biodiversity and pest control services - ucsc directory of

Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use.

This article was originally published in the Encyclopedia of Biodiversity, second edition, the copy attached is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-commercial research

and educational use. This includes without limitation use in instruction at your institution, distribution to specific colleagues, and providing a copy to your institution’s administrator.

All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited.

For exceptions, permission may be sought for such use through Elsevier’s permissions site at:

http://www.elsevier.com/locate/permissionusematerial

Philpott Stacy M. (2013) Biodiversity and Pest Control Services. In: Levin S.A. (ed.) Encyclopedia of Biodiversity, second edition, Volume 1, pp. 373-385. Waltham, MA: Academic Press.

© 2013 Elsevier Inc. All rights reserved.

Author's personal copy

En

Biodiversity and Pest Control ServicesStacy M Philpott, University of Toledo, Toledo, OH, USA

r 2013 Elsevier Inc. All rights reserved.

GlossaryAgricultural intensification A process of change in crop

and noncrop vegetation and management practices on

farms. Changes in vegetation include reducing the numbers

of crop species and varieties, and limiting trees, trap crops,

and weeds. Other local changes in management include

increasing the application of chemical pesticides and

fertilizers, increased tillage and irrigation, and heavier

mechanization. At the landscape level, intensification

includes converting natural habitat to crop fields,

destroying edge habitats, simplifying landscapes, avoiding

fallows, and fragmenting natural habitat.

Agrobiodiversity Typically refers to the level of species

diversity (with some research in this context on genetic

diversity or diversity among communities and ecosystems).

cyclopedia of Biodiversity, Volume 1 http://dx.doi.org/10.1016/B978-0-12-3847

At the species level, agrobiodiversity refers to species

richness, species evenness, and community composition (or

varietal richness, evenness, and composition) of both

planned and unplanned vegetation, and all other organisms

on a farm and in farming landscapes.

Biological control The use of naturally occurring or

introduced natural enemies (e.g., predators and parasitoids)

to suppress the populations of, and damage caused

by, pests.

Complementarity Resource partitioning among

consumer species that results in utilization of a greater

extent of available resources.

Intraguild predation Species interaction where predators

feed on herbivores as well as other predators, and where

trophic levels are not well defined.

Introduction

A major focus of agricultural research is investigating the re-

lationship between biodiversity and pest control. As natural

systems are converted to agriculture, provisioning of some

vital ecosystem services can decline (Kremen et al., 2004).

Ecosystem services, such as pest control, are ecosystem pro-

cesses that improve and sustain human life (Daily, 1997). In

agricultural systems, pest control problems may be exacer-

bated by biodiversity loss. Pests, defined as noxious weeds,

insects, mites, and fungi, cause economic damage to crop

plants (Hill, 1987). Many different forms of pest control are

used, including cultural control, mechanical control, chemical

control, and biological control. Biological pest control in-

volves attempts to use natural enemies (e.g., predators and

parasitoids) to suppress the populations of, and damage

caused by, pests. Biological pest control has been used for

centuries. Early records from ancient China (near 300 AD)

indicate that farmers used ants as natural enemies in orange

groves to control mite populations (Huang and Yang, 1987).

Classical biological control has focused on introduction of

species into agricultural areas in order to reduce pests to below

economic damage levels. By the 1980s, 160 species of preda-

tory arthropods and 16 insectivorous birds had been released

for pest control in the USA (Letourneau et al., 2009). To date,

more than 2000 species have been released worldwide (van

Lenteren et al., 2006).

With agricultural intensification, use of biological methods

of pest control has declined, being replaced with chemical

control and the use of genetically modified organisms to

combat pests (Benbrook, 2001). But such changes incur

environmental costs and exacerbate biodiversity losses in

agricultural landscapes (Bengtsson et al., 2005; Relyea, 2005).

Pesticides can cause reproductive problems for agricultural and

off-farm biodiversity, and contaminate waterways significantly.

Secondary pest outbreaks, and nontarget mortality of natural

enemies, often lead to increasing pesticide use, and continuing

dependence on pesticides to combat ever-increasing pest loads

(e.g., pesticide treadmill) (Van den Bosch, 1989).

Although ecological researchers have long maintained an

interest in understanding relationships between diversity and

trophic interactions, there is renewed interest in understand-

ing natural processes of pest control in agroecosystems, due to

growth of organic and ecological agriculture. Using biological

control of pests necessitates understanding relationships be-

tween agricultural management, pest and natural enemy

communities, and agricultural landscapes. Thus biodiversity

impacts on pest control can be evaluated at a number of levels

of biological organization (e.g., genetic diversity within a

species, species diversity within a taxon, functional diversity

within trophic level, and interactions within complex food

webs) and at distinct spatial scales (e.g., farm plot, habitat,

landscape, and region) (Letourneau and Bothwell, 2008)

(Figure 1).

At the level of biological communities, agroecological re-

search examines how two components of agrobiodiversity

affect pest control. Planned biodiversity includes crop plants,

other vegetation, and livestock chosen by the farmer to be in

the agroecosystem. Associated biodiversity includes all other

organisms that occur and survive in an agroecosystem de-

pending on the management style chosen by the farmer and

the surrounding landscape (Vandermeer and Perfecto, 1995).

Thus researchers have focused on understanding how changes

in agroecosystem management and agricultural landscapes

directly affect natural enemies and pests, and specifically have

examined the mechanisms underlying relationships between

biodiversity of natural enemies, pests, and plants, and pest

control services.

The study explores how biodiversity, both within farms

and across landscapes, affects pest control. It focuses on how

19-5.00344-0 373

Crop diversity (varieties,cultivars and species)

Landscape diversityand proximity tononcrop habitats

Species interactionsamong naturalenemy species

Pest control services

Natural enemy speciesfunctional diversity

Natural enemy speciesdiversity and identity

Pest diversityand identity

Noncrop plantdiversity

Figure 1 Major influences of biodiversity (at several levels of biological organization and distinct spatial scales) on pest control. Each of thelevels of diversity influence pest control in several ways and interact resulting in complex multitrophic interactions.

374 Biodiversity and Pest Control Services


changes in crop and noncrop plant diversity, natural enemy

diversity, and changes in diversity at multiple trophic levels

result in complex effects on pest control. It then shifts

to patterns beyond the farm by examining how landscape

diversity including maintaining noncrop vegetation nearby

to farm fields, proximity to natural habitats, and habitat

heterogeneity affect pest control. Finally, the study discusses

conservation biological control and provides some conclu-

sions. Although pests occur in a variety of ecosystems, from

a wide array of taxonomic groups, it focuses on insect pests

in terrestrial agricultural systems, and includes examples

from other systems and pests where relevant to inform the

discussion.

Agricultural Intensification and Impacts onBiodiversity

Creation and intensification of agriculture result in bio-

diversity loss with important implications for pest control.

Destruction of habitat, conversion to agriculture, and simpli-

fication of landscape structure are the principal causes for

biodiversity declines (Harrison and Bruna, 1999; Bianchi

et al., 2006). Furthermore, agricultural habitats are created at

an ever-accelerating rate (Bawa et al., 2004), and agricultural

intensification results in dramatic biodiversity losses (Letour-

neau and Bothwell, 2008). Although natural ecosystems have

largely intact food webs, with naturally occurring processes

that maintain pest populations at certain levels, natural con-

trol is lost with agricultural intensification (Swift and Ander-

son, 1993). Agricultural intensification refers to two general

processes: (1) changes in the vegetation diversity in an

agroecosystem (including crop species and varieties and other

vegetation components such as trees, trap crops, and weeds)

and (2) changes in management practices and intensity of

production including soil amending, chemical use, tillage, and

irrigation, among others (Altieri, 1999). Agricultural intensi-

fication includes modifications at the local (e.g., shortening

crop rotation cycles, decreasing crop diversity, increasing in-

puts, implementation of genetically modified crops, increased

tillage, increasing field size, and increased mechanization) and

landscape scales (e.g., converting natural habitat to fields,

destroying edge habitats, simplifying landscapes, avoiding

fallows, and fragmenting natural habitat) (Tscharntke et al.,

2005). Intensified, or modern, agriculture is highly simplified

and includes low diversity of plant species and crop varieties

(e.g., about 70 species are planted in 1440 million ha) (Altieri,

1999). The impacts of intensive agricultural production on

biodiversity and ecosystem services are a major research focus.

