensification might exacerbate pest problems by concentratingarthropod resources and decreasing populations of natural ene-mies. In the following sections we discuss how disruptions in bio-diversity of pests and natural enemies caused by agriculturalintensification can influence species interactions and have strongimpacts on biological control.

3. Why does biodiversity matter? Exploring agricultural foodwebs

Reductions in biodiversity can disrupt food webs and weakenbiological control (Tylianakis et al., 2007; Macfadyen et al., 2009;Schmitz and Barton, 2014; Tylianakis and Binzer, 2014). Trophiccascades have been a central concept in biocontrol studies sinceHairston et al. (1960) proposed the ‘‘Green World Hypothesis’’,whereby natural enemies protect plants by regulating pests. How-ever, the role of biodiversity in generating trophic cascades hasbeen questioned (Strong, 1992; Polis and Strong, 1996; Polis,1999). A key criticism is that in complex food webs, removal of asingle species is unlikely to influence cascades. Indeed, studieshave shown that natural enemy diversity can promote (Cardinaleet al., 2003; Snyder et al., 2006; Crowder et al., 2010) or weakentrophic cascades (Finke and Denno, 2004, 2005). Understandingthe food webs in which natural enemies and pests interact is thuscentral to understanding relationships between biodiversity andbiological control.

Arthropod food webs are discussed by Tylianakis and Binzer,2014, and we do not expound on them here. Weeds also play keyroles in agricultural food webs and may thus influence biodiversityand biological control (Fig. 1). Farmers generally aim to manageweeds given their considerable agricultural and economic risks,although they do acknowledge the ecological benefits of weeds(Wilson et al., 2008; Jabbour et al., 2013). As hypothesized by Root(1973), plant diversity is often negatively associated with herbi-vore abundance (Cardinale et al., 2012). Weeds comprise a largecomponent of floral diversity in agroecosystems, given the compa-rably low diversity of most crop plantings, and thus may play a keyrole in limiting pests from the bottom-up.

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In addition to the potential contribution of weed diversity tolimiting pests, the resource of weed seeds in particular can havemajor impacts on food webs. Weed seed resources can support ahigh diversity of granivorous and omnivorous species includingmammals, birds, arthropods, earthworms, and slugs (Frankeet al., 2009). A detailed study of the seed-based food web on an or-ganic farm in the UK estimated that 274 arthropod, 53 bird, and 10mammal species likely used seeds as a resource (Evans et al.,2011). However, these effects can be quite nuanced and dependenton crop type. A recent study focused on farmland birds showedthat genetically-modified beet and oilseed crop systems had lessweed seed resources used by birds than conventional systems(Gibbons et al., 2006). In contrast, genetically-modified maizehad more seed available for birds than conventional systems.Although seed resources can support omnivores, seed availabilitymay also distract from insect pest control by natural enemies(e.g., Frank et al., 2011).

These studies demonstrate that natural enemy consumers andtheir resources (arthropod and weedy pests) interact in complexfood webs (see also Tylianakis and Binzer, 2014). Food-web ecol-ogy is a burgeoning field that could thus contribute to our under-standing of the relationship between biodiversity and biologicalcontrol. We expound on this issue in the following section.

4. Relating richness to biological control

4.1. Mechanisms underlying effects of richness on biological control

The mechanisms by which species richness affects biologicalcontrol of arthropods have been reviewed (Schmitz, 2007; Letour-neau et al., 2009), and we only briefly discuss them to provide con-text for the remainder of the review (Fig. 2). Positive richnesseffects occur when species act complementarily in terms of pestsuppression, or when one or more species facilitates prey captureby another, such that the combined impact of multiple species ex-ceeds the mortality any species exerts on its own (Losey and Den-no, 1998; Finke and Snyder, 2008; Northfield et al., 2010). Positiverichness effects can also occur through ‘‘insurance effects’’, where amore species rich community effectively performs biological con-trol despite disturbances because one or more species is resilientto a disturbance even while others are negatively affected (Naeemand Li, 1997; Yachi and Loreau, 1999). In contrast, increasing spe-cies richness can negatively impact biological control when naturalenemies feed on each other, an occurrence known as intraguildpredation, which limits predator density and impact on pests(Finke and Denno, 2004, 2005; Rosenheim, 2007). Behavioral inter-ference among predator species can also weaken biological controlwith increases in natural enemy richness (Schmitz, 2007).

