Entomologia Experimentalis et Applicata88: 203–209, 1998.© 1998Kluwer Academic Publishers. Printed in the Netherlands.

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Partitioning two- and three-trophic-level effects of resistant plants on thepredator, Nabis roseipennis

R. S. Pfannenstiel∗ & K. V. YearganDepartment of Entomology, University of Kentucky, Lexington, KY 45046, USA;∗Current address : Tree Fruit Res. & Ext. Center, 1100N. Western Ave, Wenatchee, WA 98801, USA

Accepted 24 May 1998

Abstract

Two- and three-trophic-level effects of resistant soybean plants on the development and fecundity of the predatorNabis roseipennisReuter (Hemiptera: Nabidae) were determined. The nabids, like many hemipteran predators,feed on plants as well as arthropod prey. The life history traits ofN. roseipenniswhen feeding onPseudoplusiaincludens(Hübner) (Lepidoptera: Noctuidae) fed the resistant soybean cultivar PI 229358 or the susceptible Cobb’and while exposed to these resistant and susceptible soybean cultivars or a no-plant control were determined.Nymphal survival ofN. roseipenniswas unaffected by either prey or plant treatment. Development time wasextended and fecundity ofN. roseipenniswas reduced by feeding on prey fed the resistant plant but not by exposureto resistant soybean plants. Thus, three-trophic-level effects of the resistant cultivar PI 229358 on prey qualitywere more important than two-trophic-level effects of direct plant feeding on development and fecundity ofN.roseipennis. Consistency of these results with those of other predatory hemipterans and the potential impact of dietcomposition on the effects of resistant plants are discussed.

Introduction

Plant resistance to insects is known to affect insectpredators and parasitoids either by antibiotic effectsthrough their prey/hosts or by mechanical means thatprevent or hinder movement (Boethel & Eikenbary,1986). Hemipteran predators may feed on plants aswell as arthropod prey (Ridgway & Jones, 1968;Stoner, 1970, 1972). Generally, these predators cannotdevelop on a diet of only plant material (exclud-ing pollen) or, if they become adults after feedingon a diet of plant material, they cannot reproduce.Feeding on plants has been hypothesized to affectpredatory hemipteran development and survival dur-ing periods of prey absence (Stoner, 1970, 1972),and it has been shown to increase these predators’mortality in crops treated with systemic pesticides(Ridgway et al., 1967). Most studies of feeding onplant foliage by hemipteran predators have used ex-cised leaves, leaflets or leaf sections (Stoner, 1970,1972; Naranjo & Stimac, 1985; Rogers & Sulli-van, 1986), which may negatively affect feeding byhemipteran predators. Excising foliage stops move-

ment of fluids within the plant and may decrease theability of a sucking predator to feed on the plant. Plantfeeding by hemipteran predators has been studied ei-ther in the absence of prey feeding or in combinationwith prey feeding (Stoner, 1970, 1972; Naranjo &Stimac, 1985; Rogers & Sullivan, 1986). Predatordevelopment and performance may be affected by dif-ferences in plant genotypes by feeding directly on theplants or on prey that have developed on these plants.Studies designed to specifically separate the effectsof plants through two- and three-trophic-level feedinghave not been done for hemipteran predators. How-ever, Rogers & Sullivan (1986) showed that resistantplants affected growth and development ofGeocorispunctipes(Say) (Hemiptera: Lygaeidae) and their datasuggested that feeding directly on resistant plants mayhave less influence than feeding on prey reared onresistant plants.

We conducted a study to partition the two- andthree-trophic-level effects of resistant soybeans on thebionomics ofNabis roseipennisReuter (Hemiptera:Nabidae). Nabids, particularlyN. roseipennis, are

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among the most abundant predators in soybean (Shep-ard et al., 1974; McPherson et al., 1982; Fergusonet al., 1984; Braman & Yeargan, 1990), and theyare a major predator of lepidopteran eggs and larvae(McCarty et al., 1980; Richman et al., 1980). Theimportance of two- and three-trophic-level effects onnabid bionomics was examined using a factorial de-sign with three plant and two prey treatments. Theplant treatments directly assessed the importance oftwo-trophic-level feeding and the prey treatments ad-dressed the effects of three-trophic-level feeding onnabid development and fecundity. The examination ofinteractions determined if two- and three-trophic-leveleffects are additive or synergistic.