Intensification affects biodiversity generally, but natural

enemies, especially predator species, tend to be more strongly

affected by habitat disturbance and loss leading to shifts in the

ratios of prey to predator species, and subsequent effects for

ecosystem processes (Bruno and Cardinale, 2008). A recent

meta-analysis, covering 66 studies, found that both the species

richness and abundance of predatory insects (as well as birds

and spiders) was significantly higher in organic compared

with conventional (or modern, intensive) farms, whereas the

abundance of pest species and nonpredatory insects was

higher in conventional farms (Bengtsson et al., 2005). Specific

groups of predators, such as carabids, are more abundant,

diverse, and more evenly distributed in organic compared with

conventional farms (Kromp, 1999). Frequently, organic agri-

culture benefits species richness and abundance of plants,

predatory arthropods, and nonpredatory arthropods (Hole

et al., 2005; Letourneau and Bothwell, 2008). Other low-

intensity agroecosystems, such as shaded tropical agroforests,

harbor a high richness of predator species (e.g., ants and

birds) (Perfecto et al., 1996; Philpott et al., 2008). Similarly,

shade tree diversity within cacao agroforests positively impacts

parasitoid wasp richness (Sperber et al., 2004). The charac-

teristics of organic farms likely to increase biodiversity of

MAC_ALT_TEXT Figure 1

Biodiversity and Pest Control Services 375


natural enemies include agrochemical elimination, crop

rotation, maintaining areas of seminatural vegetation, and

preservation of mixed, or species-rich, farming (Hole et al.,

2005; Macfadyen et al., 2009). In agroforests, increases in

canopy diversity, density, and structural complexity correlate

with increased predator diversity (Philpott et al., 2008). Thus,

less-intensive agricultural systems, such as organic and eco-

logical farms, that include a high plant and natural enemy

diversity, noncrop habitats, and landscape heterogeneity may

support higher biodiversity, promoting pest control services.

Despite the large number of studies that demonstrate higher

abundance of natural enemies in organic farms, relatively few

have examined differences in pest control, or cascading effects

on crop yields (Letourneau and Bothwell, 2008). These and

studies comparing pest control in diverse versus species poor

farms, farms in simple versus complex landscapes, and the

effects of releases of single versus multiple biological control

agents are more common, and essential for understanding

how pest control is affected by biodiversity.

Vegetation Diversity and Pest Control

The number of crop plants and varieties, weeds, planned weed

strips, shade trees, and the temporal and spatial organization

of plant species all affect pest populations and natural enemy

assemblages. Andow (1991) reviewed the impacts of vege-

tation diversity on arthropod populations to test the resource

concentration and natural enemies hypotheses proposed by

Root (1973). The natural enemies hypothesis states that in

polycultures (fields with multiple crop species), natural enemy

abundance and diversity are higher due to more continuous

food availability compared with monocultures (fields with a

single crop species) (Root, 1973). The resource concentration

hypothesis states that in monocultures, specialized herbivores

have a more concentrated and unlimited food supply, thus

supporting higher populations (Root, 1973). Thus, herbivore,

or pest loads are affected by vegetation diversity in two major

ways, with a number of possible mechanisms explaining each.

Andow (1991) found that across 209 studies (and 287

herbivore species) reviewed, 51.9% of herbivore populations

were denser in polycultures and 15.3% had higher population

densities in polycultures. However, more herbivore species

were found in polycultures than in monocultures. Across all

studies, evidence indicated that both resource concentration

and natural enemy increases suppress herbivores.

Crop Diversity

Increasing crop diversity can be accomplished across both

space and time and can affect pest control via several mech-

anisms. Crop diversity can be altered by increasing the num-

ber of cultivars or varieties of a single species (e.g., increasing

genetic diversity), increasing the species diversity of crops,

adding crop rotations, and by increasing the architectural di-

versity of the crops. For several decades, scientists predicted

that pest outbreaks should be more frequent in monocultures

than in polycultures because crops associated with tax-

onomically diverse plantings will be less frequently attacked

than those associated with simple mixtures (Elton, 1958;

Root, 1973). Andow (1991) reviewed several hypotheses of

how crop diversity may reduce herbivore loads and increase

natural enemies. Herbivores, especially specialists, he wrote,

should be less common in polycultures because they have

problems locating host plants, because host-location cues may

be interrupted by the mix of plant species, and plant quality is

more variable. Parasitoids and predators should better deter

pests in polycultures because they can switch prey when cer-

tain species become rare, natural enemy reproduction takes

place more often in polycultures, and there are alternative

hosts in polycultures. Natural enemy populations are further

benefited in polycultures because therein exist prey refuges

that allow prey populations to survive, stabilize the popu-

lation fluctuations between prey and predators, and thereby

make continual prey suppression possible. Several studies

show empirical support for these hypotheses.

Increasing crop diversity has variable impacts on herbivore

populations. Increasing genetic diversity can protect crops

from pests, including crop diseases. Increasing the crop species

can limit the dispersal of disease spores, and at the same time

increase crop yields (Altieri, 2004). For example, in a study in

China, increasing rice varieties planted across a large area

decreased attack by rice blast (by 94%) and increased yields

(by 89%) compared with single-variety monocultures (Zhu

et al., 2000). Although examples with diseases are somewhat

more common, increased genetic diversity can also hinder

insect pests. Increasing the diversity of willows in a field de-

creases the population density, oviposition rate, and plant

damage caused by herbivorous beetles (Peacock and Herrick,

2000). Large-scale increases in corn acreage for biofuel pro-

duction (19% increase between 2006 and 2007 in the USA)

have negatively impacted pest control, yet increasing varieties

of corn planted may promote pest control (Landis et al.,

2008).

Intercropping, or the cultivation of two or more crops such

that they interact biologically, can reduce pest populations by

decreasing resources available, specifically to specialist herbi-

vores. Intercrops can be mixed or in neighboring rows or

strips, where crops are grown in the same field, or relay crops

where crops are grown one after the other (Vandermeer,

1992). Myriad examples empirically demonstrate that pests

are less abundant in intercrops due to mechanisms associated

with the resource concentration hypothesis (Vandermeer,

1992); however, intercropping may increase resources avail-

able to generalist herbivores (Schellhorn and Sork, 1997;

Zehnder et al., 2007). Timing of planting and fallow lands (a

temporary lack of crop diversity) can be very important in

regulating pests as is discontinuity in monocultures (Altieri,

1999). Providing some permanent vegetation helps maintain

populations of natural enemies (Altieri, 1999). Temporal in-

creases in crop diversity from using crop rotations can di-

minish pest problems. Rotations, or successional changes in

crop species planted in a single field, can minimize weed and

disease problems and can lower insect pest populations

(McLaughlin and Mineau, 1995, and references therein).

Increasing crop diversity can also lead to increased archi-

tectural diversity, or from a pest’s-eye view, habitat complexity.

Habitat complexity can strongly affect both the abundance

and diversity of natural enemies and their ability to capture



prey items (pests). Langellotto and Denno (2004) examined

the impacts within plant and within habitat complexity on

natural enemy communities. They found that in seven of

nine natural enemy guilds, and for natural enemies overall,

increasing habitat complexity increased abundance, and

decreasing habitat complexity lowered abundance. They also

reported possible mechanisms for these observations and did

not find that increased prey abundance mediated observed

increases in natural enemy abundance. Instead, refuge from

other predators, additional provided resources (e.g., alter-

native prey, nectar, and pollen), and more effective prey cap-

ture appeared to play important roles. In contrast, habitat

complexity may hinder pest control if parasitoid host-location

cues are interrupted, or if parasitoid search efficiency is

reduced (Andow, 1991).

Figure 2 A strawberry field in Watsonville, California, with sweetalyssum (Brassicaceae) featured prominently in the foreground. Thisplant species attracts beneficial insects (i.e., lacewings, syrphid flies)to the strawberry fields where they feed on pests and benefit thecrop plant.

Other Vegetation in Crop Fields

Allowing noncrop plants to grow within crop fields can also

increase natural enemy activity and decrease pest pressure.

Diversity and abundance of weeds, and trap crops, in agri-

cultural systems may also decrease pest densities because

weeds may provide alternative resources for or otherwise

harbor populations of natural enemies (Altieri, 1999). Espe-

cially in orchards and agroforests, natural enemy diversity may

be higher, and pest populations lower, where weeds or other

understory plants are maintained (Altieri, 1999). Adding strips

of weedy plants into crops (including vineyards) can increase

pest control services (Berndt et al., 2002; Jacometti et al.,

2007). Weed strips, especially of perennial plants, can also

provide habitat for natural enemies, and early sources of

predators in to crop fields. The so-called ‘‘beetle banks’’ or

strips of tussock grasses, for instance, are used throughout

Europe to provide overwintering spots for predators of crop

pests (Gurr et al., 2003, and references therein). The location

of such strips (often in the center of fields) can further

enhance the degree to which pests are suppressed in the crops

themselves.

Trap crops, additional plant species planted usually as

decoys for pests, increase plant diversity in fields, can lower

pest populations in crops, and often harbor natural enemy

populations (Figure 2). Trap crops are used in a number

of crops. In cotton fields in Australia, alfalfa strips are used

to both attract cotton pests (e.g., Creontiades dilutus) and to

provide habitat for natural enemies. When the alfalfa is

mowed, natural enemies will move into cotton crops, thus this

technique can be used to enhance biological control when

needed (Gurr et al., 2003). In citrus groves in China, an aster

(Ageratum conyzoides) is commonly planted to encourage and

stabilize populations of natural enemies of herbivorous mites

(Panonychus citri) (Liang and Huang, 1994). However, in-

creasing floral resources in agricultural systems may also

benefit herbivores by increasing herbivore fitness or masking

necessary host-location odors for the parasitoids (Lavandero

et al., 2006). In fact, some plant species used to increase

parasitoid populations may simultaneously benefit herbi-

vores, thus selection of the plant species used to enhance

diversity and resources for natural enemies must be done

with care (Lavandero et al., 2006). Finally, alley cropping, or

planting rows of woody plants in crop fields, can also reduce

pest pressure. In a number of countries, legume trees are

planted alongside maize crops which depending on the con-

text can increase soil quality, reduce pest pressure, and increase

natural enemy populations, or can increase seed predation on

the crop, and increase root competition (Schroth et al., 2000).

