Biological Control 75 (2014) 8–17

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Biological Control

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Relationships between biodiversity and biological control in agroecosystems: Current status and future challenges ⇑ David W. Crowder a, , Randa Jabbour b

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

highlights graphical abstract

 Agricultural systems are intensifying to keep up with growing human demands.  Intensive can negatively impact biodiversity and biological control.  We review biodiversity and biological control of arthropod and weedy pests.  We discuss similarities and differences between biocontrol of arthropods and weeds.  We suggest novel approaches for examining biodiversity and biological control.

article info abstract

Article history: Agricultural systems around the world are faced with the challenge of providing for the demands of a Available online 1 November 2013 growing human population. To meet this demand, agricultural systems have intensified to produce more crops per unit area at the expense of greater inputs. Agricultural intensification, while yielding more Keywords: crops, generally has detrimental impacts on biodiversity. However, intensified agricultural systems often Agricultural intensification have fewer pests than more ‘‘environmentally-friendly’’ systems, which is believed to be primarily due to Conservation extensive pesticide use on intensive . In turn, to be competitive, less-intensive agricultural systems Ecosystem functioning must rely on biological control of pests. is a complex ecosystem service that is gen- Evenness erally positively associated with biodiversity of natural enemy guilds. Yet, we still have a limited under- Richness standing of the relationships between biodiversity and biological control in agroecosystems, and the mechanisms underlying these relationships. Here, we review the effects of agricultural intensification on the diversity of natural enemy communities attacking arthropod pests and weeds. We next discuss how biodiversity of these communities impacts pest control, and the mechanisms underlying these effects. 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 used to explore the relationships between biodiversity and biological control in agroecosystems. In particular, we highlight new experimental frontiers regarding evenness, realistic manipulations of biodiversity, and functional and genetic diversity. Management shifts that aim to conserve diversity while suppressing both 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 biodiversity effects, would improve efforts to strengthen biological control in agroecosystems. Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction

⇑ Corresponding author. Human has led to the global expansion of E-mail address: [email protected] (D.W. Crowder). agriculture. The acreage of land used for crops increased by 466%

