Insect Pest Management Techniques for Environmental Protection 5

Andow CONTENTS 5.1 Introduction...1485.2 Natural Enemy Colonization ...1495.2.1 Hypothesis 1 — Natural Enemy Abundance is Increased Because the Spatial Proximity of Source Populations Re

Cultural Practices

Using Cultural Practices to Enhance Insect Pest Control

by Natural EnemiesN.A Schellhorn, J.P Harmon, and D.A Andow

CONTENTS

5.1 Introduction 1485.2 Natural Enemy Colonization 1495.2.1 Hypothesis 1 — Natural Enemy Abundance is Increased

Because the Spatial Proximity of Source Populations

Results in Higher Colonization 1505.2.2 Hypothesis 2 — Natural Enemy Abundance is Increased

Because the Previously Occupied Habitat is no Longer

Suitable, which Results in Higher Colonization 1535.2.3 Hypothesis 3 — Natural Enemy Abundance is Increased

Because a Habitat is Attractive in Some Way, which Results

in Higher Colonization 1545.3 Natural Enemy Reproduction and Longevity 1565.3.1 Hypothesis 1 — Natural Enemy Abundance is Increased

Because Food is More Abundant, which Results in Higher Reproduction, Longevity, and/or Survival 1565.3.2 Hypothesis 2 — Natural Enemy Abundance is Increased

Because Food is Available During a Longer Period of Time, which Results in Higher Reproduction, Longevity, and/or

Survival 1585.3.3 Hypothesis 3 — Natural Enemy Abundance is Increased Because

the Microclimate Allows Higher Reproduction and Longevity 1605.4 Natural Enemy Diversity 160

5.5 Conclusions 162References 163

5.1 INTRODUCTION

Cultural control of insect pests includes any modification in the way a crop orlivestock is produced that results in lower pest populations or damage This includesboth changes in production practices of the crop or livestock and changes in surroundingareas of production Some pest management specialists define cultural controls aspurposeful manipulation of production practices to reduce pest populations or damage,but the concept is used more broadly here to include any change in production practicethat results in lower pest populations or damage, whether intentional or not

Cultural controls are defined to exclude production practices that act directly oninsect pests, such as insecticide application, biological control, genetic control, andbehavioral modifiers In some treatments of the topic, plant and animal resistance isincluded as a cultural control Because both the genetics and the environment of thecrop or livestock influence plant and animal resistance to pest attack, resistance is inpart determined by cultural practices Traditionally, resistance is treated as a separatepest control tactic, and it is excluded from the present discussion of cultural control.Cultural controls include a diverse set of practices, including: sanitation; destruc-tion of alternate habitats and hosts used by the pest; tillage; water management;plant or animal density; crop rotation and fallow; crop planting date; trap cropping;vegetational diversity; fertilizer use; and harvest time Sanitation is the removal anddestruction of crop or animal material to reduce pest density, including the destruc-tion of crop residues and the disposal of animal wastes (Stern, 1991) Destruction

of alternate habitats and hosts is usually aimed at overwintering habitats and hosts,and has met with limited success Tillage is used to prepare soil for planting and toreduce weeds The various forms of tillage have diverse effects on insect pests(Stinner and House, 1990) Water management, such as irrigation, can affect pestpopulations, but because of its importance for growth and development of crops andlivestock, it has been little used as a pest control tactic (Pedigo, 1996) Plant andanimal density has significant effects on pests (Teetes, 1991) Many pests becomemore abundant at higher plant or animal density, but some become rarer Often,however, non-pest control considerations determine production densities, and thegeneral effects of density are only partially understood Crop rotation entails chang-ing the crop in subsequent plantings, and crop fallow involves suppressing all plantgrowth on a field for a production season Both practices can disrupt the normal lifecycle of a pest, reducing its populations and damage (Brust and Stinner, 1991).Planting date has dramatic effects on pests, and prior to the advent of inexpensive,synthetic organic insecticides, was widely used to avoid pest attack (Teetes, 1991).The timing of other cultural practices, such as cattle dehorning and crop harvest,can also affect pests (Stern, 1991; Pedigo, 1996) Trap cropping involves planting

a crop to attract pests, to divert them from the nearby main crop or to concentratethem for easy destruction (Hokkanen, 1991) Vegetational diversity involves using