Natural Enemy Diversity and Pest Control

Ample research has examined the relationships between

predator diversity and pest control (e.g., Pimentel, 1961; Root,

1973; Andow, 1991; Gliessman, 1989) and the complex

interactions that arise between predator diversity and prey

(Ives et al., 2005, and references therein). Further, there is a

long history of debate among experts in biological control,

and conflicting evidence as to whether single or multiple

species introductions of pest control agents are better for

controlling pests (e.g., Cardinale et al., 2003; Bianchi et al.,

2006). Increases in predator diversity do not always result in

increased pest control over single-species treatments (Finke

and Denno, 2004) and many biological control strategies

prove successful with the introduction of just a few natural

enemy species (Myers et al., 1989; Denoth et al., 2002). In fact,

biological control strategies employed with multiple species

can actually hinder biological control efforts (Denoth et al.,

2002). Yet, several empirical studies show that presence of

multiple predators can enhance prey risk for important crop

pests (Losey and Denno, 1998; Cardinale et al., 2003; Schmidt

et al., 2003; Snyder and Ives, 2003). The variation in results,

however, begs the question as to which mechanisms result in

different outcomes in multipredator experiments.

There are several different mechanisms that could poten-

tially contribute to both risk enhancement for prey (better pest

control) and risk reduction (worse pest control). Both risk

reduction and risk enhancement for pests can result in non-

additive effects – effects that do not add up to the sum of their




parts (Sih et al., 1998; Denoth et al., 2002; Bruno and Cardi-

nale, 2008). Risk enhancement can result from the sampling

effect, facilitation, species complementarity, and increased

abundance of predators. Risk reduction can result from an-

tagonistic effects such as aggression, cannibalism, and intra-

guild predation (IGP). Results from simulation models show

that the sampling effect and complementarity among species

tend to more strongly affect prey suppression than other

mechanisms (Ives et al., 2005). While different mechanisms

may show prominence in certain studies or certain agroeco-

systems, it is likely that a variety of mechanisms operate

simultaneously (Cardinale et al., 2003). Each of these mech-

anisms and resulting effects is discussed in the following

sections.

Mechanisms of Predator Diversity Effects

Sampling and Selection EffectsThe sampling effect, also called the selection effect, selection

probability, or lottery model, indicates that as richness in-

creases, the chances of finding a species with strong or unique

effects on lower trophic levels also increases (Huston, 1997;

Ives et al., 2005). Thus, in a community with higher bio-

diversity, it is more probable that one or two species respon-

sible for large effects will be present. Sampling effects may

occur where certain species have disproportionately large ef-

fects in a community, or where a single species has relatively

greater abundance, prey capture ability, longevity, reproductive

capacity, or competitive ability (Letourneau et al., 2009). In

biological control efforts, the sampling effect may be evident

with releases of specialist species. In a review of natural enemy

introductions to control agricultural pests, Denoth et al.

(2002) found that in more than 50% of the successful intro-

ductions of multiple enemy species a single species was ac-

tually responsible for the successful control. They attribute this

to the sampling effect whereby adding additional species in-

creased the chance of having a useful one. Of course, sampling

effects that result in introduction of a damaging or disruptive

natural enemy could diminish pest control (Letourneau et al.,

2009).

Predator abundance usually increases as predator diversity

increases, making it difficult to distinguish between the effects

of abundance and richness, especially in field-based studies.

Where correlations between natural enemy richness and pest

control are encountered, increased pest control could result

from simple increases in natural enemy abundance (Van Bael

et al., 2008). In the lab, experimental treatments can be set up

to distinguish the two. With replacement designs, diversity is

manipulated, but density or biomass of natural enemies is

held constant. In additive designs, diversity is manipulated

while initial density or biomass of natural enemies is held

constant. Replacement designs are generally more useful for

disentangling mechanisms of biodiversity and ecosystem

function relationships, and specifically species–specific effects,

whereas additive designs are more appropriate tests of

complementarity or nonadditive effects (Ives et al., 2005). In

addition, additive designs more likely represent what is hap-

pening in agricultural fields with enhanced vegetation,

predator refuges, and other complex structural components.

FacilitationFacilitation occurs when two or more different species of

natural enemies enhance the effect of another. There are many

examples of predator facilitation in the literature that result

in increased pest control. For example, predators that forage

on vegetation (e.g., coccinellid beetles) will often scare pests

(e.g., aphids) who then fall to the ground and are preyed on

by ground-foraging carabid beetles (Losey and Denno, 1998).

Thus the coccinellid assists the carabids to locate prey by

chasing away aphids. Clearly, however, for such facilitation to

occur and result in synergistic effects, in particular, the two

predator species must forage in the same part of the season, at

the same time of day, and not interfere with the prey capture

rates of the other species (Losey and Denno, 1999).

ComplementarityComplementarity is based on the principle that as consumer

species utilize different resources, thereby partitioning them, a

greater extent of the available resources will be consumed

(Loreau et al., 2001). If a diverse suite of natural enemies

partition resources, or are complementary, this may thus in-

crease pest control. The effects of natural enemies that feed on

different prey species, different life stages of a single prey

species, or that forage or feed in different microhabitats of

agroecosystems, or at the different times of day or seasons may

combine in a complementary fashion (e.g., Bruno and Car-

dinale, 2008; Letourneau et al., 2009). Complementarity often

leads to increases in prey risk enhancement but may depend

on the degree to which different natural enemies actually

partition resources (Bruno and Cardinale, 2008). Although

theory predicts that organisms partition resources, little em-

pirical data support that complementarity increases pest sup-

pression. This may be due to difficulty of assessing natural

enemy diets and host preferences or because many studies are

conducted in homogeneous agricultural fields without much

option for partitioning (Ives et al., 2005; Bruno and Cardinale,

2008).

Nonetheless, some studies show that species comple-

mentarity in diverse natural enemy assemblages increases pest

control. Bogran et al. (2002) found that three species of

parasitoids attacking a whitefly pest in cotton preferentially

attacked larvae of different sizes and in spatially distinct areas

of the cotton plants, thus leading to higher parasitism rates

where all three species co-occurred. Finke and Snyder (2008)

used an experimental test to separate the effects of species

richness and resource partitioning and found evidence to

support the latter. They released different mixes of specialist

parasitoids (reared on one species of aphid hosts to which

they show host ‘‘loyalty’’) and generalist parasitoids (reared on

three aphid species) into large field cages with mixes of the

aphids. They found that increasing the diversity of specialist

parasitoids resulted in higher parasitism rates and lower aphid

populations; however, increasing the richness of generalist

species did not. Thus they empirically demonstrated the im-

portance of resource partitioning as a mechanism driving

biodiversity effects. Neumann and Shields (2008) found that

releasing a combination of nematodes with complimentary

foraging strategies (e.g., an ambush and a cruiser nematode)

significantly reduced alfalfa insect damage compared with

controls and one single–species treatment; however, not all

Figure 3 Azteca instabilis ants attacking a lepidopteran larva in acoffee agroecosystem. Ants are often effective predators; however,they can interfere with the activities of other natural enemies such asparasitoids, spiders, and coccinellid beetles resulting, at times, in riskreduction for prey when in diverse assemblages. Photo by D.Gonthier.



combinations of nematodes provided effective control. Finally,

Williams-Guillen et al. (2008) compared the single- and

multitaxon impacts of birds and bats on arthropod removal

in coffee agroforests and found that each predator taxon

provided higher pest control services during different seasons

(birds during winter when migratory birds form a large frac-

tion of the community). Further, likely because of the tem-

poral separation in foraging times, birds and bats acting

together had the greatest negative effect on arthropod loads.

Functional DiversityAlthough species richness has been most often used as a

metric of diversity, functional group richness has been invoked

as a better predictor of ecosystem service as traits of organisms

more strongly relate to functions than do taxonomic classifi-

cations (Tilman et al., 1997; Diaz and Cabido, 2001). A

functional group is a grouping of species based on similarity

in behavioral, morphological, physiological, or resource use

traits (Petchy and Gaston, 2006; Philpott et al., 2009). Func-

tional diversity of natural enemy characteristics, then, might

be more important to consider than the taxonomic richness of

predators itself, as this relates more strongly to ecosystem

function (Hooper et al., 2005).