Materials and methods

Predator rearing. A laboratory colony ofN. ro-seipenniswas established in July and August 1994,from individuals collected from soybean fields atSpindletop Farm 8 km N of Lexington, KY, USA.The colony was maintained in environmental cham-bers at 27± 1 ◦C and a L15:D9 photoperiod. Nabidswere reared individually in 9-cm-diameter petri disheswith a moistened dental wick as a water source andfed frozen laboratory-rearedHeliothis virescens(F.)or Trichoplusia ni(Hübner) (both Lepidoptera: Noc-tuidae) eggs twice weekly.H. virescenswas rearedusing the methods of Ignoffo (1965) andT. ni wasreared on a modified pinto-bean diet (Shorey & Hale,1965). Within 5 days of becoming adults, male andfemale nabids were paired within the petri dishes anda green bean was provided as an oviposition substrate.Green beans with eggs were removed, disinfected witha 5% sodium hypochlorite solution to prevent fungalgrowth and placed into 15-cm-diameter petri dishesfor hatching.

Resistant and susceptible soybean cultivar selection.Two resistant (PI 171451 and PI 229358) and twosusceptible (‘Cobb’ and ‘Centennial’) cultivars wereexamined to determine a single resistant and sus-ceptible cultivar for use in this study. Seeds ofeach soybean cultivar were obtained from the USDASoybean Germplasm Collection (Urbana, IL, USA).The growth and development of the soybean looper,Pseudoplusia includens(Walker) (Lepidoptera: Noc-tuidae) was evaluated on each cultivar. FiftyP. inclu-densneonates were isolated singly in 30 ml plasticportion cups (P-100, Solo Cup Co., Urbana, IL) with

a small moistened piece of dental wick and a freshpiece of excised foliage from one of the soybean cul-tivars. Foliage was replaced daily within the diet cupsand frass removed every 2 to 3 days. Leaves from the1st to 4th fully expanded trifoliates below the termi-nal trifoliates on each variety were used to supply thefoliage for this study. Dental wicks were moistenedevery other day. Larvae were reared at 26±1 ◦C undera L5:D9 photoperiod. Larval development time andpupal weight were recorded for each individual andthe sex determined. Treatment effects were analyzedseparately for males and females using Analysis ofVariance (Proc GLM, SAS Institute, 1985) and theFisher LSD test used for mean separation. The mostresistant and most susceptible soybean cultivars wereselected using the development ofP. includenson eachcultivar as the selection criterion.

N. roseipenniseggs were obtained from femalesin the laboratory colony and placed in environmentalchambers at 27±1 ◦C for egg development and emer-gence. Newly emergedN. roseipennisnymphs wereassigned to one of three plant treatments: resistant soy-bean plant, susceptible plant, or a no-plant control.Nymphs placed on plants were put in clip cages onthe lateral leaflets of the top three fully-formed leavesof either a resistant or a susceptible soybean plant (atstage V4–V7; vegetative growth with 4–7 true nodes,Fehr & Caviness, 1977). Clip cages were made from9-mm-thick polyethylene foam sheets cut into two 5-cm squares to be used for each cage. One square wasleft unmodified and a circular section 3.5 cm in di-ameter was cut from the center of the other square.A piece of fine mesh lumite screen (Lumite Co., Cor-nelia, GA, USA) was glued to one side of the squarewith the hole to form an enclosure 3.5 cm in diame-ter and 9-mm-deep. The enclosure was formed whenthe clip cage was attached to a leaflet by placing twosquares (one with and one without an enclosure) oneither side (upper and lower) of the leaflet and placinga rubber band around them to hold them together withthe leaflet in between. An 0.8 cm diameter hole wascut in the screen for introducing soybean looper larvae(P. includens) as prey to nabid nymphs. To preventnabid escape, this hole was blocked during the experi-ment with a small piece of foam rubber. The enclosurewas always placed on the upper surface of the leaflet.The cages were supported by hooks from a wire trellis,which helped minimize damage to the soybean plantsby the cages. Plants were placed in an environmentalchamber at 27± 1 ◦C under a L15:D9 photoperiod forthe duration of the experiment. If leaflets with a nabid

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began to senesce, the nabid was moved to a healthyleaflet. Plants were replaced after about 14 d; thus thepredators had access to healthy plants throughout theexperiment.

From the cultivar selection trials (presented in theresults) PI 229358 was selected for resistance to thepestP. includens(Lambert & Kilen, 1984) and ‘Cobb’was selected as the susceptible cultivar. PI 229358also reportedly negatively affected the predatorG.punctipes(Rogers & Sullivan, 1986). Nymphs as-signed to the no-plant control were placed into 9-cm-diameter petri dishes with a moistened dental wick.Nymphs within each plant (or no-plant) treatmentwere assigned to one of two prey treatments, wherethey were fed frozenP. includenslarvae that had beenfed foliage of either resistant or susceptible soybeanplants. Thus, there were three plant treatments (resis-tant, susceptible and no-plant control) and two preytreatments (P. includensfed resistant or susceptibleplants) for a total of six treatment combinations.