Many authors have also pointed out that the positive or nega-tive impacts of species richness on ecosystem functions such asbiological control can be due to statistical chance. In this scenario,richer communities could improve biological control simply be-cause they have a higher probability of containing a superior nat-ural enemy species (Naeem and Wright, 2003; Cardinale et al.,2006). In contrast, richer communities might also have a higherprobability of containing a disruptive species (like a voraciousintraguild predator), which could weaken biological control(known as a selection effect; Loreau and Hector, 2001).

4.2. The richness-biological control relationship in studies involvingarthropod pests

Studies relating richness to arthropod biological control havevariably shown positive, negative, and neutral effects. In a meta-analysis, Letourneau et al. (2009) showed that 71% of studies

involving arthropod pests observed positive effects of natural en-emy richness on pest suppression, with particularly strong effectsin agricultural systems. Nearly all of the remaining 30% of studies,however, showed a negative relationship between natural enemyrichness on pest suppression. Yet, the magnitude of the averagenegative effect was 63% that of the average positive effect, suggest-ing that natural enemy richness was more likely to generate strongpositive impacts than strong negative effects. Letourneau et al.(2009) could not distinguish between the mechanisms underlyingthese effects of richness, however. Thus, it was unclear whethermore diverse communities promoted pest control because naturalenemies tended to act complementary or facilitated prey-captureby other species, or whether more diverse communities were morelikely to contain particularly effective natural enemy species bychance alone (otherwise known as a sampling or species identityeffect).

4.3. The richness-biological control relationship in studies involvingweedy pests

Evidence for richness effects on biological control of weeds isless common than for arthropods. However, in Wisconsin andFrance, richer seed-feeding beetle communities were associatedwith increased weed seed loss from experiments (Gaines and Grat-ton, 2010; Trichard et al., 2013). This positive relationship occurredin both crop and non-crop habitats in Wisconsin potato agroeco-systems (Gaines and Gratton, 2010). As with arthropods, indirectevidence suggests that complementarity may underlie these ef-fects. Invertebrate granivores eat smaller seeds on average com-pared to mammals and birds, such that the combined impacts ofboth guilds of natural enemies strengthened weed suppression inthe Gaines and Gratton study (2010). Different birds species varyin their weed-seed preferences as well (Perkins et al., 2007). Weedpredators also may be temporally complementary, with inverte-brate seed consumption decreasing and vertebrate consumptionincreasing as winter approaches (Davis and Raghu, 2010).

Alternatively, seed consumer richness may negatively affectweed seed predation via intraguild predation. Many granivores inthe seed-based food web are omnivores who also prey upon inver-tebrates. Small mammals feed on insects as well as seeds, andcould negatively impact invertebrate granivores. For example,excluding rodents from experimental plots in shrub-steppe habi-tats resulted in increased carabid abundance following a two yearperiod (Parmenter and MacMahon, 1988). Moreover, a study ofinvertebrate and vertebrate predation in corn fields highlightedthe potential influence of predation risk of seed predators on seedpredation rates (Davis and Raghu, 2010). Invertebrate seed preda-tion was negatively associated with abundance of spiders, poten-tial predators of granivorous crickets active in that system. Also,vertebrate seed predation rates were positively associated withcloud cover; vertebrates may avoid foraging in cropping fields onclear nights due to increased predation risk (Davis and Raghu,2010).