other plants in the crop field to reduce pest attack (Andow, 1991) This includesintercropping, strip cropping, and weedy culture Nitrogen applications such asfertilizers can have large effects on insect populations and attack, because nitrogen

is limiting to most insects that eat plants (Mattson, 1980) All of these direct culturaleffects on insect pests have been evaluated for many decades and excellent reviews

of most of these controls have been published recently Here we focus on a evaluated factor: how cultural practices affect natural enemies of insect pests, con-centrating on predators and parasitoids

less-The effects of cultural practices on natural enemies and the potential consequenteffects on insect pests are an indirect mechanism for cultural control In some cases,these indirect effects could be discussed as a type of biological control, emphasizingthe role of the natural enemies In this chapter, however, the role of the culturalpractices that can affect natural enemies will be emphasized to draw a more explicitlink between the practices that humans can manipulate and the effects on the naturalenemies In the long run, it will be useful to identify these links so that reliable,sustainable insect pest control tactics can be developed

Cultural practices can affect natural enemy population densities and species sity Either of these can influence the ability of the natural enemies to suppress pestpopulations Increased density of a particular species or a greater number of naturalenemy species can result in greater mortality of the target pest There are numerousexamples in the literature demonstrating that cultural practices can enhance naturalenemy abundance, and possibly their efficiency; however, the majority are descriptiveand usually only compare abundance in one production system to another Understand-ing the population processes involved in the population changes is necessary to develop

diver-a generdiver-al rediver-alizdiver-ation of how culturdiver-al prdiver-actices cdiver-an result in higher densities of pdiver-ardiver-asitoidsand predators Colonization, reproduction, and longevity are three fundamental popu-lation processes that influence natural enemy density By concentrating on these pop-ulation processes it is possible to develop specific predictions for mechanisms by whichcultural practices can affect natural enemy density

The effects of cultural practices on natural enemy diversity are less commonlystudied Greater species diversity of natural enemies may result in reduced pestpopulations, because each species kills a part of the pest population that otherwisewould have survived (Riechert et al., 1999; Schellhorn and Andow, 1999; but seeRosenheim, 1998) The interactions among natural enemies require further study tounderstand the role of natural enemy diversity on pests

5.2 NATURAL ENEMY COLONIZATION

Natural enemy colonization may be higher in one location than another because:(1) there were more natural enemies near the location; (2) surrounding areas becameless suitable and the natural enemies left these areas ending up in the location; or(3) the location became attractive to natural enemies and they accumulated there Thefirst hypothesis does not require that the natural enemies have a difference in preferenceamong locations If natural enemies are colonizing species (Southwood, 1962), orexhibit an oogenesis-flight syndrome (Johnson, 1960; Dingle, 1972), then they will

disperse from habitats irrespective of the relative quality of the surrounding habitats.Under these circumstances, locations that are near large numbers of natural enemieswill be colonized more readily than those farther away The second two hypothesesrequire that there is a difference in preference In the second, natural enemies areinduced to leave a deteriorating area, and in the third, they are attracted to a particularlygood area The importance of preference in habitat selection is predicted by foragingtheory (Kamil et al., 1987) Using population dynamics theory, the conditions underwhich natural enemies will become more abundant in the target habitat are developed

in Andow (1996) In practice, these three hypotheses are often difficult to distinguish

5.2.1 Hypothesis 1 — Natural Enemy Abundance is Increased Because the Spatial Proximity of Source Populations

Results in Higher Colonization

Most agricultural crops do not by themselves have sufficient resources to keepand maintain high levels of natural enemies throughout the entire year Parasites andpredators use non-crops and non-crop habitats for overwintering sites, refuges, andmore favorable microclimates, as well as additional prey, hosts, or food Many naturalenemies will move throughout the landscape to locate necessary habitats andresources Cultural control tactics can be used to take advantage of this movementand increase the colonization of fields and crops that harbor pest species If sufficientspatial and temporal synchrony is attained, natural enemy populations can increase

in an area because of the proximity of nearby source populations, and the spatialstructure of the habitats on the landscape