1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biocontrol.2013.10.010 D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 9 from 1700 to the 1980s (Meyer and Turner, 1992). This growth, species. Some of the longest-term studies of agricultural intensifi- however, has slowed in recent decades as suitable areas for culti- cation and biodiversity have focused on bird populations in Europe, vation become increasingly scarce (Matson et al., 1997). As growth which have declined dramatically over the last half-century of agricultural acreage has stagnated, agricultural systems around (Benton et al., 2003). Donald et al. (2001) showed that bird the world have intensified. Agricultural intensification is a broad populations in the UK declined with increases in cereal and milk term that encompasses many factors including, but not limited yields along with and tractor usage. Cereal yields alone to, increased use of pesticides and (see Roubos et al., explained 31% of the variability in declining bird populations, 2014), increases in size, decreases in , increases suggesting that intensification of a single crop type can impact in crop density, and increased numbers of crops grown in a season. diversity (Donald et al., 2001). This has been due in large part to dramatic increases in crop yields There is evidence, however, that agri-environment schemes en- since the 1960s, referred to as the ‘‘’’ (Pingali, acted by many European countries to encourage wildlife have led 2012), which has been spurred by technological and cultural ad- to resurgence of some bird species (Benton et al., 2003). Agri-envi- vances in crop breeding and management (Matson et al., 1997; ronment schemes provide monetary incentives for to man- Krebs et al., 1999; Benton et al., 2003). age a portion of their land to promote conservation of biodiversity While agriculture has kept pace with human population and reduced impacts on the environment (Benton et al., 2003; growth, increases in crop yields has also slowed recently (FAO, Kleijn et al., 2006). By incorporating or conserving natural habitat 2013). Moreover, agricultural intensification has negative local in agricultural ecosystems to preserve native species, these consequences such as reduced biodiversity, increased soil erosion, schemes are designed to buffer against potentially damaging pollution, and reduced socio-economic sustainability, each of effects from agricultural intensification on biodiversity. Kleijn which has other impacts (Matson et al., 1997; Stoate et al., 2001; et al., 2006 compared the abundance and richness of plants, birds, Kleijn et al., 2006). For example, reducing the number of species and arthropods at 202 paired locations across five European (reduced richness) (Hooper et al., 2005; Cardinale et al., 2006) counties. Each location contained one site managed with an and skewed relative abundance distributions (reduced species agri-environment scheme and one conventional site. The agri- evenness) (Hillebrand et al., 2008; Crowder et al., 2010) generally environment schemes had some positive impacts on abundance weaken biological control. These harmful consequences of agricul- and diversity of these groups in each country, while conventional tural intensification have led to an increased focus on methods to management did not benefit any group (Kleijn et al., 2006). The increase the sustainability of agroecosystems (Tilman, 1999; Foley authors speculated that benefits were due to reduced inputs and et al., 2011). disturbances in agri-environment fields. However, the species that Biological control is a key ecosystem service that is necessary benefitted most from agri-environment schemes did not include for sustainable crop production (Bianchi et al., 2006; Losey and many species of concern. This suggests that conserving Vaughan, 2006). Natural enemies such as predators, parasitoids, native habitat may not benefit rare species, or that species of and pathogens play a central role in limiting damage from native extinction concern declined in abundance due to factors other than and exotic pests (Hawkins et al., 1999; Losey and Vaughan, agricultural intensification. 2006). Conservative estimates suggest that the economic value Crowder et al. (2010, 2012) showed that sys- provided by insect natural enemies controlling pests attacking crop tems had marginal positive impacts on richness and significant po- plants exceeds $4.5 billion annually in the United States (Losey and sitive impacts on evenness and abundance compared with Vaughan, 2006). If weedy pests, or pests attacking humans and conventional systems. These benefits occurred across crop types (not crops) were considered the estimate of pest control and were consistent across several organismal groups including provided by insects would likely be much greater. Moreover, a arthropods, birds, non-bird vertebrates, plants, and soil organisms. multitude of species act as natural enemies of insect or weedy The benefits of organic farming were greatest for the rarest species pests such as birds, bats, fungi, nematodes, and rodents (Kirk in conventional systems (Crowder et al., 2012). Other reviews et al., 1996; Miller and Surlykke, 2001; Navntoft et al., 2009; Ra- (Bengtsson et al., 2005; Hole et al., 2005) have shown similar posi- mirez and Snyder, 2009; Williams et al., 2009; Jabbour et al., tive impacts of organic farming on richness and abundance of 2011). Thus, if these species were considered the economic value organisms. In each case, these results are likely due to reduced of biological control would be far greater than $4.5 billion annually. insecticide use in organic farming systems and/or increased habitat To improve and conserve biological control, it is essential to diversity. For example, granivorous beetle diversity has been understand the relationships between agricultural intensification, shown to be positively associated with habitat complexity on biodiversity, and pest suppression. We addresses this complex is- farms (Vanbergen et al., 2010; Trichard et al., 2013), and negatively sue by first reviewing the effects of agricultural intensification on associated with use of pesticides (Trichard et al., 2013). the biodiversity of natural enemies, and the role of natural enemies in agricultural food webs. We next discuss conceptual models 2.2. Arthropod pests relating biodiversity to natural pest control. Third, we review methodologies for examining the relationship between biodiver- Root (1973) suggested that dense, homogenous plant commu- sity and biological control in agroecosystems. We conclude by dis- nities facilitated higher herbivore populations. His ‘‘resource-con- cussing areas of research emphasis that, if addressed, would centration hypothesis’’ posits that specialist pests can locate improve our understanding of how biodiversity and biological con- plant stands, and feed more efficiently, when a single non-diverse trol operate in agroecosystems. crop is present. Thus, intensification may actually be responsible for pest outbreaks so common in . However, this 2. Effects of agricultural intensification on biodiversity hypothesis does not hold true for all cases, suggesting that re- source-concentration effects are organism dependent (Grez and 2.1. Non-pest species Gonzalez, 1995). Secondary pest outbreaks, where early-season insecticide applications kill natural enemies and result in late-sea- Agricultural intensification impacts both pest and non-pest spe- son outbreaks of pests, have also received attention as a negative cies in agricultural communities. Indeed, much of the evidence of impact of agricultural intensification. For example, Gross and the impacts of agricultural intensification on ecological Rosenheim (2011) showed that 20% of late-season pesticide costs communities comes from conservation-related studies on non-pest were attributable to early-season pesticide applications for control 10 D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 of lygus bugs. This is perhaps not surprising as pesticides can dis- 2.5. Overview rupt natural enemy populations at broad scales (Roubos et al., 2014) and might disrupt periods of temporal overlap between The studies discussed here show that agricultural intensifica- pests and their natural enemies (Welch and Harwood, 2014). tion has complex effects on pests and beneficial species. In general, Comparison of organic and conventional farming systems also more intensive systems decrease the abundance and biodiversity suggest mixed effects of intensification on pests. For example, of beneficial species such as natural enemies. At the same time, aphids tend to be more abundant in conventional farms due to intensification might exacerbate pest problems by concentrating higher-quality crops that grow faster, while mites and true bugs arthropod resources and decreasing populations of natural ene- tend to be more common in organic farms (Hole et al., 2005). mies. In the following sections we discuss how disruptions in bio- Across multiple pest groups, Bengtsson et al. (2005) found no sig- diversity of pests and natural enemies caused by agricultural nificant effect of organic farming on abundance or species richness. intensification can influence species interactions and have strong This result is perhaps surprising given that conventional farms impacts on biological control. tend to use significantly more pesticides compared with organic farms, which should limit pest populations (Bengtsson et al., 2005; Hole et al., 2005). This perhaps suggests that for many pest 3. Why does biodiversity matter? Exploring agricultural food herbivores that increased effectiveness of natural enemies in or- webs ganic farming systems might allow for pest control equivalent, or nearly equivalent, to control achieved with pesticides (Crowder Reductions in biodiversity can disrupt food webs and weaken et al., 2010, 2012). biological control (Tylianakis et al., 2007; Macfadyen et al., 2009; Schmitz and Barton, 2014; Tylianakis and Binzer, 2014). Trophic 2.3. Weeds cascades have been a central concept in biocontrol studies since Hairston et al. (1960) proposed the ‘‘Green World Hypothesis’’, Weed communities are consistently more abundant and rich in whereby natural enemies protect plants by regulating pests. How- less-intensive agricultural systems. For example, organic farms ever, the role of biodiversity in generating trophic cascades has generally harbor 2.3–2.8 times more abundant weed seed densities been questioned (Strong, 1992; Polis and Strong, 1996; Polis, and 1.3–1.6 times more weed species compared with conventional 1999). A key criticism is that in complex food webs, removal of a farms (Roschewitz et al., 2005; Gabriel et al., 2006; Hawes et al., single species is unlikely to influence cascades. Indeed, studies 2010; José-María and Sans, 2011). Frequent herbicide use in inten- have shown that natural enemy diversity can promote (Cardinale sive agroecosystems likely drives reduced weed diversity and et al., 2003; Snyder et al., 2006; Crowder et al., 2010) or weaken abundance. In addition, weed communities often vary based on trophic cascades (Finke and Denno, 2004, 2005). Understanding inorganic fertilizer use and crop rotations (Hawes et al., 2010). the food webs in which natural enemies and pests interact is thus Hawes et al. (2010) showed that fertilizer use and rotations ex- central to understanding relationships between biodiversity and plained as much variation in weed abundance/ diversity as farm biological control. type across 109 conventional, integrated, and organic farms. Syn- Arthropod food webs are discussed by Tylianakis and Binzer, thetic fertilizer use was negatively associated with weed abun- 2014, and we do not expound on them here. Weeds also play key dance, an unsurprising result given that farms using synthetic roles in agricultural food webs and may thus influence biodiversity fertilizers also likely use synthetic herbicides. However, organic and biological control (Fig. 1). Farmers generally aim to manage manures are known as likely sources of weed seed (Mt. Pleasant weeds given their considerable agricultural and economic risks, and Schlather, 1994), a risk that farmers and scientists acknowl- although they do acknowledge the ecological benefits of weeds edge readily in discussions of weed introduction and weed spread (Wilson et al., 2008; Jabbour et al., 2013). As hypothesized by Root (Jabbour et al., 2013). (1973), plant diversity is often negatively associated with herbi- Weed communities on farms are also influenced by the sur- vore abundance (Cardinale et al., 2012). Weeds comprise a large rounding landscape (see also Chisholm et al., 2014). For example, component of floral diversity in agroecosystems, given the compa- weed vegetation and seedbank diversity in German wheat fields rably low diversity of most crop plantings, and thus may play a key was positively associated with landscape complexity around farms role in limiting pests from the bottom-up. (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 organic fields in simple landscapes. In contrast, effects of landscape com- plexity on weed seedbanks in Mediterranean dryland systems were 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 might be a strategy for less-intensive farmers to manage weeds.