Functional diversity, especially of important predators, may

be more strongly affected by agricultural intensification than

species richness. For example, Flynn et al. (2009) found that

bird functional diversity declined with agricultural intensifi-

cation more quickly than did species richness. Further,

Schweiger et al. (2007) found that declines in specialist para-

sitoids were stronger than generalist parasitoids with habitat

degradation. This may be especially important if species

complementarity is an important mechanism maintaining

positive effects of predator diversity on pest control. Philpott

et al. (2009) examined patterns behind significant positive

relationships between richness of insectivorous birds and

arthropod removal in tropical agroforestry systems. They div-

ided birds into functional groups based on characteristics re-

lated to predatory function (e.g., body size, diet, foraging

strategy, and strata) and then correlated changes in functional

richness with both species richness and pest control function.

Species richness and functional richness were highly correlated

across the nine study sites examined, and functional richness

correlated significantly with arthropod removal. However,

simple species richness remained a better predictor of eco-

system function than functional richness either because the

traits included were not sufficient to explain all variation, or

because presence of important predator species played a more

important role.

Functional Redundancy and the Insurance HypothesisFunctional redundancy may result in increased pest control

under the insurance hypothesis. Functional redundancy, or a

lack of complementarity among co-occurring species, indicates

that natural enemies share traits such as similar foraging

modes, diets, and strategies, and thus can be placed in the

same functional group. Removing functionally redundant

species from a community in theory has no effect on the

ecosystem, whereas adding functionally redundant species can

increase interspecific competition but does not affect pest

control function (Straub et al., 2008, and references therein).

However, agricultural systems are constantly disturbed, and

even functionally equivalent species may respond differently

to environmental changes (Perfecto et al., 2004). Thus, the

importance of maintaining functionally redundant species can

be supported under the insurance hypothesis.

The insurance hypothesis suggests generally that functional

redundancy is important for maintaining ecosystem services

should conditions change (Yachi and Loreau, 1999). In the

context of pest control, this means that as crops are harvested,

fields are tilled, or as weed strips are mowed, the resulting

changes to natural enemy effectiveness will be buffered by the

presence of functionally redundant species within the agro-

ecosystem. Functional redundancy has been inferred from

studies finding no effect of increased predator diversity on pest

control. In some cases, spider species richness does not affect

predation (Sokol-Hessner and Schmitz, 2002) and the diversity

of aphid-feeding natural enemies does not increase predation

(Chang, 1996). But, functional redundancy is difficult to show

unequivocally because neutral effects of predator species may

result from a combination of other effects (Straub et al., 2008).

Intraguild InterferenceIntraguild interference refers to negative interactions between

natural enemy species including predation, cannibalism,

predator avoidance behavior, and predator–predator com-

petition (Figure 3) (Lang, 2003). Among phytophagous in-

sects released as biological control agents there is a very high

degree of competitive interactions. Denno et al. (1995) found

that in 91% of releases (45 studies), biological control agents

competed with each other. If such interactions are sufficiently

antagonistic, this may result in herbivore release and potential

pest outbreaks, but depends on the nature of the interactions




involved (Rosenheim et al., 1999; Snyder and Wise, 2001;

Perez-Lachaud et al., 2004; Ives et al., 2005). IGP occurs where

trophic levels are not clearly defined, and predator species feed

on herbivores as well as other predators (Polis et al., 1989;

Rosenheim et al., 1995, Ives et al., 2005).

Interspecific interactions result in both enhanced and

reduced prey risk. Herbivore suppression may decline due to

IGP (Rosenheim et al., 1995; Snyder and Wise, 2001; Finke

and Denno, 2005). Finke and Denno (2005) examined the

effects of several spider species, a coccinellid, and a mirid bug

on prey in salt marshes and found that increasing spider

richness reduced prey suppression due to both IGP and non-

lethal effects of some spider species on others. However, the

effects of IGP by spiders changed with habitat complexity; in

complex habitats where mirids find refuges to escape spider

predation, effects on herbivores were greater than in simple

habitats where the combination of predator species resulted in

risk reduction for prey (Finke and Denno, 2002). Ant foraging

interrupts spiders, resulting in lower predation rates (probably

due to both IGP and direct interference) (Halaj et al., 1997).

Pell et al. (2008) report that the exotic coccinellid predator

Harmonia axyridis interferes with other predators via canni-

balism, interfering with oviposition of parasitoids, and by

feeding on parasitized pest eggs (coincidental IGP). IGP by

the ladybeetle does not diminish with increased prey and

contributes to its success as an exotic invasive species in agri-

cultural landscapes (Snyder et al., 2004). In contrast, IGP

sometimes results in risk enhancement for prey. Lang (2003)

investigated the interactions between carabid beetles and spi-

ders (lycosids and lyniphiids) in winter wheat. Carabid beetles

negatively affected lycosid abundance, likely due to IGP, or by

altering emigration rate of spiders out of carabid-free cages. In

contrast, linyphiid abundance was not affected by the presence

of carabids. Overall, predators did not negatively affect para-

sitism rates on aphids, and the overall impacts of predators,

despite evidence of IGP, were synergistic resulting in higher

predation rates where predator diversity was higher.

The strength of intraguild interactions in determining pest

control outcomes is highly context dependent; effects vary

with habitat complexity, prey density, type of IGP, and size and

mobility of the intraguild predator and prey species (Muller

and Brodeur, 2002; Pell et al., 2008). Intraguild interactions

most likely occur when natural enemies have similar hunting

modes and foraging locations (Schmitz, 2007). Strength

of intraguild effects also depends on plant architecture. In

recently cut alfalfa fields, carabids are effective and quick

predators on aphids, and also reduce predation rates leaving a

longer term positive impact on pests (Snyder and Ives, 2001).

Where plants are taller, carabids were no longer effective

predators and still reduced parasitism thus having only

negative impacts on biological control.

Finally, effects of IGP may be stronger for omnivorous

rather than coincidental IGP. Coincidental IGP occurs where

predators eat parasitized hosts, whereas omnivorous IGP

occurs where predators consume other predators. Because

coincidental IGP is coupled with direct predation on pests

(e.g., intraguild predators eat prey and parasitoids simul-

taneously), omnivorous IGP most strongly interferes with pest

suppression (Straub et al., 2008). In biological control strat-

egies, coincidental IGP actually can increase pest suppression

(Rosenheim and Harmon, 2006). Thus, in sum, even where

IGP occurs, a diverse assemblage of predators may still pro-

mote better pest control than a species-poor assemblage

without interspecific effects (Letourneau et al., 2009).

Evidence that Predator Diversity Enhances Pest Control

Several compelling examples demonstrate that natural enemy

diversity can enhance pest control, many from controlled

lab and cage studies in temperate agricultural studies that are

discussed above (see Facilitation and Complementarity). In

addition, Cardinale et al., 2003 investigated the effects of a

coccinellid, a parasitic wasp, and the damselbug on pea aphids

on alfalfa in large field exclosures and found increased pest

control (and increased yields) when all three species were

together. However, establishment rate of natural enemy spe-

cies (for insect pests but not for weed pests) can be signifi-

cantly lowered when multiple species of agents are released

(Denoth et al., 2002). This could be due to competitive ex-

clusion, to bias in the data set, or due to the fact that managers

often continue releasing agents in sequence until one is suc-

cessfully established (Denoth et al., 2002). Lower establish-

ment could also be due to intraspecific aggression, or to IGP

among agents released, or those already residing within the

target agricultural systems, as discussed above (see Intraguild

Interference).

Relatively little manipulation of predator diversity has been

conducted in tropical agricultural systems, but there are in-

creasing numbers of compelling examples from coffee and

cacao agroforests that both invertebrate and vertebrate natural

enemy diversity relates to increased pest control. Tylianakis

et al. (2008) examined a number of agricultural systems

(pasture, rice coffee, abandoned coffee, forest) and found that

parasitism of nectar and pollen-feeding wasps was higher

where parasitoid diversity was higher. Perfecto et al. (2004)

excluded birds from coffee plants in Mexico and found that

suppression of an artificial outbreak was greater in farms with

higher diversity and abundance of birds. They attributed the

increase in pest removal to increased abundance of a par-

ticular insectivore species in the more complex coffee habitat,

thereby providing field evidence for the sampling effect.

Borkhataria et al. (2006) found in shade coffee farms that

birds alone and the combination of birds and lizards signifi-

cantly reduced arthropod abundance (but not the abundance

of parasitoids or arthropod predators), and that coffee leaf-

miners responded weakly to predator removal. Further, the

combination of birds and lizards was an additive effect. They

concluded that vertebrate predator diversity is important in

controlling pests, and that in their system, vertebrate predators

do not disrupt arthropod natural enemies through IGP.

Several authors have conducted meta-analyses to review

how biodiversity affects herbivore or pest densities. The results

widely vary, perhaps due to the studies included, the criteria

for inclusion of studies, or the experimental method used.

Cardinale et al. (2006) reviewed studies to examine the effects

of consumer diversity on resource depletion. Of 111 experi-

ments, eight covered the effects of terrestrial predators on prey.

Overall, a diverse mix of predators (43 species) removed prey

better than a nondiverse mix, but prey suppression was not

greater for a diverse mix than for the single best predator



species thus supporting the sampling effect. Schmitz (2007)

examined studies specifically to evaluate support for different

mechanisms driving multipredator effects. He found that in

just under half of the studies examined (45.6%) that predator

diversity resulted in risk enhancement or additive effects of

predators, and in almost as many cases (40.3%), predator

diversity resulted in risk reduction. He found widespread

evidence for substitutable effects and for interspecific inter-

ference (including IGP) among natural enemy species; further,

risk enhancement with multiple predator species was more

likely in lab compared with field studies.