Overwintering is a crucial part of the life cycle for most insects in temperateareas Culture control tactics take advantage of this to directly reduce pests, forexample, by sanitation and tillage These same practices may also work to decreasenatural enemy abundance Overwintering might also be a key to abundant naturalenemy populations Adding overwintering sites such as hedge rows, grassy edges,non-crop habitats or other landscape modifications has been touted as a culturalcontrol technique with great potential to increase enemy populations, strengthen theinsect-enemy interaction, and increase the diversity of natural enemy species (Wrat-ten and Thomas, 1990) By increasing natural enemy overwintering survival, colo-nization from these overwintering sites may be an important mechanism to increasedensities of natural enemies associated with target crops, fields, and livestock.Some artificial overwintering sites such as human-made boxes have found suc-

cess in increasing the abundance of predators such as the green lacewing Chrysoperla

carnea Stephens (Sengonca and Frings, 1989) and Polistes wasps (Gillaspy, 1971).

Natural overwintering sites can be improved by management techniques For ple, adding leaves, grass, or other organic litter to the base of trees may lead to

exam-higher quality overwintering sites for the predaceous mite Metaseiulus occidentalis (Deng et al., 1988) and the coccinellid Stethorus punctum punctum (Fell and Hull,

1996) Where overwintering is associated with suppression of reproduction and thenatural enemies continue to feed, planting specific vegetation and ensuring adequatefood sources may be the key for reducing overwintering mortality (James, 1989)

Extensive research has been performed to determine how natural boundaries andedges surrounding agricultural fields influence aphid predators in cereal and graincrop systems in Europe Studies have demonstrated how hedges and other boundaryareas are crucial to the overwintering survival of species of carabid and staphylinidpredators (Sotherton, 1984) By applying insecticides to these habitats, Sotherton(1984) was able to show a considerable reduction in the predator populations inadjoining crops the next spring Other evidence for increased movement of naturalenemies from overwintering sites include mark and recapture studies that have shownpredators from edge habitats immigrate into nearby crop fields, and correlationsbetween the number of predators in overwintering sites and the number of thosepredators in fields early in the growing season (Coombes and Sotherton, 1986) Forsome natural enemies such as species of ground beetles, progeny of overwinteredadults have been shown to immigrate into adjacent fields and then have an affinityfor returning to the same boundary areas as the previous generation (Coombes andSotherton, 1986) In many systems, it may be important to look for changes innatural enemies’ populations both within and between generations.

Maintaining field boundaries in an appropriate habitat can be an important way

to increase colonization of a variety of natural enemy species into target fields, but

it is important to consider numerous factors including the type of crop, field ary, key predators, and disturbance schedule (e.g., pesticide applications, tillage,harvest) Each of these variables can have a significant effect on the timing andextent of predator colonization (Coombes and Sotherton, 1986; Thomas et al., 1991;Wallin, 1985) For example, Carillo (1985) showed that earwigs (Dermaptera) seem

bound-to have more limited movement through barley than they do through non-cropgrasses Wallin (1985) showed that different species of carabids used adjacent fieldboundaries at different times of the year for different purposes

In some cases, overwintering sites that are separated from crop fields are

nec-essary for the survival of the natural enemy Minute solitary egg parasitoids, Anagrus

spp., have been found to be an important mortality factor for the western grape

leafhopper, Erythroneura elegantula, an economically significant pest of grapes in the western U.S (Corbett and Rosenheim, 1996) Anagrus spp require an egg host

to overwinter; however, all of the major species of leafhoppers found in grapesoverwinter in the adult stage Therefore, other leafhoppers must be used as over-

wintering hosts of the parasitoids Anagrus spp can overwinter in the eggs of a

native non-pest leafhopper found in wild blackberries and then move into vineyardsthe next year (Doutt and Nakata, 1973) Vineyards within 5.6 km of blackberrieshave been reported to benefit from parasitoids emigrating from the blackberry

refuges (Doutt and Nakata, 1973) Kido et al (1984) showed that Anagrus adults were also capable of parasitizing another leafhopper species, Edwardsiana pruni-

cola, that overwinters as an egg in French prune tree orchards They showed a

correlation between grape leafhopper parasitism in vineyards and Anagrus dispersal during early spring from nearby French prune tree orchards that harbored E pruni-

cola Laboratory studies revealed that parasitoids reared on one leafhopper species

can readily parasitize the other species (Kido et al., 1984; Williams, 1984), so eitheralternative host can act as an overwintering refuge to increase the colonization ofparasitoids to vineyards early in the growing season