2.4. Other pests

There is evidence that agricultural intensification influences pathogens (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 the Fig. 1. A hypothetical agricultural food web, where arrows indicate energy flow. spread of crop pathogens. While not a focus of this review due to Biological control of weeds and insect prey involve several of the same animal limited studies, effects of biodiversity on biological control of groups, including potential intraguild predation amongst birds, mammals, and pathogens should be examined further. insect omnivores and predators. D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 11

In addition to the potential contribution of weed diversity to involving arthropod pests observed positive effects of natural en- limiting pests, the resource of weed seeds in particular can have emy richness on pest suppression, with particularly strong effects major impacts on food webs. Weed seed resources can support a in agricultural systems. Nearly all of the remaining 30% of studies, high diversity of granivorous and omnivorous species including however, showed a negative relationship between natural enemy mammals, birds, arthropods, earthworms, and slugs (Franke richness on pest suppression. Yet, the magnitude of the average et al., 2009). A detailed study of the seed-based food web on an or- negative effect was 63% that of the average positive effect, suggest- ganic farm in the UK estimated that 274 arthropod, 53 bird, and 10 ing that natural enemy richness was more likely to generate strong mammal species likely used seeds as a resource (Evans et al., positive impacts than strong negative effects. Letourneau et al. 2011). However, these effects can be quite nuanced and dependent (2009) could not distinguish between the mechanisms underlying on crop type. A recent study focused on farmland birds showed these effects of richness, however. Thus, it was unclear whether that genetically-modified beet and oilseed crop systems had less more diverse communities promoted pest control because natural weed seed resources used by birds than conventional systems enemies tended to act complementary or facilitated prey-capture (Gibbons et al., 2006). In contrast, genetically-modified maize by other species, or whether more diverse communities were more had more seed available for birds than conventional systems. likely to contain particularly effective natural enemy species by Although seed resources can support omnivores, seed availability chance alone (otherwise known as a sampling or species identity may also distract from insect pest control by natural enemies effect). (e.g., Frank et al., 2011). These studies demonstrate that natural enemy consumers and their resources (arthropod and weedy pests) interact in complex 4.3. The richness-biological control relationship in studies involving food webs (see also Tylianakis and Binzer, 2014). Food-web ecol- weedy pests ogy is a burgeoning field that could thus contribute to our under- standing of the relationship between biodiversity and biological Evidence for richness effects on biological control of weeds is control. We expound on this issue in the following section. less common than for arthropods. However, in Wisconsin and France, richer seed-feeding beetle communities were associated with increased weed seed loss from experiments (Gaines and Grat- 4. Relating richness to biological control ton, 2010; Trichard et al., 2013). This positive relationship occurred in both crop and non-crop habitats in Wisconsin potato agroeco- 4.1. Mechanisms underlying effects of richness on biological control systems (Gaines and Gratton, 2010). As with arthropods, indirect evidence suggests that complementarity may underlie these ef- The mechanisms by which species richness affects biological fects. Invertebrate granivores eat smaller seeds on average com- control of arthropods have been reviewed (Schmitz, 2007; Letour- pared to mammals and birds, such that the combined impacts of neau et al., 2009), and we only briefly discuss them to provide con- both guilds of natural enemies strengthened weed suppression in text for the remainder of the review (Fig. 2). Positive richness the Gaines and Gratton study (2010). Different birds species vary effects occur when species act complementarily in terms of pest in their weed-seed preferences as well (Perkins et al., 2007). Weed suppression, or when one or more species facilitates prey capture predators also may be temporally complementary, with inverte- by another, such that the combined impact of multiple species ex- brate seed consumption decreasing and vertebrate consumption ceeds the mortality any species exerts on its own (Losey and Den- increasing as winter approaches (Davis and Raghu, 2010). no, 1998; Finke and Snyder, 2008; Northfield et al., 2010). Positive Alternatively, seed consumer richness may negatively affect richness effects can also occur through ‘‘insurance effects’’, where a weed seed predation via intraguild predation. Many granivores in more species rich community effectively performs biological con- the seed-based food web are omnivores who also prey upon inver- trol despite disturbances because one or more species is resilient tebrates. Small mammals feed on insects as well as seeds, and to a disturbance even while others are negatively affected (Naeem could negatively impact invertebrate granivores. For example, and Li, 1997; Yachi and Loreau, 1999). In contrast, increasing spe- excluding rodents from experimental plots in shrub-steppe habi- cies richness can negatively impact biological control when natural tats resulted in increased carabid abundance following a two year enemies feed on each other, an occurrence known as intraguild period (Parmenter and MacMahon, 1988). Moreover, a study of predation, which limits predator density and impact on pests invertebrate and vertebrate predation in corn fields highlighted (Finke and Denno, 2004, 2005; Rosenheim, 2007). Behavioral inter- the potential influence of predation risk of seed predators on seed ference among predator species can also weaken biological control predation rates (Davis and Raghu, 2010). Invertebrate seed preda- with increases in natural enemy richness (Schmitz, 2007). tion was negatively associated with abundance of spiders, poten- Many authors have also pointed out that the positive or nega- tial predators of granivorous crickets active in that system. Also, tive impacts of species richness on ecosystem functions such as vertebrate seed predation rates were positively associated with biological control can be due to statistical chance. In this scenario, cloud cover; vertebrates may avoid foraging in cropping fields on richer communities could improve biological control simply be- clear nights due to increased predation risk (Davis and Raghu, cause they have a higher probability of containing a superior nat- 2010). ural enemy species (Naeem and Wright, 2003; Cardinale et al., 2006). In contrast, richer communities might also have a higher probability of containing a disruptive species (like a voracious 4.4. Overview intraguild predator), which could weaken biological control (known as a selection effect; Loreau and Hector, 2001). Studies involving arthropods and weeds have shown variable effects of richness on biological control. However, most studies 4.2. The richness-biological control relationship in studies involving have not examined other aspects of biodiversity such as evenness, arthropod pests genetic diversity, or functional trait diversity, and mechanisms are largely inferred rather than demonstrated. Research is needed that Studies relating richness to arthropod biological control have expands beyond richness effects and develops sophisticated ap- variably shown positive, negative, and neutral effects. In a meta- proaches for isolating mechanisms underlying biodiversity effects. analysis, Letourneau et al. (2009) showed that 71% of studies We discuss these two issues in the remainder of this review. 12 D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17