4.4. Overview

Studies involving arthropods and weeds have shown variableeffects of richness on biological control. However, most studieshave not examined other aspects of biodiversity such as evenness,genetic diversity, or functional trait diversity, and mechanisms arelargely inferred rather than demonstrated. Research is needed thatexpands beyond richness effects and develops sophisticated ap-proaches for isolating mechanisms underlying biodiversity effects.We discuss these two issues in the remainder of this review.

Fig. 2. Effects of richness on biological control, where the amount of leaf surface covered by predators correlates with the number of prey captured. In (A,B), the predatorsforage in different locations, and more prey are consumed across the whole leaf when both predators are present (A) compared to only one predator (B). In (C–F), thepredators overlap in their distribution. If predators are redundant (C–E) the same amount of prey are captured regardless of whether one (D) or both (C,E) predators arepresent. However, if intraguild predation occurs (F), total predator density decreases and biological control weakens (F).

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5. Novel research concepts: moving beyond studies of richnessand biological control

Most studies involving biodiversity and biological control ofarthropod and weed pests have examined the effects of speciesrichness. Indeed, the terms ‘‘biodiversity’’ and ‘‘richness’’ are oftenused synonymously by many authors, and incorrectly whenauthors equate richness to total diversity of a system. In the fol-lowing section we describe new frontiers in biodiversity and bio-logical control research that should be addressed to movebeyond an understanding of richness effects and increase the rele-vance for real-world agroecosystems.

5.1. Effects of evenness

Evidence is accumulating that evenness can have similar effectsto richness on a variety of ecosystem processes including biologicalcontrol (Hillebrand et al., 2008). Crowder et al. (2010) showed thatrelatively small increases in evenness of predator and pathogencommunities significantly improved control of the Colorado potatobeetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), gen-erating a strong trophic cascade and larger potato plants. Theauthors showed that intraspecific competition was reduced inmore even communities, leading to increased natural enemy sur-vival in even communities and greater pest control.

Fig. 3 shows a conceptual model for how evenness might influ-ence pest control. When natural enemy species are complemen-tary, a more even community captures more prey (A). Thisoccurs because when the community is uneven, the rare speciesdoes not saturate its’ resource niche, such that total prey consumeddecreases (B). In contrast, when natural enemies are redundant,evenness does not affect pest control because any combination ofindividuals captures the same number of prey (C,D). When preda-tors differ in their effectiveness at biological control, evennesscould have negative or positive impacts. In this case, when the

community is uneven and the more voracious predator is domi-nant, prey consumption increases compared with the even com-munity (E,F). However, if a community is uneven and the morevoracious predator is rare, evenness would have a positive effecton pest control.

This conceptual model represents some of the possible effects ofevenness on pest control, and is not meant to be exhaustive. Ineach scenario, if predator density was infinitely high, evennesswould not matter, as even the rare species would saturate its’niche. However, species rarely exist at high-enough densities to killall prey available to them (Northfield et al., 2010), such that effectsof evenness on prey consumption in most conditions will be med-iated by abundance. To our knowledge no study has varied densityand evenness in a systematic manner to test these predictions. Fu-ture research in this area is therefore warranted to uncover scenar-ios where evenness will have positive, negative, or neutral impactson biocontrol.

5.2. Realistic manipulations of biodiversity

One drawback of experiments relating biodiversity to ecosys-tem functions has been a lack of realism (Bracken et al., 2008;Byrnes and Stachowicz, 2009). In most experiments, treatmentsconsist of single species in monoculture or diverse communitieswith even distributions, such that realism is sacrificed to increaserigor and interpretability. Communities in agroecosystems, how-ever, do not vary in such predictable manners (Crowder et al.,2012). Moreover, the effects of biodiversity on ecosystem functionscan differ significantly in randomly assembled communities com-pared with non-random assemblages reflecting real-world varia-tion (Bracken et al., 2008). As described earlier, Crowder et al.(2010) overcame this problem by establishing evenness treatmentsthat reflected variation in species evenness on farms. In this way,biological control and plant densities in experimental trials wereinformative for potential impacts on farms. While these