Significant correlation between the presence of French prune tree refuges andhigher parasitoid abundance in grape vineyards has been found repeatedly (Kido

et al., 1984; Murphy et al., 1996) To prove that these refuges were the source ofparasitoids in grape vineyards, however, it was necessary to show that the overwin-tering parasitoids were indeed immigrating into adjacent vineyards Corbett andRosenheim (1996) used rare element labeling to mark overwintering parasitoids inthe refuge and then track their movement by recapturing individuals in the vineyardsthe next year This mark-recapture experiment demonstrated that parasitoids fromthe nearby refuges do colonize adjacent vineyards, yet the contribution colonistsmade to the total early season parasitoid population was relatively low and variable(1% and 34% of parasitoids in two experimental vineyards) By immigrating early

in the season, even the smaller numbers of parasitoids from these refuges may beable to play a critical role in increasing parasitism and controlling populations ofthe western grape leafhopper (Murphy et al., 1998)

It is also possible that the prune tree refuge may increase parasitoid immigration

in more subtle ways Flying insects accumulate in sheltered regions downwind ofnatural or artificial windbreaks (Lewis and Stephenson, 1966) Because dispersing

A epos accumulate at a much greater rate downwind of prune tree refuges, it has

been speculated that the French prune trees act both as a collection of overwinteringhosts and as a natural windbreak which influences the colonization of dispersingparasitoids (Corbett and Rosenheim, 1996) Further research may be needed to deter-mine optimal refuge size and placement in order to provide sufficient pest control.Aphid parasitoids in grass and cereal crops provide another example of an asso-ciation between higher colonization of natural enemies and the proximity of overwin-tering sites (Vorley and Wratten, 1987) Barley and early sown wheat (drilled beforemid-October) provide a significant source of parasitoids that immigrate into laterplanted wheat fields This was demonstrated both by trapping parasitoids in spatially

oriented baffle traps, and by calculating the expected number of Aphidius spp

para-sitoids and comparing it to the actual field surveys The early sown fields may benefitthe parasitoids in two ways First, it creates an overwintering refuge with high densities

of aphid hosts in the fall The early sown fields also allow for the development of anaphid host early in the season, which in turn allows for parasitoid populations to build

up when other hosts may be relatively scarce Vorley and Wratten (1987) suggestedthat one early planted wheat field generated sufficient parasitoids in the spring toaccount for immigration into about 25 late planted fields Early movement of parasi-toids in the spring may coincide with the initial build up of aphids in the other fields,when parasitoids are capable of the greatest impact on aphid populations

Natural enemy populations may benefit from managing landscapes to increasethe temporal availability of habitats and food so that resources are available fornatural enemies throughout the growing season This has been studied for aphidsand their parasitoids on a variety of weeds and other non-crop hosts (Perrin, 1975;Stary and Lyon, 1980; Müller and Godfrey, 1997) Generalist predators such ascoccinellids have also been shown to use resources from weeds and other non-crophabitats, especially early in the growing season (Banks, 1955; Perrin, 1975; Bentonand Crump, 1981; Honek, 1982; Hodek and Honek, 1996) For example, in Central

Bohemia, populations of the predator Coccinella septempunctata L were found to

colonize habitats sequentially, starting with overwintering sites, then alfalfa andclover in early spring, followed by spring cereals later in the year (Honek, 1982).Other species use field boundaries and edges at different times throughout the seasonfor reproduction and possible recolonization of adjacent fields (Boller et al., 1988;Wallin, 1985) Trap crops such as alfalfa interplanted with cotton may also provide

a source of predators that can colonize adjacent fields and attack pest species (Corbett

et al., 1991) Trap crops allow for the build up of pest and enemy populations inareas adjacent to crops being targeted for pest control Few studies, though, haveshown more than changes in the relative abundance of insects in the trap crops andother added habitats Future studies are needed to understand the mechanisms ofincreased abundance and how to use this information for more effective culturalcontrol