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 predators forage 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), the predators 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 are present. However, if intraguild predation occurs (F), total predator density decreases and biological control weakens (F).

5. Novel research concepts: moving beyond studies of richness community is uneven and the more voracious predator is domi- and biological control nant, prey consumption increases compared with the even com- munity (E,F). However, if a community is uneven and the more Most studies involving biodiversity and biological control of voracious predator is rare, evenness would have a positive effect arthropod and weed pests have examined the effects of species on pest control. richness. Indeed, the terms ‘‘biodiversity’’ and ‘‘richness’’ are often This conceptual model represents some of the possible effects of used synonymously by many authors, and incorrectly when evenness on pest control, and is not meant to be exhaustive. In authors equate richness to total diversity of a system. In the fol- each scenario, if predator density was infinitely high, evenness lowing section we describe new frontiers in biodiversity and bio- would not matter, as even the rare species would saturate its’ logical control research that should be addressed to move niche. However, species rarely exist at high-enough densities to kill beyond an understanding of richness effects and increase the rele- all prey available to them (Northfield et al., 2010), such that effects vance for real-world agroecosystems. of evenness on prey consumption in most conditions will be med- iated by abundance. To our knowledge no study has varied density 5.1. Effects of evenness and evenness in a systematic manner to test these predictions. Fu- ture research in this area is therefore warranted to uncover scenar- Evidence is accumulating that evenness can have similar effects ios where evenness will have positive, negative, or neutral impacts to richness on a variety of ecosystem processes including biological on biocontrol. control (Hillebrand et al., 2008). Crowder et al. (2010) showed that relatively small increases in evenness of predator and pathogen 5.2. Realistic manipulations of biodiversity communities significantly improved control of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), gen- One drawback of experiments relating biodiversity to ecosys- erating a strong trophic cascade and larger potato plants. The tem functions has been a lack of realism (Bracken et al., 2008; authors showed that intraspecific competition was reduced in Byrnes and Stachowicz, 2009). In most experiments, treatments more even communities, leading to increased natural enemy sur- consist of single species in or diverse communities vival in even communities and greater pest control. with even distributions, such that realism is sacrificed to increase Fig. 3 shows a conceptual model for how evenness might influ- rigor and interpretability. Communities in agroecosystems, how- ence pest control. When natural enemy species are complemen- ever, do not vary in such predictable manners (Crowder et al., tary, a more even community captures more prey (A). This 2012). Moreover, the effects of biodiversity on ecosystem functions occurs because when the community is uneven, the rare species can differ significantly in randomly assembled communities com- does not saturate its’ resource niche, such that total prey consumed pared with non-random assemblages reflecting real-world varia- decreases (B). In contrast, when natural enemies are redundant, tion (Bracken et al., 2008). As described earlier, Crowder et al. evenness does not affect pest control because any combination of (2010) overcame this problem by establishing evenness treatments individuals captures the same number of prey (C,D). When preda- that reflected variation in species evenness on farms. In this way, tors differ in their effectiveness at biological control, evenness biological control and plant densities in experimental trials were could have negative or positive impacts. In this case, when the informative for potential impacts on farms. While these D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 13

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 predators forage 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 predators feeding 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 not impact 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) community can outperform the even (E) community when the more effective predator is dominant, although the uneven community will underperform if the more effective predator is not dominant (not shown).