To prepareP. includensfor feeding to the nabids,neonates were placed on excised leaves from either theresistant or the susceptible soybean plant in a 15 cmdiameter petri dish at 27± 1 ◦C. The top four fullyformed leaves on greenhouse grown soybean plants ofeither the resistant or the susceptible variety were usedfor feedingP. includens.Leaves were cut from theplant and each petiole was placed in moistened cot-ton to slow leaf desiccation. Larvae were transferreddaily onto fresh foliage in a clean petri dish. Whenlarvae reached a predetermined size (mean weight of3.2 mg) within the late 2nd to early 3rd instar, theywere collected and frozen at−80 ◦C for later use.Equal sized larvae were used for both the suscepti-ble or resistant treatments. Larvae that fed on eitherthe resistant or the susceptible cultivar were removedfrom the freezer, and one was fed to each nabid nymphdaily. Hereafter,P. includenslarvae that had fed onPI 229358 will be referred to as ‘resistant prey’, andlarvae that had fed on Cobb ‘susceptible prey’. Thescreens of the cages were misted daily to simulate dewand to provide a water source for theN. roseipennisnymphs. Dental wicks in the no-plant treatments weremoistened every other day. After the nabids developedinto adults, they were transferred to 9 cm diameterpetri dishes with a moistened dental wick and were fedtwo larvae per day. Three to 6 d after females becameadults, they were isolated with a male for 24 h for mat-ing. Fresh green beans were supplied to females as anoviposition substrate on the 6th day after becoming anadult, and they were changed daily until females were

20 days old, at which time monitoring of ovipositionwas discontinued.

Data were collected on nymphal survival, devel-opment time from egg hatch to adulthood, weight atadulthood, and fecundity over the 20 day-period afterreaching the adult stage. Twenty-fourN. roseipennisnymphs were set up for each plant× prey treatmentcombination, with six nymphs on each of four indi-vidual plants within each treatment combination or sixnymphs placed individually in petri dishes for a no-plant control. No-plant controls were set up for bothresistant and susceptible prey. Factorial analysis ofvariance for unbalanced data according to GLM pro-cedure (SAS Institute, 1985) was used to analyze thedata. Males and females were analyzed separately forall data except survival because the sex of immaturescould not be determined. Each plant within a treatmentcombination was considered a replicate for analysis ofsurvival data. Pre-planned comparisons were resistantvs susceptible plants, plant treatment vs no-plant, andprey effect in the no-plant controls. A significant planteffect is indicative of two-trophic-level effects (i.e., di-rect plant feeding by the predator), and significant preyeffects indicate a three-trophic-level effect of resistantplants through the prey insect.

Results

Soybean cultivar evaluation and selection.Soybeancultivar and larval gender significantly affected thegrowth (F = 5.27, df = 3, 125, P= 0.0019 andF = 5.05, df= 1, 125, P= 0.0263, respectively) anddevelopment (F = 33.89, df = 3, 125, P< 0.0001and F = 9.89, df = 1, 125, P = 0.0021, re-spectively) ofP. includens. Larvae of both male andfemaleP. includensfeeding on PI 229358, PI 171451and ‘Centennial’ took longer to develop to the pupalstage than when feeding on foliage of ‘Cobb’ (males:16.4, 16.5, and 16.9 vs 15.5 d, and females: 16.0,16.1 and 16.1 vs 15.1 d, respectively). Pupae resultingfrom larvae feeding on Centennial were slightly heav-ier than those feeding on ‘Cobb’ but not significantlyso (males: 190.9 vs 179.2 mg and females: 179.2vs 169.0, respectively). Weights of pupae from indi-viduals feeding on PI 229358 were lower than thosefeeding on PI 171451 (males: 133.1 vs 161.8 mg, andfemales: 123.9 vs 140.5 mg, respectively) and bothweighed less than those fed Cobb or Centennial. Cobbwas selected as the most susceptible cultivar forP.