5.2.2 Hypothesis 2 — Natural Enemy Abundance is Increased Because the Previously Occupied Habitat is no Longer

Suitable, which Results in Higher Colonization

Unlike natural systems that typically have one disturbance over multiple years,agricultural systems are subject to multiple disturbances within and between growingseasons Preparing the ground, planting seed, applying nutrients and pesticides,cultivation, and harvest can all act as significant disturbances to the crop ecosystem.Ecologists have begun to recognize that such disturbances can play a key role instructuring ecological communities and population dynamics (Pickett and White,1985) Harvesting, for example, can have a tremendous detrimental effect on naturalenemy populations Honek (1982) estimated that alfalfa harvesting destroyed 90%

of the recently immigrated Coccinella septempunctata population Carillo (1985) demonstrated that cutting ryegrass for forage caused the European earwig, Forficula

auricularia to immigrate to field margins Therefore, it is important to find ways to

encourage frequent colonization and recolonization of natural enemies to maintainhigh population densities of natural enemies

Refuges can be created in and around crop fields to reduce the effects of bance on natural enemies and increase the likelihood of their recolonization Thishas been examined by comparing the effects of block versus strip harvesting of

distur-alfalfa on the population dynamics of a parasitoid Aphidius smithi and its aphid host

Acyrthosiphon pisum (van den Bosch et al., 1966; van den Bosch et al., 1967) Forage

crops like alfalfa are cut and harvested two to four times a year Each time, the fieldsare left devoid of vegetation for several days, creating a harsh microclimate whereboth parasitoid and host are exposed to direct solar radiation Furthermore, theysuggested that the lack of vegetation causes a decline in aphid parasitoids because

of a radical reduction in their obligatory host Altering planting and cutting datescan ameliorate these disturbances By leaving strips of unmowed alfalfa, aphids andparasitoids are given a temporal refuge from cutting disturbances These refuges

allow A smithi to retain a population in the fields so they can respond to aphid outbreaks as they occur Additionally, it appears that A smithi females gradually

move from the taller, older alfalfa into the younger strips between cuttings Thisincreased immigration into young alfalfa puts the parasitoids in contact with young

aphid colonies, where they can have the greatest suppressive effect on aphid lations Gradual movement of parasitoids away from older plants to younger onesalso means there will be fewer parasitoids at risk of being killed when the olderplants are harvested These temporal refuges reduce the effect of cutting on theparasitoid population and increase the parasitoid’s overall ability to control aphidpests Similarly, Mullens et al (1996) found that alternating the removal of manurefrom poultry facilities created temporal refuges that helped increase densities of

popu-predatory mites, Macrocheles spp., that helped control fly pest populations.

Using a metapopulation model, Ives and Settle (1997) suggested a theoreticalbasis for the phenomena observed by van den Bosch (van den Bosch et al., 1966;van den Bosch et al., 1967) If fields are asynchronously planted and harvested,mobile natural enemies will have time to disperse from mature fields into youngerones Therefore, the enemies can have a larger overall effect in controlling herbivorepopulations (Ives and Settle, 1997) If there are few mobile enemies in asynchronousplantings, then insect pest populations increase at alarming rates Further studiescan help determine what systems have the greatest potential for using refuges togive a greater advantage to natural enemy populations

5.2.3 Hypothesis 3 — Natural Enemy Abundance is Increased Because a Habitat is Attractive in Some Way, which

Results in Higher Colonization

Some predators and parasitoids can perceive and respond to sensory informationfrom plants Flowers, which are important sources of nectar for parasitoids, have

been found to attract the parasitoid Microplitis croceipes by olfactory stimuli (Takasu and Lewis, 1993), and the parasitoid Cotesia rubecula by both olfactory and visual

stimuli (Wäckers, 1994) Flowers and flower nectar also attract parasitoids of thetarnished plant bug (Streams et al., 1968; Shahjahan, 1974) Since many parasitoidshave been found to forage for nectar and other food sources, increasing the avail-ability and physical proximity of these sources may increase the immigration ofparasitoids from other sources to target fields This, however, remains to be defini-tively documented

Natural enemies can also be attracted to plants at growth stages that may be

associated with prey or hosts The parasitoid Campoletis sonorensis was attracted

to flowers and other plant parts that are associated with the presence of its host

cotton bollworm (Elzen et al., 1983) The polyphagous heteropteran predator, Orius

insidiosus is attracted to volatile chemicals from maize silk, which may help it feed

on prey (Reid and Lapman, 1989) Other plants and volatile plant chemicals are

detected by and attractive to the parasitoids Peristenus pseudopallipes (Monteith, 1960), Diaeretiella rapae (Read et al., 1970), Heydenia unica (Camors and Payne, 1972), Eucelatoria spp (Nettles, 1979), and the chrysopid predator Chrysoperla

carnea (Flint et al., 1979).