approaches add realism to experiments testing biological control, a species are lumped into functional groups based on ecological potential drawback is that realistic biodiversity designs can be sta- traits, species in any group are considered ecologically redundant tistically messy due to covariance in species abundances in man- and species in different groups are complementary (Hillebrand aged ecosystems. Crowder et al. (2010) dealt with this issue by and Matthiessen, 2009). Species can be functionally grouped based including in statistical models the abundance of each predator spe- on resource/habitat preferences and seasonal differences (North- cies in addition to biodiversity, and suggested that information field et al., 2012). Increased numbers of functional groups are ex- theoretic criterion could be used to distinguish between effects pected to increase biological control, while increased diversity of particular species and effects of biodiversity per se. Despite these within a functional group would not (Northfield et al., 2012). For challenges, more experiments should attempt to realistically vary example, on ragwort plants, moth larvae feed on leaves while flea biodiversity to improve our understanding of how biological con- beetles tunnel into leaf petioles and roots (McEvoy et al., 1991). trol operates in real-world agroecosystems. These two herbivores therefore represent two functional feeding Diversity at multiple trophic levels also occurs in agroecosys- groups, and their combined presence improves ragwort control tems. For example, rarely do agricultural systems contain a single (James et al., 1992). A meta-analysis to test whether multiple nat- pest or plant species, as weeds and crop plants are often inter- ural enemies used to control weeds had independent or non-inde- mixed. This variation can affect the biodiversity-biological control pendent effects on plant performance showed that, indeed, relationship. For example, intraguild predation amongst generalist antagonistic effects were likely to occur if both enemies were predators could be lessened by the availability of multiple prey attacking the same plant part (Stephens et al., 2013). However, species, although this could also weaken biological control of a fo- grouping species into functional groups can be difficult because cal species (Frank et al., 2010, 2011). Frank et al. (2011) showed we often do not have sufficient ecological information to create that seed subsidies in open-field plots increased the abundance functional groups of broad relevance for ecosystem services such of omnivorous carabids in corn, but there was also more cutworm as biological control (Wright et al., 2006). damage documented. In general, however, few studies have exam- Understanding functional diversity would improve our ability ined effects of diversity at multiple trophic levels on biological con- to conserve natural enemy communities to improve biological con- trol, even though predators, herbivores, and plants co-exist in trol. If managers could predict which functional groups are impor- intricate food webs (Tylianakis and Binzer, 2014). Future research tant, they could conserve functional diversity rather than diversity in this area could improve our understanding of realistic variation per se. Weed diversity can also be partitioned into functional throughout food webs on biological control. groups that are more relevant to farmers. For example, weed spe- cies vary throughout the season in timing of germination and seed 5.3. Functional diversity rain (e.g., cool season vs. warm season weeds), factors that relate to timing of herbicide, cultivation, planting, and harvest decisions. Functional diversity, rather than biodiversity per se, may often Functional diversity can also be important when considering tem- underlie the biodiversity-biological control relationship. When poral dynamics of arthropod pests, as natural enemy species with 14 D.W. Crowder, R. Jabbour / Biological Control 75 (2014) 8–17 different temporal dynamics (i.e., species that attack in different 6. Elucidating mechanisms underlying the biodiversity- parts of a day or in a season) may be necessary to achieve adequate biological control relationship pest control (Welch and Harwood, 2014). Annual and perennial weeds require distinct management approaches, given the ability Ecologists have struggled to identify the reasons that biodiver- for some perennials to propagate vegetatively, particularly prob- sity might influence ecosystem functions like biological control lematic for organic farmers (e.g., Turner et al., 2007). (Naeem and Wright, 2003; Cardinale et al., 2006). For example, po- However, the utility of functional diversity schemes has been sitive effects could be driven by complementary (where species at- questioned, because classifications often fail to explain ecological tack prey in unique ways) or facilitation (where one natural enemy processes (Wright et al., 2006). For example, assigning plants to might increase prey-capture by another species). Negative effects random functional groups explained as much variation in biomass of biodiversity might be driven by factors such as intraguild preda- and nitrogen assimilation as when plants were placed in well-de- tion, where different natural enemies feed on each other rather fined groups (grasses, forbs, legumes and woody plants). Schmitz than pests. One roadblock has been that many traits differ among (2007) provided one of the most detailed descriptions of functional species such as size, feeding preferences, and metabolism (Huston, diversity in a system of spiders feeding on grasshopper prey. In this 1997; Loreau and Hector, 2001). Thus, many traits are varied scheme, Schmitz defined functional groups based on habitat do- whenever species diversity is manipulated, making it difficult to mains, which encompass the microhabitats chosen by natural ene- identify how a single trait like complementary niches might influ- mies and the extent of spatial movement in those microhabitats, ence biological control (Finke and Snyder, 2008; Northfield et al., and showed these groupings had strong predictive ability for pred- 2010). One approach to separate positive or negative species inter- ator–prey relationships (Schmitz, 2008). While informative, such actions from identity effects is to determine whether ecological schemes require detailed ecological information, and would likely performance of diverse communities exceeds each single species need to be developed on a case-by-case basis. Moreover, several (Petchey 2003). This approach, however, fails to identify mecha- studies have suggested that climate change might shift the func- nisms underlying effects of biodiversity like complementarity or tional roles of species in ecosystems, changing functional group- intraguild predation (Petchey 2003). Models have also been used ings and food-web interactions (Barton and Schmitz, 2009; to test for effects of diversity in conjunction with species identity Schmitz and Barton, 2014; Tylianakis and Binzer, 2014) in addition effects (Crowder et al., 2010), yet this method also fails to identify to altering temporal interactions between species (Welch and Har- mechanisms. Here we discuss novel methods that can directly test wood, 2014). This will complicate our understanding of how bio- specific mechanisms underlying the relationship between biodi- logical control might operate during periods of climate change. versity and biological control.