Fig. 3. Effects of richness on biological control, where the amount of leaf surface covered by predators correlates with the number of prey captured. In (A,B), the predatorsforage in different locations, and more prey are captured when the community is even (A) than when it is uneven (B). In the latter scenario, there are too-few predatorsfeeding on the leaf edge to effectively capture prey in this spatial niche. In (C,D), the predators overlap in their distribution, and are redundant, such that evenness does notimpact biological control. In (E,F) the predators overlap in their distribution, but one is more effective at prey capture than the other. In this case, the uneven (F) communitycan outperform the even (E) community when the more effective predator is dominant, although the uneven community will underperform if the more effective predator isnot dominant (not shown).

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approaches add realism to experiments testing biological control, apotential drawback is that realistic biodiversity designs can be sta-tistically messy due to covariance in species abundances in man-aged ecosystems. Crowder et al. (2010) dealt with this issue byincluding in statistical models the abundance of each predator spe-cies in addition to biodiversity, and suggested that informationtheoretic criterion could be used to distinguish between effectsof particular species and effects of biodiversity per se. Despite thesechallenges, more experiments should attempt to realistically varybiodiversity to improve our understanding of how biological con-trol operates in real-world agroecosystems.

Diversity at multiple trophic levels also occurs in agroecosys-tems. For example, rarely do agricultural systems contain a singlepest or plant species, as weeds and crop plants are often inter-mixed. This variation can affect the biodiversity-biological controlrelationship. For example, intraguild predation amongst generalistpredators could be lessened by the availability of multiple preyspecies, although this could also weaken biological control of a fo-cal species (Frank et al., 2010, 2011). Frank et al. (2011) showedthat seed subsidies in open-field plots increased the abundanceof omnivorous carabids in corn, but there was also more cutwormdamage documented. In general, however, few studies have exam-ined effects of diversity at multiple trophic levels on biological con-trol, even though predators, herbivores, and plants co-exist inintricate food webs (Tylianakis and Binzer, 2014). Future researchin this area could improve our understanding of realistic variationthroughout food webs on biological control.

5.3. Functional diversity

Functional diversity, rather than biodiversity per se, may oftenunderlie the biodiversity-biological control relationship. When

species are lumped into functional groups based on ecologicaltraits, species in any group are considered ecologically redundantand species in different groups are complementary (Hillebrandand Matthiessen, 2009). Species can be functionally grouped basedon resource/habitat preferences and seasonal differences (North-field et al., 2012). Increased numbers of functional groups are ex-pected to increase biological control, while increased diversitywithin a functional group would not (Northfield et al., 2012). Forexample, on ragwort plants, moth larvae feed on leaves while fleabeetles tunnel into leaf petioles and roots (McEvoy et al., 1991).These two herbivores therefore represent two functional feedinggroups, and their combined presence improves ragwort control(James et al., 1992). A meta-analysis to test whether multiple nat-ural enemies used to control weeds had independent or non-inde-pendent effects on plant performance showed that, indeed,antagonistic effects were likely to occur if both enemies wereattacking the same plant part (Stephens et al., 2013). However,grouping species into functional groups can be difficult becausewe often do not have sufficient ecological information to createfunctional groups of broad relevance for ecosystem services suchas biological control (Wright et al., 2006).

Understanding functional diversity would improve our abilityto conserve natural enemy communities to improve biological con-trol. If managers could predict which functional groups are impor-tant, they could conserve functional diversity rather than diversityper se. Weed diversity can also be partitioned into functionalgroups that are more relevant to farmers. For example, weed spe-cies vary throughout the season in timing of germination and seedrain (e.g., cool season vs. warm season weeds), factors that relate totiming of herbicide, cultivation, planting, and harvest decisions.Functional diversity can also be important when considering tem-poral dynamics of arthropod pests, as natural enemy species with

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different temporal dynamics (i.e., species that attack in differentparts of a day or in a season) may be necessary to achieve adequatepest control (Welch and Harwood, 2014). Annual and perennialweeds require distinct management approaches, given the abilityfor some perennials to propagate vegetatively, particularly prob-lematic for organic farmers (e.g., Turner et al., 2007).