Finally, Letourneau et al. (2009) reviewed 62 studies,

yielding 266 comparisons of diverse versus nondiverse mix-

tures of natural enemies. They found that in 69.5% of

comparisons increased natural enemy diversity resulted in

increases in pest suppression; in 30% of cases, increased di-

versity resulted in decreases in pest suppression. They also

compared several study characteristics to determine how ef-

fects differed across system and location. In temperate areas,

pest suppression as a result of natural enemy diversity was

significant in agricultural systems, but not in natural systems,

and pest suppression occurred in both temperate and tropical

agricultural systems. Additionally, mean effect sizes (magni-

tude of pest suppression) were greater in cage compared with

field studies. Thus a great deal of empirical evidence indicates

that natural enemy diversity can enhance prey risk, but

diversity effects are far from consistent.

One major limitation of studies conducted to date is the

relatively low number of natural enemy species included in

high-diversity treatments. In most meta-analyses, reporting

the results of multipredator impacts on single prey species, the

mean diversity of predators and parasitoids included is

between three and four species (Borer et al., 2005; Letourneau

et al., 2009). However, this is a far cry from the actual diversity

of predators recorded, even in species-poor temperate agro-

ecosystems. Natural enemy species richness for single herbi-

vore species ranges from 13 to 86 species in several systems in

the USA and northern Mexico (Letourneau et al., 2009, and

references therein). Further, when full prey–natural enemy

communities are reported, numbers increase even more dra-

matically. More than 220 species of birds reportedly feed on

agricultural pests in the USA (Letourneau et al., 2009), and

hundreds of species of predators feed on insect pests in tro-

pical agricultural systems. Furthermore, the magnitude of di-

versity effects on pest suppression increases significantly with

predator richness (Letourneau et al., 2009), thus more studies

are needed that manipulate a greater number of species in

field or lab experiments, or new methods and models need be

developed to examine the impacts of multiple predator species

in highly species-rich communities.

Changes in Diversity at Multiple Trophic Levels

As agroecosystems are complex, so are the interactions therein,

and interactions between diversity at multiple trophic levels

may affect pest control. Differences in both plant diversity and

predator diversity have distinct effects on pest populations.

Yet, there may be complex interactions between diversity at

different trophic levels that influences pests. Although many

focus on diversity at the natural enemy trophic level, it is clear

from other work presented that plant diversity has strong

bottom-up effects in agricultural systems (Root, 1973; Andow,

1991). Moreover, multipredator effects are rarely placed within

the context of other interactions and most studies aimed at

testing multipredator effects examine only predator, prey, and

plant trophic levels. However, adding vertical diversity within

food webs (e.g., a fourth trophic level) may alter biodiversity

effects at lower trophic levels (Duffy et al., 2007). In the few

studies conducted to date, for example, addition of herbivore

species can both weaken and strengthen the relationship be-

tween biodiversity and ecosystem function (Duffy et al., 2007).

A few studies have examined whether the effects multiple

predator species have on herbivores and plants may be altered

by the presence of a larger predator species, or a parasite of

one or more predator species, and those that manipulate di-

versity at multiple levels are rare. Aquilino et al. (2005) ma-

nipulated predator diversity (from one to three species) and

plant diversity (from one to two species). They used three

plant species (alfalfa, clover, and fava beans) and three

predator species (two species of coccinellid and a damselbug).

They found that increasing predator diversity resulted in an

increase in predation on pea aphids (on both monocultures

and polycultures), but that increasing plant diversity decreased

predation rate by the same magnitude (in both single- and

multipredator treatments). Negative effects of IGP on a single

pest species may disappear in studies including alternate prey

species (Schmitz, 2007) indicating that even simple changes to

prey richness may affect the effects of predator diversity.

Finally, Macfayden et al. (2009) used a food web approach to

examine whether diversity changes at all trophic levels influ-

enced whether organic farms are more resistant to establish-

ment of novel pests. In comparing food web networks in

10 pairs of organic and conventional farms in England,

they found that organic farms had higher richness of plants,

herbivores, and parasitoid species. However, in farms with

more species, food web connectivity was lower, and parasitism

rates and numbers of parasitoid species attacking herbivores

did not differ in the diverse organic farms and the con-

ventional farms. Thus, in systems where complexity of an

entire food web was examined, increased predator diversity

did not necessarily result in increased pest control. Despite the

difficulty in manipulating the vast array of species in multiple

trophic levels, more complete investigation will be necessary

for fully understanding how differences in diversity at multiple

trophic levels affect pest control (Ives et al., 2005).

Agricultural Landscapes and Biodiversity

Agricultural landscapes represent a wide variety of habitats

including crops, noncrop vegetation patches, woodlands,

wetlands, grasslands, and forests. In such landscapes, the

presence of noncrop vegetation, the distance to natural areas,

and the complexity of the landscape can all affect pest control.

Noncrop Habitats

Hedgerows, live fences, and other linear habitats within agri-

cultural systems provide habitat for birds, bats, dung beetles,



and butterflies (Harvey et al., 2005) and specifically for several

groups of invertebrate natural enemies (Bianchi et al., 2006).

As agricultural habitats are constantly disturbed, hedgerows

and other crop margins provide stable resource bases for

natural enemies (Bianchi et al., 2006). The characteristics of

noncrop habitats that benefit natural enemies include pro-

viding alternate prey, nectar and pollen, nesting sites, and host

plants necessary for reproduction and life-cycle completion

(Landis et al., 2000; Bianchi et al., 2006), and are similar to

benefits provided by vegetation diversity within crop fields.

Hedgerows and field margins increase the movement of

predators across agricultural landscapes similarly to how a

high-quality matrix may increase movement of organisms

between forest fragments (Vandermeer and Carvajal, 2001;

Tscharntke et al., 2005). In some cases, increases in predator

diversity in hedgerows can increase pest control. For example,

linear vegetation strips in vineyards in California facilitate

movement of natural enemies in the grapes, and thereby in-

crease pest control (Benton et al., 2003). Field margins and

hedgerows can slow movement of fungal pathogens and can

serve as barriers to the movement of pests, thereby improving

pest control (Altieri, 1999). However, if the field margins

provide alternative habitat for beneficial insects and other

predators such that they forage more in the margins than in

the crop, or prefer the crop-margin habitats more than the

natural habitats, then this may harm pest control (Benton

et al., 2003; Bianchi et al., 2006).

Proximity to Natural Areas

Distance to natural areas such as woodlands and grasslands

can also affect pest control because natural enemies may find

refuge in nearby natural habitats. Species of higher trophic

levels, such as natural enemies, tend to be more strongly

(a) (b)

Figure 4 Two contrasting agricultural landscapes differing in habitat heter(a) contains a high diversity of both crops (banana, mango, coffee, and ricelandscape (b) near Toledo, Ohio, shows large corn and soybean monocultucontrol is more effective in high diversity landscapes.

negatively affected by isolation from natural habitats (Klein

et al., 2006, and references therein). These declines in richness

are likely due to more unstable populations of predator and

parasitoid species, increased energy requirements, and a lack

of food and nectar sources when far from natural habitats

(Klein et al., 2006). In agroforest landscapes in Indonesia,

both diversity of natural enemies and parasitism rates of trap-

nesting hymenopteran brood declined with distance from

forest, and for natural enemies, this landscape factor was a

more important predictor than light intensity or the number

of plant species in crop areas (Klein et al., 2006). Furthermore,

in coffee agroforests in Mexico, ant richness declines markedly

with distance from forest fragments, especially in less diverse

agroecosystems leading to less diversity of predatory species

further from forest fragments (Perfecto and Vandermeer, 2002;

Armbrecht and Perfecto, 2003). Predation rates may also de-

crease with increased distance from noncrop habitats at field

margins. Parasitism rate declines, likely because parasitoids

(and predators) are more susceptible to habitat fragmentation

than herbivores (Kruess and Tscharntke, 1994; Bianchi et al.,

2006). Thus landscapes with a greater diversity of habitats, and

especially with smaller habitat patches may be preferable for

increasing natural enemy function.