5.4. Genetic diversity 6.1. Linking experiments with models Genotypic diversity can have strong consequences for ecologi- Theoretical models have provided insight into the mechanisms cal processes (Hughes et al., 2008; Cook-Patton et al., 2011). How- underlying the effects of biodiversity on biological control (Sih ever, few studies have examined effects of genetic diversity on et al., 1998; Ives et al., 2005; Casula et al., 2006). However, models biological control. Studies from plants indicate that variation in ge- of biodiversity and biological control have rarely been confronted netic diversity within plant species can have similar effects com- with data. Northfield et al. (2010) showed how models could be pared with species diversity on ecosystem functions such as linked with a complex experiment to explore the relationship be- biomass production (Schweitzer et al., 2005; Crutsinger et al., tween biodiversity and biological control. This study relied on a re- 2006; Johnson et al., 2006; Cook-Patton et al., 2011). Complemen- sponse-surface design (Inouye, 2001; Paini et al., 2008) whereby tarity has also been shown to drive positive effects of genetic diver- total abundance and species diversity were varied systematically. sity, similar to species-diversity studies (Cook-Patton et al., 2011). Response-surface designs allow for isolation of interspecific inter- There is evidence that genetic diversity within species that act as actions characteristic of additive designs (Sih et al., 1998; Ives biological control agents results in variation in climatic tolerances, et al., 2005), while also taking advantage of substitutive design prey and habitat preferences, and synchrony with hosts among which eliminate confounding effects of abundance across treat- others (Hopper et al., 1993). Hopper et al. (1993) showed up to ments (Connolly 1988; Hooper et al., 2005). 14-fold variation in these traits within populations of a single nat- The Northfield et al. (2010) study varied densities and species ural enemy species. This suggests that genetic diversity within nat- richness of a community of predators attacking aphids on collard ural enemy species, and impacts on biological control, should be a plants. The authors took advantage of the concept of niche satura- priority area for future research. tion, whereby a single predator species is only capable of consum- ing a proportion of the total prey base. As abundance of a predator 5.5. Overview species increases, they consume all of their available prey, and thereby saturate their niche, where the proportion of prey remain- Considerable attention has been paid to the role of natural en- ing is the proportion outside of the predator’s niche. Thus, if a sec- emy species richness in biological control. However, the relevance ond predator can consume additional prey, it indicates they were of studies examining biodiversity, biological control, and real- able to consume prey outside of the first predator’s niche, indicat- world management could be improved by further examining other ing a complementary feeding interaction. Using this framework, dimensions of biodiversity in agroecosystems. In particular, we Northfield et al. (2010) evaluated their experimental results with highlight the potential importance of evenness, functional diver- a model that extended upon the framework developed by Casula sity, and genetic diversity. These facets of biodiversity consistently et al. (2006). In the model, parameters were included for niche par- vary across real-world agroecosystems, and uncovering the mech- titioning, facilitation, and niche overlap. The authors used likeli- anisms through which these factors impact biological control is a hood-ratio tests to selectively explore whether each factor significant challenge for ecology. One step in the right direction improved the fit of the model to the data. In this way, Northfield might be moving towards experiments that use realistic manipula- et al. (2010) were able to convincingly demonstrate that niche par- tions of biodiversity to improve our understanding of processes in titioning was a key factor driving positive biodiversity effects on real-world ecosystems. aphid 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, insects, and managing for conservation of diverse groups that con- and could be applied to other systems. Moreover, the model would tribute to this function such as invertebrates, mammals, and birds. allow for variation in richness and evenness, while still having the Managers can work to restore diversity through a variety of capacity to test mechanisms. Future studies should use this frame- manipulations. work and/or expand on it to test mechanisms driving biodiversity For example, crop rotation has nutrient and pest management effects on biological control. benefits, and serves as a strategy to diversify agricultural systems. A comparison of rotation systems in Iowa, ranging from 2 to 4 year sequences with varying levels of synthetic inputs, demonstrated 6.2. Manipulations of niche-breadth that weeds were suppressed