The reaction of insects to plant stimuli often depends on the physiological state

of the insect For example, it has been found that hungry female parasitoidsresponded to food-associated odors, while well-fed females responded to the host-associated odors (Takasu and Lewis, 1993; Wäckers, 1994) The ability of an insect

to respond to an odor may also depend on previous experience Microplitis croceipes

is able to learn different odors and associate them with either host or food resources(Lewis and Takasu, 1990) Parasitic flies have also been found to be attracted to orrepelled by plant odors from different trees, depending on the flies’ age in relation

to reproductive maturity (Monteith, 1960)

Natural enemies are also capable of perceiving and responding to other plant

cues In studying the mechanistic response of the predator Orius tristicolor White

to a corn-bean-squash polyculture, five possible cues were described that couldinfluence insect immigration: plant density, plant architecture, visual cues, volatilechemicals, and microclimate such as relative humidity (Letourneau, 1990) Theresults suggest that plant architecture and density increased colonization of thepredator, regardless of prey density or plant diversity Others have noted differences

in predator abundance associated with variation in plant architecture and density,perhaps caused by microclimatic differences (Honek, 1982)

Many species have the ability to detect their prey or hosts from a distance Frass

from the larvae and scales from adult of the corn earworm Helicoverpa zea (Boddie)

contain chemical stimuli that invoke higher activity rates and oriented host-seeking

behavior in the larval parasitoid M croceipes, and egg parasitoids Trichogramma

spp (Jones et al., 1971; Jones et al., 1973; Gross et al., 1975) However, it remainsuncertain how these attractants influence the population dynamics of the parasitoidsand on what spatial scales these attractants can cause increases in colonization.Some natural enemies have also found to be attracted to volatile plant chemicalsthat are induced by insect herbivory These compounds might be important in hosthabitat location and have been shown to be involved in the host location process

Attraction has been observed for the parasitoids Cotesia marginiventris (Turlings

et al., 1990; Alborn et al., 1997), Microplitis croceipes (McCall et al., 1993),

Cor-tesia glomerata (Mattiacci et al., 1994), and Cardiochiles nigriceps (De Moraes

et al., 1998); the predaceous mites Metaseiulus occidentalis, Phytoseiulus persimilis (Sabelis and van de Baan, 1983), and Amblyseius potentillae (Dicke et al., 1990);

and anthocorid predators (Drukker et al., 1995) Natural enemies have been shown

to respond to plants that are typical food sources for their hosts or prey It has beenrecently shown that plants give off different amounts of volatile compounds inresponse to different species of herbivores, and distinct parasitoid species can dif-ferentiate these chemical signals and may respond only to those compounds asso-ciated with their preferred hosts (De Moraes et al., 1998) Herbivore-induced plantvolatiles have been shown to cause increased numbers of natural enemies in fieldsituations (Drukker et al., 1995), but it is unclear at what distance natural enemiesare attracted from and at what spatial scale they can be attracted These results,however, demonstrate an enormous potential for using trap crops, intercropping,variation in planting pattern, or artificial chemicals to increase the attractiveness andcolonization of species-specific natural enemies to target fields

Another method of increasing colonization is to use artificial sprays applied to

target fields The abundance of the generalist predator, Coleomegilla maculata can

be increased with sprays of sugar plus wheast, an artificial food source that is a

mixture of a yeast, Saccharomyces fragilis, plus its whey substrate (Nichols and

Neal, 1977) A similar result has been found for coccinellid populations using sugar

solutions (Ewert and Chiang, 1966; Schiefelbein and Chiang, 1966) Adult

Chrysop-erla carnea Stephens are attracted to sucrose sprays mixed with the amino acid

tryptophan, and by mixing tryptophan with artificial honeydews, greater numbers

of adults will colonize sprayed fields (Hagen et al., 1976) Adding tryptophan to anartificial food source may not only increase immigration, but promote egg laying sothat the predaceous larvae can have a significant effect on pest numbers in key areas.The effectiveness of both of these methods is severely reduced if other honeydewand food sources are readily available Whether these other sources interfere withthe olfactory cues or whether their presence alters predator searching behaviorremains to be clarified