Habitat Heterogeneity

At the landscape level, habitat heterogeneity can strongly

benefit pest control services. Including a high degree of habitat

heterogeneity in agricultural landscapes (including many dif-

ferent types of crop fields, natural habitat areas, hedgerows,

fencerows, wetlands, etc.) can increase the diversity of natural

enemies in crop fields, and also can provide stability of

resources for maintaining natural enemy populations

(Figure 4) (Altieri, 1999). Habitat heterogeneity increases

ogeneity. The high heterogeneity landscape from Sumatra, Indonesia) and includes forest trees and weed patches. The low heterogeneity

res and a very small forest fragment. Most evidence indicates pest




with increased number of habitats, and generally with smaller

patch size; spatial arrangement of patches may also be im-

portant. In landscapes with small patches, natural enemies

may be better able to reach all areas of a crop field, and col-

onize early in the growing season. Heterogeneous landscapes

may support higher abundance and diversity of natural en-

emies simply due to the different preferences of different

species for different habitats (Bianchi et al., 2006). Boatman

(1994) demonstrated that carabid beetles move from field

margins approximately 15–30 m into field margins, and thus

the locations of field margins could be maximized to increase

the abundance of polyphagous predators. Furthermore, some

natural enemies can move only short distances into crop fields

from margins but the dispersal distances vary with species

examined (Nicholls et al., 2001; Bianchi et al., 2006). Thies

and Tscharntke (1999) studied the effects of habitat com-

plexity of noncrop habitats and their role on oilseed rape

crops. They found that presence of structurally complex non-

crop habitats related to lower parasitism of the pest than

presence of simple noncrop habitats nearby.

Even in intensive, extensive agricultural systems, landscape

diversity can be important in promoting biological control.

Marino and Landis (1996) explored parasitoid diversity and

attacks in cornfields in Michigan embedded in complex (small

plots with abundant hedgerows) and simple (large plots with

rare hedgerows) landscapes near and far from hedgerows.

They found that parasitoid richness was similar in both

habitats, and parasitism rates were five times higher in com-

plex than in simple landscapes, but that distance from

hedgerows did not affect parasitism in either landscape. In the

Midwest US, relative removal rates of aphid pests in soybean

fields were increased by landscape diversity (e.g., number

and evenness of different habitats) (Gardiner et al., 2009). In

addition, abundance of coccinellid beetles (the main predator

encountered in soy fields) was positively affected by the

amount of natural habitat in the surrounding area. Con-

versely, in these same landscapes, increases in area planted

with corn (largely for biofuel production) resulted in strong

decreases in biological control of soybean aphids due to de-

clines in habitat heterogeneity and specifically losses of area

formerly in fallow or conservation lands (Landis et al., 2008).

A few recent reviews have specifically targeted effects of

habitat heterogeneity at the landscape scale on pest control.

Bianchi et al. (2006) conducted a literature review to examine

the impacts of landscape complexity on natural enemy activity

in relation to pest pressure. They defined complex landscapes

as those with a high proportion of noncrop habitats (e.g.,

forests, hedgerows, tree lines, grasslands, wetlands, and fal-

lows) and with small patches (large perimeter to area ratios).

In 74% of the studies examined, pest control was enhanced in

complex landscapes. Further, pest pressure (defined as popu-

lation densities, crop injury, and survival and population

growth rate of aphids) was reduced in complex landscapes

in 45% of observations. They highlighted that landscapes

with herbaceous vegetation (80% of studies with enhanced

natural enemy activity), woody vegetation (71%), and land-

scape patchiness (70%) were those that most related to in-

creased natural enemy activity.

Studies since this time have documented that parasitism

rate increases with forest area (measured at multiple scales),

proximity to forest, and proximity to road edges (Bianchi

et al., 2008). But just as with relationships between natural

enemy diversity and pest control, the mechanisms underlying

relationships between landscape diversity and pest control

services need to be more specifically examined. Benton et al.

(2003) reported that a mosaic of farm fields connected by

noncrop habitat benefits birds, predatory ground beetles, and

spiders. Thus in sum, several aspects of agricultural land-

scapes, including noncrop habitat, and spatial structure of

the landscape affect pest control services provided by natural

enemies, and movement of natural enemies across agricultural

landscapes (Tscharntke et al., 2005).

Conservation Biological Control

Conservation biological control is a process by which man-

agers manipulate plants and other aspects of agricultural

landscapes in order to increase abundance and diversity

of natural enemies (Barbosa, 1998; Fiedler et al., 2008).

Normally, managers increase enemy populations by planting

nectar sources, floral resources, seed production, and plants

that support alternative prey, or shelter (Landis et al., 2000).

Out of 34 studies that have evaluated the impact of habitat

management (e.g., purposeful plant additions) to increase

natural enemies, most have focused on just four plant species,

all annual, and most not native to the study area (Fiedler et al.,

2008). One study did evaluate the effectiveness of several

native perennial plants in attracting natural enemies com-

pared with plants commonly examined in habitat manage-

ment trials (Fiedler et al., 2008, and references therein). Many

of the native plants screened attracted high numbers of natural

enemies, more so than the commonly used nonnative plants,

and in addition, these other plants may provide additional

ecosystem services (e.g., increasing pollinator abundance and

rural beauty) (Fiedler et al., 2008).

Because impacts of natural enemy richness on prey sup-

pression are variable and context dependent, making clear

recommendations to farmers is difficult. Understanding the

traits that increase pest suppression is key (Straub et al., 2008).

If, for example, the selection effect is operative in a particular

agroecosystem, one could recommend the important predator,

rather than planning to conserve natural enemy diversity

more broadly (Straub et al., 2008). Likewise, promoting the

conservation of functionally redundant species within a

community should not negatively impact function, and to the

contrary may improve pest control services if conditions

change (Yachi and Loreau, 1999; Straub et al., 2008). Further,

there are often nontarget impacts of introduced biological

control agents, and if many species need to be introduced,

there is even greater chance of impacts on nontarget species

(Denoth et al., 2002). Thus, considering pest control using

naturally occurring predators and parasitoids is important.

Conclusions

Several levels of biological and habitat diversity affect pest

control in complex manners. Vegetation diversity including

crop genetic diversity, crop species richness, and noncrop plants



in farm fields can increase the number and function of natural

enemies in crop fields. Predator diversity is a strongly context-

dependent predictor of pest control, sometimes resulting in

increased risk for pests where functional richness or comple-

mentarity is high, or where single species of effective predators

are found. Yet IGP and other interspecific interactions between

natural enemy species may result in risk reduction. At the

habitat level, vertical structure of crop plants, weeds, and

shade trees may promote population stability and diversity of

natural enemies. Landscape complexity, including incorpor-

ating hedgerows and other types of noncrop habitat, as well as

maintaining highly complex landscapes with a high amount of

natural habitat seem to best promote pest control services.

Pest control, however, as an important ecosystem service in

human-managed systems, should be examined in a larger

context. First, pest control has a long history, and has in

agroecological farms moved away from a pest elimination

mentality toward understanding complex ecological inter-

actions. For example, in traditional Guatemalan agroecosys-

tems, farmers have intricate knowledge of their agricultural

systems, and insects that feed on crops; however, they do not

consider them pests (Morales and Perfecto, 2001). Instead,

they consider the multitude of techniques used (e.g., inter-

cropping, natural composting, and allowing for survival of

beneficial insects) as a way to keep the insects from becoming

pests. Many traditional agricultural systems, which incorporate

traditional knowledge, and high levels of planned and asso-

ciated biodiversity have complex ecological webs that result in

high levels of natural pest suppression (Gliessman, 1989);

Vandermeer et al., 2010). Thus considering not only strategies

for eliminating pests, but also employing strategies to main-

tain complex food webs may be warranted.

Whatever pest control strategies are promoted should also

be considered in the context of farmers whose livelihoods

strongly depend on crop production. For example, Steffan-

Dewenter et al. (2007) examined a number of ecosystem ser-

vices provided in shaded and unshaded cacao agroforests in

Indonesia. They discovered that conversion of forest to cacao

systems negatively affected plant biomass and a range of

ecosystem services, but had little effect on species richness of

associated biodiversity, overall. Reducing shade cover in the

cacao farms, however, resulted in nonlinear changes in bio-

diversity, ecosystem services, cacao production, and income.

Reducing shade cover in cacao farms from 80% to 40% re-

sulted in higher levels of ecosystem services provided, and

marginal increases in income. Eliminating shade cover al-

together (to 0%) drastically lowered ecosystem function, but

boosted incomes by 40%, and thus provided obvious benefits

to farmers, at the cost of other ecosystem benefits. Thus any

strategy aimed at increasing pest control services, or conser-

vation biological control need consider not only the ecological

principles discussed here, but also the farmers’ livelihood.

Appendix

List of Courses

1. Agroecology

2. Biodiversity and Ecosystem Function

3. Ecosystem Services

4. Integrated Pest Management

5. Sustainable Agriculture

See also: Agrobiodiversity. Biodiversity and Ecosystem Services.Ecology of Agriculture

References

Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agriculture,Ecosystems & Environment 74: 19–31.

Altieri MA (2004) Linking ecologists and traditional farmers in the search forsustainable agriculture. Frontiers in Ecology and the Environment 2: 35–42.

Andow D (1991) Vegetational diversity and arthropod population response. AnnualReview of Entomology 36: 561–586.

Aquilino KM, Cardinale BJ, and Ives AR (2005) Reciprocal effects of host plant andnatural enemy diversity on herbivore suppression: An empirical study of amodel tritrophic system. Oikos 108: 275–282.

Armbrecht I and Perfecto I (2003) Litter-twig dwelling ant species richness andpredation potential within a forest fragment and neighboring coffee plantations ofcontrasting habitat quality in Mexico. Agriculture, Ecosystems & Environment97: 107–115.