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Table 1. Calculated F statistics (F) and probability levels (P) of treatment effects onN. roseipen-nis life history characteristics from ANOVA including all main effects and interactions as well aspre-planned comparisons tested by contrast

Development time Adult weight Fecundity

F P F P F P

Females

Full model 3.80 0.007∗ 3.11 0.019∗ 3.98 0.008∗Plant 2.05 0.143 1.91 0.163 0.30 0.745

Prey 9.73 0.004∗ 11.71 0.002∗ 17.71 <0.001∗Plant× prey 3.37 0.045∗ 0.25 0.784 0.34 0.716

Planned comparisons

Plant vs no-plant 0.02 0.884 0.71 0.404 0.09 0.764

Res. vs sus. plant 4.10 0.050∗ 2.95 0.094 0.49 0.491

Prey effect in controls 9.18 0.013∗ 1.92 0.167 20.13 0.004∗

Males

Full model 1.97 0.121 2.99 0.033∗Plant 1.88 0.175 1.52 0.240

Prey 0.37 0.549 8.05 0.010∗Plant× prey 2.19 0.135 0.95 0.402

Planned comparisons

Plant vs no-plant 3.73 0.065 0.03 0.858

Res. vs sus. plant 0.04 0.853 3.02 0.097

Prey effect in controls 11.42 0.007∗ 8.77 0.017∗∗Indicates comaprisons significant atP < 0.05.Degrees of freedom for comparisons:Development and weight, males: Full model = 5, 23; Plant = 2, 23; Prey = 1, 23; Interaction = 2, 23Development and weight, females: Full model = 5, 37; Plant = 2, 37; Prey = 1, 37; Interaction = 2,37.Fecundity: Full model = 5, 28; Plant = 2, 28; Prey = 1, 28; Interaction = 2, 28.

includensand PI 229358 was selected for use as theresistant plant.

Partitioning effects of resistant plants.Neither plantnor prey treatment affected nabid survival (F = 0.19;df = 5, 23; P = 0.961) (Figure 1). Resistantplants affected predator development and fecunditythrough feeding on prey reared on the resistant plants,but not as a result of direct plant feeding (Table 1).Weight of adult males feeding on resistant prey wassignificantly lower than males feeding on larvae thatdeveloped on the susceptible soybean variety, inde-pendent of plant treatment (Figure 2). Developmenttime of males was not significantly affected by eitherplant or prey treatments across the whole experiment.However, preplanned comparison between prey feed-ing treatments in the no-plant controls only showedthat males feeding on resistant prey took significantlylonger to develop (P = 0.007) (Figure 3).

Figure 1. Percent survival ofN. roseipennisreared onP. includens(fed resistant or susceptible soybean foliage) and soybean (resistantplant, susceptible plant or the no-plant control). Error bars are±SE.

Female weight, development time, and fecunditywere negatively affected by consumption of resistantprey. Adult weight was reduced in females feeding onresistant prey but it was not affected by plant treat-

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Figure 2. Weight of adultN. roseipennisreared onP. includens(fed resistant or susceptible soybean foliage) and soybean (resistantplant, susceptible plant or the no-plant control). Error bars are±SE.

Figure 3. Development time ofN. roseipennisreared onP. inclu-dens(fed resistant and susceptible soybean foliage) and soybean(resistant plant, susceptible plant or the no-plant control). Error barsare±SE.

Figure 4. Fecundity of femaleN. roseipennisreared onP. includens(fed resistant and susceptible soybean foliage) and soybean (resis-tant plant, susceptible plant or the no-plant control). Error bars are±SE.

ments (Figure 2). Development time of females wasaffected by both prey and plant treatments (Table 1).Female development took longer when feeding on ei-ther resistant prey or developing on resistant plantsthan when feeding on susceptible prey and caged on ansusceptible plant (Figure 3). Development of femalestook the longest when feeding on resistant larvae withno plant (Figure 3) possibly indicating that plants(even resistant ones) provided some benefit. Whenplants and prey were both provided, it appeared thatthe effect of plants and prey on female developmentwas additive, since predators that developed on re-sistant prey and resistant plants took the longest tobecome adults while predators fed susceptible larvaeand plants took the shortest time to develop. Predatorsexposed to combinations of resistant and susceptibletreatments developed at intermediate rates. Fecundity(Figure 4) was affected in a similar way as most otherpredator characteristics; prey, but not plant treatment,affected reproduction. The number of eggs laid byN. roseipennisover the first 20 days after becomingadults was reduced by 40 to 51% when feeding onresistant prey.

There was a significant interaction between plantpresence and the prey treatments (F = 6.55; df = 1;P = 0.0147). FemaleN. roseipennisfed suscepti-ble prey developed faster without the presence of asoybean plant and those fed resistant prey developedfaster in the presence of a soybean plant (Figure 3).N.roseipennisdid not benefit from exposure to soybeanplants in other instances.