5.3 NATURAL ENEMY REPRODUCTION AND LONGEVITY

Natural enemy abundance is increased if reproduction is increased by greaterfecundity and longevity of adults or higher survival of offspring Therefore, culturalpractices that directly affect these processes can reduce insect pest damage Greaterreproduction and adult and larval survival often depend on the quality of the habitat.Habitat quality probably has several components, including food availabilitythroughout the season, food abundance, microclimatic suitability, disturbanceregime, and presence of natural enemies of the natural enemies Of these factors,food availability has received the vast majority of research attention, and our analysisalso concentrates on this factor

5.3.1 Hypothesis 1 — Natural Enemy Abundance is Increased Because Food is More Abundant, which Results

in Higher Reproduction, Longevity, and/or Survival

The diet of adult parasitoids and predators can have important effects on theirlifetime reproductive success (Hagan, 1986; Bugg, 1987; Osakabe, 1988; Heimpel

et al., 1997) Adult female parasitoids of many species feed on host insects (hostfeeding) or a variety of sugar sources, and both can improve egg maturation, adultmaintenance, and survival (Jervis and Kidd, 1986, 1996; Heimpel and Collier, 1996;Heimpel et al., 1997; Olson and Andow, 1998) Furthermore, for those species thathost-feed, the combination of host feeding and access to honey meals can signifi-cantly increase parasitoid lifetime reproductive success (Heimpel et al., 1997).Extremely low lifetime reproductive success and survival were found for individualsthat did not have access to honey (Leius, 1961; Syme, 1975; Idris and Grafius, 1995;Heimpel et al., 1997; Olson and Andow, 1998) Although fewer studies haveaddressed how diet influences lifetime reproductive success of predators and mites,some studies have shown that sugar sources and pollen can increase their fecundityand longevity (McMurtry and Scriven, 1964; Bugg et al., 1987) Abundant sugarand pollen in the field can greatly increase lifetime reproductive success of parasi-toids and predators by enhancing fecundity and longevity

One of the most common sources of sugar and pollen in agricultural systems isfrom the non-crop plants that border or grow within the agricultural field These

plants (often referred to as weeds) provide sugar sources as floral and extrafloralnectar, which are visited by natural enemies (Rogers, 1985; Pemberton and Lee,1996) Flower nectar, extrafloral nectaries, and pollen have all been shown to increasefecundity of parasitoids, predators, and mites (De Lima and Leigh, 1984; Heimpel

et al., 1997) Numerous species of parasitoids are frequently observed to feed onfloral (Leius, 1961, 1967; Elliott et al., 1987; Jervis et al., 1993) and extrafloralnectar (Rogers, 1985; Bugg et al., 1989, Pemberton and Lee, 1996) as well ashoneydew excreted by homopteran insects (Elliot et al., 1987; Evans, 1993) Nectar

is an important food source for adult parasitoids and like honeydew, the consumption

of nectar can result in increased fecundity and longevity (Syme, 1975; Idris andGrafius, 1995; Jervis et al., 1996) Work by Idris and Grafius (1995) found that

parasitoid fecundity was higher when Barbarea vulgaris, Brassica kabar, or Daucus

carota flowers or honey-water was used as food, compared with no food Hagley

and Barber (1992) found that the fecundity of adult Pholetesor ornigis (Braconidae) increased when individuals were confined with flowers of creeping charlie (Glen-

choma hederacea L.), dandelion (Taraxacum officinale Weber), and apple (Malus domesticus L.), but not with flowers of chickweed (Stellaria media L.) or Shepherd’s

purse (Capsella bursapastoris L.) Others have also reported that not all nectar

sources provided benefits to parasitoids (Elliot et al., 1987), and Idris and Grafius(1995) suggested that the accessibility of nectar is related to floral characters,particularly the width of the corolla opening in relation to the size of the forager.Honeydew from aphids has also been reported to increase fecundity in natural

enemies The fecundity of P ornigis increased when individuals were confined with terminal leaves of apple with honeydew of the aphid Aphis pomi DeGeer, but not

when confined with terminal leaves of apple without honeydew or with flowers of

round-leaved mallow (Malva neglecta Waller) or red clover (Trifolium pratense L.).