However, the utility of functional diversity schemes has beenquestioned, because classifications often fail to explain ecologicalprocesses (Wright et al., 2006). For example, assigning plants torandom functional groups explained as much variation in biomassand nitrogen assimilation as when plants were placed in well-de-fined groups (grasses, forbs, legumes and woody plants). Schmitz(2007) provided one of the most detailed descriptions of functionaldiversity in a system of spiders feeding on grasshopper prey. In thisscheme, Schmitz defined functional groups based on habitat do-mains, which encompass the microhabitats chosen by natural ene-mies and the extent of spatial movement in those microhabitats,and showed these groupings had strong predictive ability for pred-ator–prey relationships (Schmitz, 2008). While informative, suchschemes require detailed ecological information, and would likelyneed to be developed on a case-by-case basis. Moreover, severalstudies have suggested that climate change might shift the func-tional roles of species in ecosystems, changing functional group-ings and food-web interactions (Barton and Schmitz, 2009;Schmitz and Barton, 2014; Tylianakis and Binzer, 2014) in additionto altering temporal interactions between species (Welch and Har-wood, 2014). This will complicate our understanding of how bio-logical control might operate during periods of climate change.

5.4. Genetic diversity

Genotypic diversity can have strong consequences for ecologi-cal processes (Hughes et al., 2008; Cook-Patton et al., 2011). How-ever, few studies have examined effects of genetic diversity onbiological control. Studies from plants indicate that variation in ge-netic diversity within plant species can have similar effects com-pared with species diversity on ecosystem functions such asbiomass production (Schweitzer et al., 2005; Crutsinger et al.,2006; Johnson et al., 2006; Cook-Patton et al., 2011). Complemen-tarity has also been shown to drive positive effects of genetic diver-sity, similar to species-diversity studies (Cook-Patton et al., 2011).There is evidence that genetic diversity within species that act asbiological control agents results in variation in climatic tolerances,prey and habitat preferences, and synchrony with hosts amongothers (Hopper et al., 1993). Hopper et al. (1993) showed up to14-fold variation in these traits within populations of a single nat-ural enemy species. This suggests that genetic diversity within nat-ural enemy species, and impacts on biological control, should be apriority area for future research.

5.5. Overview

Considerable attention has been paid to the role of natural en-emy species richness in biological control. However, the relevanceof studies examining biodiversity, biological control, and real-world management could be improved by further examining otherdimensions of biodiversity in agroecosystems. In particular, wehighlight the potential importance of evenness, functional diver-sity, and genetic diversity. These facets of biodiversity consistentlyvary across real-world agroecosystems, and uncovering the mech-anisms through which these factors impact biological control is asignificant challenge for ecology. One step in the right directionmight be moving towards experiments that use realistic manipula-tions of biodiversity to improve our understanding of processes inreal-world ecosystems.

6. Elucidating mechanisms underlying the biodiversity-biological control relationship

Ecologists have struggled to identify the reasons that biodiver-sity might influence ecosystem functions like biological control(Naeem and Wright, 2003; Cardinale et al., 2006). For example, po-sitive effects could be driven by complementary (where species at-tack prey in unique ways) or facilitation (where one natural enemymight increase prey-capture by another species). Negative effectsof biodiversity might be driven by factors such as intraguild preda-tion, where different natural enemies feed on each other ratherthan pests. One roadblock has been that many traits differ amongspecies such as size, feeding preferences, and metabolism (Huston,1997; Loreau and Hector, 2001). Thus, many traits are variedwhenever species diversity is manipulated, making it difficult toidentify how a single trait like complementary niches might influ-ence biological control (Finke and Snyder, 2008; Northfield et al.,2010). One approach to separate positive or negative species inter-actions from identity effects is to determine whether ecologicalperformance of diverse communities exceeds each single species(Petchey 2003). This approach, however, fails to identify mecha-nisms underlying effects of biodiversity like complementarity orintraguild predation (Petchey 2003). Models have also been usedto test for effects of diversity in conjunction with species identityeffects (Crowder et al., 2010), yet this method also fails to identifymechanisms. Here we discuss novel methods that can directly testspecific mechanisms underlying the relationship between biodi-versity and biological control.