Barbosa P (1998) Conservation Biological Control. San Diego, CA: Academic Press.Bawa KS, Kress WJ, Nadkami NM, et al. (2004) Tropical ecosystems into the 21st

century. Science 306: 227–228.Benbrook C (2001) Do GM crops mean less pesticide use? Pesticide Outlook 12:

204–207.Bengtsson J, Ahnstrom J, and Weibull AC (2005) The effects of organic agriculture

on biodiversity and abundance: A meta-analysis. Journal of Applied Ecology 42:261–269.

Benton TG, Vickery JA, and Wilson JD (2003) Farmland biodiversity: Is habitatheterogeneity the key? Trends in Ecology & Evolution 18: 182–188.

Berndt LA, Wratten SD, and Hassan P (2002) Effects of buckwheat flowers onleafroller (Lepidoptera: Tortricidae) parasitoids in a New Zealand vineyard.Agricultural and Forest Entomology 4: 39–45.

Bianchi F, Booij C, and Tscharntke T (2006) Sustainable pest regulation in agriculturallandscapes: A review on landscape composition, biodiversity and natural pestcontrol. Proceedings of the Royal Society B: Biological Sciences 273: 1715.

Bianchi FJJA, Goedhart P, and Baveco J (2008) Enhanced pest control in cabbagecrops near forest in The Netherlands. Landscape Ecology 23: 595–602.

Boatman N (1994) Field Margins: Integrating Agriculture and Conservation. Surrey,UK: British Crop Protection Council.

Bogran CE, Heinz KM, and Ciomperlik MA (2002) Inter-specific competition amonginsect parasitoids: Field experiments with whitefiles as hosts in cotton. Ecology83: 653–668.

Borer ET, Seabloom EW, Shurin JB, et al. (2005) What determines the strength of atrophic cascade? Ecology 86: 528–537.

Borkhataria RR, Collazo JA, and Groom MJ (2006) Additive effects of vertebratepredators on insects in a Puerto Rican coffee plantation. Ecological Applications16: 696–703.

Bruno JF and Cardinale BJ (2008) Cascading effects of predator richness. Frontiersin Ecology and the Environment 6: 539–546.

Cardinale BJ, Harvey CT, Gross K, and Ives AR (2003) Biodiversity and biocontrol:Emergent impacts of a multi-enemy assemblage on pest suppression and cropyield in an agroecosystem. Ecology Letters 6: 857–865.

Cardinale BJ, Srivastava DS, Duffy JE, et al. (2006) Effects of biodiversity on thefunctioning of trophic groups and ecosystems. Nature 443: 989–992.

Chang GC (1996) Comparison of single versus multiple species of generalistpredators for biological control. Environmental Entomology 25: 207–212.

Daily G (1997) Nature’s Services: Societal Dependence on Natural Ecosystems.Washington: Island Press.

Denno RF, McClure MS, and Ott JR (1995) Interspecific interactions inphytophagous insects: Competition reexamined and resurrected. Annual Reviewof Entomology 40: 297–331.

Denoth M, Frid L, and Myers JH (2002) Multiple agents in biological control:Improving the odds? Biological Control 24: 20–30.



Diaz S and Cabido M (2001) Vive la difference: Plant functional diversity matters toecosystem processes. Trends in Ecology & Evolution 16: 646–655.

Duffy JE, Cardinale BJ, France KE, et al. (2007) The functional role ofbiodiversity in ecosystems: Incorporating trophic complexity. Ecology Letters 10:522–538.

Elton CS (1958) The Ecology of Invasions by Animals and Plants. London, UK:Methuen.

Fiedler AK, Landis DA, and Wratten SD (2008) Maximizing ecosystem services fromconservation biological control: The role of habitat management. BiologicalControl 45: 254–271.

Finke DL and Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: Implications for prey suppression. Ecology 83:643–652.

Finke DL and Denno RF (2004) Predator diversity dampens trophic cascades.Nature 429: 407–410.

Finke DL and Denno RF (2005) Predator diversity and the functioning ofecosystems: The role of intraguild predation in dampening trophic cascades.Ecology Letters 8: 1299–1306.

Finke DL and Snyder WE (2008) Niche partitioning increases resource exploitationby diverse communities. Science 321: 1488.

Flynn D, Gogol-Prokurat M, Nogeire T, et al. (2009) Loss of functional diversityunder land use intensification across multiple taxa. Ecology Letters 12: 22–33.

Gardiner M, Landis D, Gratton C, et al. (2009) Landscape diversity enhancesbiological control of an introduced crop pest in the north-central USA.Ecological Applications 19: 143–154.

Gliessman SR (1989) Ecological Basis for Sustainable Agriculture. New York, NY:Springer-Verlag.

Gurr GM, Wratten SD, and Luna JM (2003) Multi-function agricultural biodiversity:Pest management and other benefits. Basic and Applied Ecology 4: 107–116.

Halaj J, Ross DW, and Moldenke AR (1997) Negative effects of ant foraging onspiders in Douglas-fir canopies. Oecologia 109: 313–322.

Harrison S and Bruna E (1999) Habitat fragmentation and large-scale conservation:What do we know for sure? Ecography 22: 225–232.

Harvey CA, Villanueva C, Villacıs J, et al. (2005) Contribution of live fences to theecological integrity of agricultural landscapes. Agriculture, Ecosystems &Environment 111: 200–230.

Hill D (1987) Agricultural Insect Pests of Temperate Regions and their Control.New York: Cambridge University Press.

Hole DG, Perkins AJ, Wilson JD, et al. (2005) Does organic farming benefitbiodiversity? Biological Conservation 122: 113–130.

Hooper DU, Chapin FS, Ewel JJ, et al. (2005) Effects of biodiversity on ecosystemfunctioning: A consensus of current knowledge. Ecological Monographs 75:3–35.

Huang HT and Yang P (1987) The ancient cultured citrus ant. BioScience 37:665–671.

Huston MA (1997) Hidden treatments in ecological experiments: Re-evaluating theecosystem function of biodiversity. Oecologia 110: 449–460.

Ives AR, Cardinale BJ, and Snyder WE (2005) A synthesis of subdisciplines:Predator–prey interactions, and biodiversity and ecosystem functioning. EcologyLetters 8: 102–116.

Jacometti MA, Wratten SD, and Walter M (2007) Management of understorey toreduce the primary inoculum of Botrytis cinerea: Enhancing ecosystem servicesin vineyards. Biological Control 40: 57–64.

Klein A, Steffan-Dewenter I, and Tscharntke T (2006) Rain forest promotes trophicinteractions and diversity of trap-nesting Hymenoptera in adjacent agroforestry.Journal of Animal Ecology 75: 315–323.

Kremen C, Williams NM, Bugg RL, Fay JP, and Thorp RW (2004) The arearequirement of an ecosystem service: Crop pollination by native beecommunities in California. Ecology Letters 7: 1109–1119.

Kromp B (1999) Carabid beetles in sustainable agriculture: A review on pest controlefficacy, cultivation impacts and enhancement. Agriculture, Ecosystems &Environment 74: 187–228.

Kruess A and Tscharntke T (1994) Habitat fragmentation, species loss, andbiological control. Science 264.

Landis DA, Gardiner MM, Van Der Werf W, and Swinton SM (2008) Increasingcorn for biofuel production reduces biocontrol services in agriculturallandscapes. Proceedings of the National Academy of Sciences 105: 20552.

Landis DA, Wratten SD, and Gurr GM (2000) Natural enemies of arthropod pests inagriculture. Annual Review of Entomology 45: 175–201.

Lang A (2003) Intraguild interference and biocontrol effects of generalist predatorsin a winter wheat field. Oecologia 134: 144–153.

Langellotto GA and Denno RF (2004) Responses of invertebrate natural enemies tocomplex-structured habitats: A meta-analytical synthesis. Oecologia 139: 1–10.

Lavandero B, Wratten SD, Didham RK, and Gurr G (2006) Increasing floral diversityfor selective enhancement of biological control agents: A double-edged sward?Basic and Applied Ecology 7: 236–243.

Letourneau DK and Bothwell SG (2008) Comparison of organic and conventionalfarms: Challenging ecologists to make biodiversity functional. Frontiers inEcology and the Environment 6: 430–438.

Letourneau DK, Jedlicka JA, Bothwell SG, and Moreno CR (2009) Effects of naturalenemy biodiversity on the suppression of arthropod herbivores in terrestrialecosystems. Annual Review of Ecology, Evolution, and Systematics 40: 573–592.

Liang W and Huang M (1994) Influence of citrus orchard ground cover plants onarthropod communities in China: A review. Agriculture, Ecosystems &Environment 50: 29–37.

Loreau M, Naeem S, Inchausti P, et al. (2001) Biodiversity and ecosystemfunctioning: Current knowledge and future challenges. Science 294: 804–808.

Losey JE and Denno RF (1998) Positive predator-predator interactions: Enhancedpredation rates and synergistic suppression of aphid populations. Ecology 79:2143–2152.

Losey JE and Denno RF (1999) Factors facilitating synergistic predation: Thecentral role of synchrony. Ecological Applications 9: 378–386.