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Discussion

These results indicate that resistant plants affect thedevelopment of the hemipteran predatorN. roseipen-nis. However, this effect was primarily a three-trophic-level interaction mediated through prey which hadfed on resistant plants. The presence of resistant orsusceptible soybean plants, had little effect on the de-velopment ofN. roseipennis. Only a small negativeeffect of resistant plants on female nabid develop-ment time was observed, with development time offemales being faster on susceptible than on resistantplants. The effect of the resistant plants through preyfeeding was more noticeable. Significant reductionsin adult weight and fecundity, as well as an increasein development time, occurred when predators fedon prey that had fed on the resistant soybean cul-tivar. A 40% reduction in fecundity coupled withdelayed development could dramatically affect nabidpopulations in soybean fields. Nabids consistently areone of the most abundant predatory taxa in soybean(Pfannenstiel & Yeargan, 1998) and are the preda-tors most commonly observed feeding on lepidopteraneggs in soybean in Kentucky (Pfannenstiel, 1995).N.roseipennismay also be responsible for a significantproportion of the mortality of lepidopteran larvae (Mc-Carty et al., 1980). Reductions in nabid densities maylead to increases in populations of lepidopteran pestsin soybeans.

Hemipteran predators use plants as a resource formoisture and possibly for food (Ridgway & Jones,1968; Stoner, 1970, 1972). Direct feeding on plantsmay place these predators at risk of ingesting planttoxins and of being affected by resistant plants in asimilar way as herbivores. However, the degree thathemipteran predators use plants for food and the ef-fect of resistant plants on their development are notwell understood. Most of them, when placed withplants, but no prey, survive for a greater period oftime than when no plant is present. Plant reproductivestructures reported to serve as important food sourcesfor hemipteran predators include seeds (Stoner, 1970,1972), and pollen (Stoner, 1972; Salas-Aguilar &Ehler, 1977; Kiman & Yeargan, 1985). However,seeds removed from their hulls, as used in Stoner(1972) may not normally be available to predatorsbecause of their hard shells. Plant foliage also af-fects development of predaceous hemipterans, but toa lesser degree, and this effect varies among differentstudies (Stoner, 1970, 1972; Naranjo & Stimac, 1985).In the presence of high quality prey, direct effects

of plants on growth and development may be negli-gible or subtle. Plants may be much more importantin the presence of low quality prey, or very low preydensities, than with high quality or abundant prey.

Rogers & Sullivan (1986) studied the impact of re-sistant soybean on the predatorG. punctipes. Whenthe prey,Anticarsia gemmatalisHübner (Lepidoptera:Noctuidae), was reared on artificial diet there wasno effect of plant variety through predators’ feedingdirectly on the plants on growth rate, mortality, de-velopment time, size (head width) or survival of thepredator. However, whenA. gemmataliswas reared onfoliage of the different soybean varieties there weresignificant negative effects of the resistant varieties(through feeding on resistant prey) onG. punctipesgrowth rate, nymphal development time and nymphalmortality. WhenP. includenswas used as the prey,there was an effect of soybean variety on nymphal de-velopment period, but not on mortality or adult headwidth. The largest differences observed were betweentreatments using soybean-reared larvae and diet-rearedlarvae, suggesting that the effects of feeding treat-ments were mediated through the prey. However,this study was not designed to specifically determinethe pathway of the antibiotic effects. Additionally, astudy of the effects of soybeans and various weedson G. punctipesshowed no effect of plant presenceon nymphal development time or fecundity, althoughthere was a small effect on survival and adult size(Naranjo & Stimac, 1985).

In this study, prey quality was more importantfor N. roseipennisthan plant quality. Predaceoushemipterans in the field capture and feed on a diver-sity of prey (Crocker & Whitcomb, 1980; Braman &Yeargan, 1989). The presence of a diverse prey assem-blage, including high quality prey or a prey type (orstage) that does not feed on the resistant plants (e.g.,lepidopteran eggs), may nullify or reduce the effect ofthe resistant prey.

Acknowledgements

We thank H. Ludwig for laboratory assistance. J.Baskin, G. C. Brown, P. L. Cornelius, T. E. Cottrell,K. F. Haynes, A. J. Moore, B. C. Pass, D. A. Potterand A. Sih (all at the University of Kentucky) providedreviews of early drafts of this article. This is publica-tion number 97–08–21 of the University of KentuckyExperiment Station.

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