Parasitoids given aphid honeydew oviposited a greater proportion of their eggs thanthose confined with apple leaves without honeydew (Hagley and Barber, 1992)Sugar sources have a great effect on parasitoid longevity (Leius, 1967; Syme,1975; Heimpel et al., 1997; Olson and Andow, 1998), and are known to expand life

8 to 20 times that without a sugar source (Collier, 1995; Heimpel and Rosenheim,

1995; Heimpel et al., 1997) The life span of sugar-fed Aphytis spp females varies

between 2 and 6 weeks when a sugar source is provided, whereas that of deprived females rarely exceeds three days (Avidov et al., 1970; Heimpel et al.,

sugar-1997) Sugar-fed Trichogramma females live 17 days, but only 2 to 3 days without

sugar (Olson and Andow, 1998), and aphid honeydew did not extend life as long as

sugar (McDougal and Mills, 1997) The longevity of Diadegma insulare females was significantly greater when they fed on the wildflower B vulgaris than on several

other wildflowers commonly found in the surrounding area or water or without food(Idris and Grafius, 1995) In addition to honey and nectar, aphid honeydew is also

known to increase longevity Adult longevity of Diadegma insulare and Pholetesor

ornigis was increased when they were provided with aphid honeydew (Hagley and

Barber, 1992; Idris and Grafius, 1995) However, there was no effect of longevity

for P ornigis when adults where confined with flowers (Hagley and Barber, 1992).

Insect predators are also known to feed on nectar and pollen (Sundby, 1967;Yokoyama, 1978; Crocker and Whitcomb, 1980; De Lima and Leigh, 1984; Bugg,

1987; Hodek and Honek, 1996) Their fecundity and longevity was enhanced byfloral resources (De Lima, 1980; Agnew et al., 1982; Bugg et al., 1987) De Lima

(1980) and De Lima and Leigh (1984) showed that a bigeyed bug, Geocoris pallens

Stål, attained maximum longevity, fecundity, and per capita prey consumption rateswhen cotton extrafloral nectar was available in addition to prey Extrafloral nectaralone, however, was not sufficiently nutritious to sustain reproduction (De Lima and

Leigh, 1984) Geocoris punctipes Say and Collops vittatus Say were found to live

twice as long on common knotweed compared to alfalfa, although the effects ofalternative prey associated with the weed were not clarified (Bugg et al., 1987) It

is possible that prey associated with common knotweed may compete with the pest

species so that Geocoris spends more time searching on the knotweed than on the

crop plant

The relative abundance of prey sources can also influence natural enemies

Populations of Coleomegilla maculata were studied in maize monocultures and

maize-bean-squash polycultures (Andow and Risch, 1985) Populations of this cinellid beetle were greater and predation on artificial prey was higher in monocul-tures, which had higher prey abundance, than in the polycultures, which had foodavailable for a longer part of the growing season Individuals had a higher foragingsuccess rate under higher food densities (Risch et al., 1982) and were also found tohave stayed longer (Wetzler and Risch, 1984)

coc-5.3.2 Hypothesis 2 — Natural Enemy Abundance is Increased Because Food is Available During a Longer Period

of Time, which Results in Higher Reproduction,

Longevity, and/or Survival

Cropping systems that maintain weeds and flowering herbs often provide thefirst food resources of the season, which allows for earlier development of insectpredators compared to systems without the weeds and flowers Female carabids

(Poecilus cupreus L.) were significantly larger and had significantly more eggs earlier

in the season in a cereal crop subdivided by strips of weeds and wild flowering herbscompared to a weed-free cereal area (Zangger et al., 1994) Earlier development ofcarabids may result in higher predator abundance early in the season and greaterpotential for suppressing pest populations

Pollen has been shown to affect predaceous mite populations similarly Pollencan increase the fecundity of predaceous mites (McMurtry and Johnson, 1965;Osakabe, 1988), and egg production was highest when tea pollen was provided to

the predaceous mite, Amblyseius sojaensis Ehara (McMurtry and Scriven, 1964).

Furthermore, it has been demonstrated that a greater percentage of the population

of predaceous mite, Amblyseius hibisci, reached maturity on tea pollen alone than

when feeding solely on spider mites (Osakabe, 1988) The poor survival on spider

mites occurred because young instars of A hibisci became entangled in the webbing

of the spider mites When the spider mite Panonychus citri was at low densities on citrus leaves, however, A hibisci controlled it when tea pollen was added (Osakabe

et al., 1987) The seasonal abundance of A hibisci was closely correlated with peaks