in all systems, and yield and profit was the same or improved in diversified rotations as compared Several authors have directly demonstrated complementarity to the conventional 2-year corn- rotation (Davis et al., by directly manipulating niche breadth of species independent of 2012). Weeds in the diversified rotations were managed using a species identity. One of the best examples comes from the study variety of strategies, effective by targeting weeds at different of Finke and Snyder (2008). In this study, three species of parasit- stages in the life cycle and season (Liebman and Gallandt, 1997). oids were ‘‘trained’’ to use a single species of aphids (i.e., they were Furthermore, crop rotations in these areas were effective at con- specialists) or multiple aphid species (i.e., they were generalists) as trolling corn rootworm pests that lay eggs in corn fields, as eggs hosts. The authors then directly manipulated the niche overlap and hatching in soybean fields the following year die (Onstad et al., species diversity independently within the parasitoids communi- 2003). ties. They showed that only when aphids were specialists and used One notable result of agricultural intensification and specializa- separate host resources did increased biodiversity improve biolog- tion has been the decoupling of crop and livestock production sys- ical control, directly demonstrating that niche complementarity tems. The availability and low cost of synthetic fertilizer has improved biological control. enabled crop production without the need for animal manure, Gable et al. (2012) used a different approach, whereby ecologi- and efficient feedlot technology and inexpensive feed has enabled cal engineers were used to naturally manipulate plant habitats and livestock production separate from cropland. Re-integrating crop niche relationships among species. In this study, conducted on col- and livestock systems has been proposed as a solution to many lard plants, lady beetle predators typically foraged only on leaf environmental problems of modern agriculture, such as nitrogen edges while parasitoids and true bug predators foraged in leaf cen- leaching, poor soil quality, and manure management (Russelle ters. In turn, when leaves were intact, this spatial niche partition- et al., 2007). Re-integration also has the potential to improve pest ing among species led to an improvement in biological control only control via biological control in the form of . In Montana, when a diverse community of natural enemies was present. How- grazing of dryland grain fallow and alfalfa contributed to ever, when diamondback moths were present on leaves, they management of wheat steam sawfly and alfalfa weevil, major pests chewed holes in leaves, which allowed lady beetles to forage over in these respective systems, and weedy plants (Goosey et al., 2005; the entire plant surface. In this case, increases in biodiversity did Goosey, 2012). Although this strategy may be logistically and eco- not improve biological control. Thus, by directly manipulating spa- nomically challenging for a single grower to accomplish, partner- tial niche partitioning among predators, the authors showed that ships amongst growers within a local area could lead to spatial complementarity could explain the biodiversity-biological successful integration. control relationship. Crop rotations and coupling crop and livestock production are An advantage of these approaches is that they might reveal how just two of many potential options for growers to potentially con- diversity effects naturally vary across ecosystems, with species serve biodiversity and promote ecosystem services like biological complementing one another only in certain situations. The draw- control. To truly promote sustainability in our agroecosystems, it back is that they require quite a detailed understanding of species will be essential for managers to consider multiple aspects of com- traits, so complementarity can be directly manipulated. Despite munities such as richness, evenness, abundance, and species iden- this challenge, more studies in this vein would help uncover mech- tity to maximize potential benefits for farming systems. While this anisms driving the relationship between biodiversity and biologi- is a daunting challenge, it is one we must overcome for agriculture cal control. to continue to meet the demands of a growing human population in an ever-changing world. 7. Managing for biodiversity and biological control Acknowledgments Overall, agricultural managers face an uncertain future of more extreme and changing climatic conditions, depleting water supply, We thank W.E. Snyder for useful discussions that helped the and increased costs of fossil fuels. In this review we show that manuscript. This project was supported by a USDA AFRI Fellowship diversification of agroecosystems generally decreases impacts on Grant (WNW-2010-05123) to DC. natural resources, promotes more diverse natural enemy commu- nities, and strengthens biological control. 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