Macfadyen S, Gibson R, Polaszek A, et al. (2009) Do differences in food webstructure between organic and conventional farms affect the ecosystem service ofpest control? Ecology Letters 12: 229–238.

Marino PC and Landis DA (1996) Effect of landscape structure on parasitoiddiversity and parasitism in agroecosystems. Ecological Applications 6: 276–284.

McLaughlin A and Mineau P (1995) The impact of agricultural practices onbiodiversity. Agriculture, Ecosystems & Environment 55: 201–212.

Morales H and Perfecto I (2001) Traditional knowledge and pest management in theGuatemalan highlands. Agriculture and Human Values 17: 49–63.

Muller CB and Brodeur J (2002) Intraguild predation in biological control andconservation biology. Biological Control 25: 216–223.

Myers JH, Higgins C, and Kovacs E (1989) How many insect species are necessaryfor the biological control of insects? Environmental Entomology 18: 541–547.

Neumann G and Shields EJ (2008) Multiple-species natural enemy approach forbiological control of alfalfa snout beetle (Coleoptera: Curculionidae) usingentomopathogenic nematodes. Journal of Economic Entomology 101:1533–1539.

Nicholls CI, Parrella M, and Altieri MA (2001) The effects of a vegetational corridoron the abundance and dispersal of insect biodiversity within a northernCalifornia organic vineyard. Landscape Ecology 16: 133–146.

Peacock L and Herrick S (2000) Responses of the willow beetle Phratoravulgatissima to genetically and spatially diverse Salix spp. plantations. Journalof Applied Ecology 37: 821–831.

Pell JK, Baverstock J, Roy HE, Ware RL, and Majerus MEN (2008) Intraguildpredation involving Harmonia axyridis: A review of current knowledge and futureperspectives. BioControl 53: 147–168.

Perez-Lachaud G, Batchelor TP, and Hardy ICW (2004) Wasp eat wasp: Facultativehyperparasitism and intraguild predation by bethylid wasps. Biological Control30: 149–155.

Perfecto I, Rice RA, Greenberg R, and VanderVoort ME (1996) Shade coffee: Adisappearing refuge for biodiversity. Bioscience 46: 598–608.

Perfecto I and Vandermeer J (2002) The quality of agroecological matrix in atropical montane landscape: Ants in coffee plantations in southern Mexico.Conservation Biology 16: 174–182.

Perfecto I, Vandermeer JH, Bautista GL, et al. (2004) Greater predation in shadedcoffee farms: The role of resident neotropical birds. Ecology 85: 2677–2681.

Petchy OL and Gaston KJ (2006) Functional diversity: Back to basics and lookingforward. Ecology Letters 9: 741–758.

Philpott SM, Arendt WJ, Armbrecht I, et al. (2008) Biodiversity loss in LatinAmerican coffee landscapes: Review of the evidence on ants, birds, and trees.Conservation Biology 22: 1093–1105.

Philpott SM, Soong O, Lowenstein JH, et al. (2009) Functional richness andecosystem services: Bird predation on arthropods in tropical agroecosystems.Ecological Applications 19: 1858–1867.

Pimentel D (1961) Species diversity and insect population outbreaks. Annals of theEntomological Society of America 54: 76–86.

Polis GA, Hurd SD, Jackson CT, and Sanchez-Pinero F (1989) Multi-factorpopulation limitation: Variable spatial and temporal control of spiders on Gulf ofCalifornia islands. Ecology.

Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity andproductivity of aquatic communities. Ecological Applications 15: 618–627.

Root RB (1973) Organization of a plant-arthropod association in simple and diversehabitats: The fauna of collards (Brassica oleracea). Ecological Monographs 43:95–124.



Rosenheim JA and Harmon JP (2006) The influence of intraguild predation on thesuppression of a shared prey population: An empirical assessment. In: BrodeurJ and Boivin G (eds.) Trophic and Guild Interactions in Biological Control, pp.1–20. Dordrecht, The Netherlands: Springer.

Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, and Jaffee B (1995) Intraguildpredation among biological-control agents: Theory and evidence. BiologicalControl 5: 303–335.

Rosenheim JA, Limburg DD, and Colfer RG (1999) Impact of generalist predatorson a biological control agent, Chrysoperla carnea: Direct observations.Ecological Applications 9: 409–417.

Schellhorn NA and Sork VL (1997) The impact of weed diversity on insectpopulation dynamics and crop yields in collards, Brassica oleracea(Brassicaceae). Oecologia 111: 233–240.

Schmidt MH, Lauer A, Purtauf T, et al. (2003) Relative importance of predators andparasitoids for cereal aphid control. Proceedings of the Royal Society B:Biological Sciences 270: 1905–1909.

Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88: 2415–2426.Schroth G, Krauss U, Gasparotto L, Duarte Aguilar JA, and Vohland K (2000) Pests

and diseases in agroforestry systems of the humid tropics. Agroforestry Systems50: 199–241.

Schweiger O, Musche M, Baily D, et al. (2007) Functional richness of localhoverfly communities (Diptera, Syrphidae) in response to land use acrosstemperate Europe. Oikos 116: 461–472.

Sih A, Englund G, and Wooster D (1998) Emergent impacts of multiple predatorson prey. Trends in Ecology & Evolution 13: 350–355.

Snyder WE, Clevenger GM, and Eigenbrode SD (2004) Intraguild predation andsuccessful invasion by introduced ladybird beetles. Oecologia 140: 559–565.

Snyder WE and Ives AR (2001) Generalist predators disrupt biological control by aspecialist parasitoid. Ecology 82: 705–716.

Snyder WE and Ives AR (2003) Interactions between specialist and generalist naturalenemies: Parasitoids, predators, and pea aphid biocontrol. Ecology 84: 91–107.

Snyder WE and Wise DH (2001) Contrasting trophic cascades generated by acommunity of generalist predators. Ecology 82: 1571–1583.

Sokol-Hessner L and Schmitz OJ (2002) Aggregate effects of multiple predatorspecies on a shared prey. Ecology 83.

Sperber CF, Nakayama K, Valverde MJ, and Neves FS (2004) Tree species richnessand density affect parasitoid diversity in cacao agroforestry. Basic and AppliedEcology 5: 241–251.

Steffan-Dewenter I, Kessler M, Barkmann J, et al. (2007) Tradeoffs between income,biodiversity, and ecosystem functioning during tropical rainforest conversion andagroforestry intensification. Proceedings of the National Academy of Sciences104: 4973.

Straub CS, Finke DL, and Snyder WE (2008) Are the conservation of natural enemybiodiversity and biological control compatible goals? Biological Control 45:225–237.

Swift and Anderson (1993) Biodiversity and ecosystem function in agroecosystems.In: Schultze E and Mooney HA (eds.) Biodiversity and Ecosystem Function, pp.57–83. New York: Springer.

Thies C and Tscharntke T (1999) Landscape structure and biological control inagroecosystems. Science 285: 893.

Tilman D, Knops J, Wedin D, et al. (1997) The influence of functional diversity andcomposition on ecosystem processes. Science 277: 1300–1302.

Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, and Thies C (2005) Landscapeperspectives on agricultural intensification and biodiversity–ecosystem servicemanagement. Ecology Letters 8: 857–874.

Tylianakis JM, Rand TA, Kahmen A, et al. (2008) Resource heterogeneity moderatesthe biodiversity-function relationship in real world ecosystems. PLoS Biology 6:947–956.

Van Bael S, Philpott SM, Greenberg R, et al. (2008) Birds as predators in tropicalagroforestry systems. Ecology 89: 928–934.

Van den Bosch R (1989) The Pesticide Conspiracy. Berkeley: University ofCalifornia Press.

van Lenteren JC, Bale J, Bigler E, Hokkanen HMT, and Loomans AM (2006)Assessing risks of releasing exotic biological control agents of arthropod pests.Annual Review of Entomology 51: 609–634.

Vandermeer J and Carvajal R (2001) Metapopulation dynamics and the quality ofthe matrix. American Naturalist 158: 211–220.

Vandermeer J and Perfecto I (1995) Breakfast of Biodiversity: The Truth About RainForest Destruction. Oakland, CA: Institute for Food and Development Policy.

Vandermeer J, Perfecto I, and Philpott S (2010) Ecological complexity and pestcontrol in organic coffee production: Uncovering an autonomous ecosystemservice. Bioscience 60: 527–537.

Vandermeer JH (1992) The Ecology of Intercropping. New York, NY: CambridgeUniversity Press.

Williams-Guillen K, Perfecto I, and Vandermeer J (2008) Bats limit insects in aneotropical agroforestry system. Science 320: 70.

Yachi S and Loreau M (1999) Biodiversity and ecosystem productivity in afluctuating environment: The insurance hypothesis. Proceedings of the NationalAcademy of Sciences 96: 1463–1468.

Zehnder G, Gurr GM, Kuhne S, et al. (2007) Arthropod pest management inorganic crops. Annual Review of Entomology 52: 57–80.

Zhu Y, Chen H, Fan J, et al. (2000) Genetic diversity and disease control in rice.Nature 406: 718–722.

biodiversity and pest control services - ucsc directory of

Documents