6.1. Linking experiments with models

Theoretical models have provided insight into the mechanismsunderlying the effects of biodiversity on biological control (Sihet al., 1998; Ives et al., 2005; Casula et al., 2006). However, modelsof biodiversity and biological control have rarely been confrontedwith data. Northfield et al. (2010) showed how models could belinked with a complex experiment to explore the relationship be-tween biodiversity and biological control. This study relied on a re-sponse-surface design (Inouye, 2001; Paini et al., 2008) wherebytotal abundance and species diversity were varied systematically.Response-surface designs allow for isolation of interspecific inter-actions characteristic of additive designs (Sih et al., 1998; Iveset al., 2005), while also taking advantage of substitutive designwhich eliminate confounding effects of abundance across treat-ments (Connolly 1988; Hooper et al., 2005).

The Northfield et al. (2010) study varied densities and speciesrichness of a community of predators attacking aphids on collardplants. The authors took advantage of the concept of niche satura-tion, whereby a single predator species is only capable of consum-ing a proportion of the total prey base. As abundance of a predatorspecies increases, they consume all of their available prey, andthereby saturate their niche, where the proportion of prey remain-ing is the proportion outside of the predator’s niche. Thus, if a sec-ond predator can consume additional prey, it indicates they wereable to consume prey outside of the first predator’s niche, indicat-ing a complementary feeding interaction. Using this framework,Northfield et al. (2010) evaluated their experimental results witha model that extended upon the framework developed by Casulaet al. (2006). In the model, parameters were included for niche par-titioning, facilitation, and niche overlap. The authors used likeli-hood-ratio tests to selectively explore whether each factorimproved the fit of the model to the data. In this way, Northfieldet al. (2010) were able to convincingly demonstrate that niche par-titioning was a key factor driving positive biodiversity effects onaphid biological control (measured in reduction of aphid numbers).

D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 15

The framework developed by Northfield et al. (2010) is general,and could be applied to other systems. Moreover, the model wouldallow for variation in richness and evenness, while still having thecapacity to test mechanisms. Future studies should use this frame-work and/or expand on it to test mechanisms driving biodiversityeffects on biological control.

6.2. Manipulations of niche-breadth

Several authors have directly demonstrated complementarityby directly manipulating niche breadth of species independent ofspecies identity. One of the best examples comes from the studyof Finke and Snyder (2008). In this study, three species of parasit-oids were ‘‘trained’’ to use a single species of aphids (i.e., they werespecialists) or multiple aphid species (i.e., they were generalists) ashosts. The authors then directly manipulated the niche overlap andspecies diversity independently within the parasitoids communi-ties. They showed that only when aphids were specialists and usedseparate host resources did increased biodiversity improve biolog-ical control, directly demonstrating that niche complementarityimproved biological control.

Gable et al. (2012) used a different approach, whereby ecologi-cal engineers were used to naturally manipulate plant habitats andniche relationships among species. In this study, conducted on col-lard plants, lady beetle predators typically foraged only on leafedges while parasitoids and true bug predators foraged in leaf cen-ters. In turn, when leaves were intact, this spatial niche partition-ing among species led to an improvement in biological control onlywhen a diverse community of natural enemies was present. How-ever, when diamondback moths were present on leaves, theychewed holes in leaves, which allowed lady beetles to forage overthe entire plant surface. In this case, increases in biodiversity didnot improve biological control. Thus, by directly manipulating spa-tial niche partitioning among predators, the authors showed thatspatial complementarity could explain the biodiversity-biologicalcontrol relationship.

An advantage of these approaches is that they might reveal howdiversity effects naturally vary across ecosystems, with speciescomplementing one another only in certain situations. The draw-back is that they require quite a detailed understanding of speciestraits, so complementarity can be directly manipulated. Despitethis challenge, more studies in this vein would help uncover mech-anisms driving the relationship between biodiversity and biologi-cal control.

7. Managing for biodiversity and biological control

Overall, agricultural managers face an uncertain future of moreextreme and changing climatic conditions, depleting water supply,and increased costs of fossil fuels. In this review we show thatdiversification of agroecosystems generally decreases impacts onnatural resources, promotes more diverse natural enemy commu-nities, and strengthens biological control. While agricultural inten-sification is likely to continue, it is clear that future farmingsystems will have to consider biodiversity and natural ecosystemfunctions such as biological control to continue to meet the globalchallenges facing agriculture in a sustainable and efficient manner.

One central management challenge that this paper poses is‘‘how can we manage for diversity while suppressing both insectand weedy pests?’’ Insects and weeds are rarely considered in con-cert by researchers, although growers of course face both everyday. As demonstrated here, many taxa in agricultural food webscontribute to biological control of insects and weeds. In turn, asresearchers and practitioners in diversified farming systems, wemust focus more on integrating biological control of weeds and

insects, and managing for conservation of diverse groups that con-tribute to this function such as invertebrates, mammals, and birds.Managers can work to restore diversity through a variety ofmanipulations.

For example, crop rotation has nutrient and pest managementbenefits, and serves as a strategy to diversify agricultural systems.A comparison of rotation systems in Iowa, ranging from 2 to 4 yearsequences with varying levels of synthetic inputs, demonstratedthat weeds were suppressed in all systems, and yield and profitwas the same or improved in diversified rotations as comparedto the conventional 2-year corn-soybean rotation (Davis et al.,2012). Weeds in the diversified rotations were managed using avariety of strategies, effective by targeting weeds at differentstages in the life cycle and season (Liebman and Gallandt, 1997).Furthermore, crop rotations in these areas were effective at con-trolling corn rootworm pests that lay eggs in corn fields, as eggshatching in soybean fields the following year die (Onstad et al.,2003).

One notable result of agricultural intensification and specializa-tion has been the decoupling of crop and livestock production sys-tems. The availability and low cost of synthetic fertilizer hasenabled crop production without the need for animal manure,and efficient feedlot technology and inexpensive feed has enabledlivestock production separate from cropland. Re-integrating cropand livestock systems has been proposed as a solution to manyenvironmental problems of modern agriculture, such as nitrogenleaching, poor soil quality, and manure management (Russelleet al., 2007). Re-integration also has the potential to improve pestcontrol via biological control in the form of grazing. In Montana,sheep grazing of dryland grain fallow and alfalfa contributed tomanagement of wheat steam sawfly and alfalfa weevil, major pestsin these respective systems, and weedy plants (Goosey et al., 2005;Goosey, 2012). Although this strategy may be logistically and eco-nomically challenging for a single grower to accomplish, partner-ships amongst growers within a local area could lead tosuccessful integration.

Crop rotations and coupling crop and livestock production arejust two of many potential options for growers to potentially con-serve biodiversity and promote ecosystem services like biologicalcontrol. To truly promote sustainability in our agroecosystems, itwill be essential for managers to consider multiple aspects of com-munities such as richness, evenness, abundance, and species iden-tity to maximize potential benefits for farming systems. While thisis a daunting challenge, it is one we must overcome for agricultureto continue to meet the demands of a growing human populationin an ever-changing world.

Acknowledgments

We thank W.E. Snyder for useful discussions that helped themanuscript. This project was supported by a USDA AFRI FellowshipGrant (WNW-2010-05123) to DC.

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