sign in sign up
<<
Home , Foraging, Lygus hesperus, Predation

BEHAVIOR or ? Field Observations of by hesperus (: )

1 JAY A. ROSENHEIM, RACHEL E. GOERIZ, AND EMILY F. THACHER

Department of Entomology, University of California, Davis, CA 95616

Environ.Entomol.33(5): 1362Ð1370 (2004) ABSTRACT When important agricultural pests are instead of strict , their impact on the plant may change as the omnivore shifts between consumption of plants and consumption of . Lygus hesperus, a key pest of cotton, is known from laboratory and Þeld studies to be an omnivore, but no Þeld studies have ever quantiÞed the importance of as a source of food.Cotton growers have long considered the impact of L. hesperus on cotton to be enigmatic, because sometimes crop damage seems to be higher or lower than would be expected based upon the density of L. hesperus estimated through sweep net samples.Here, we conducted focal observations of L. hesperus foraging freely in the Þeld to quantify the relative importance of predation versus herbivory as food resources and to determine whether omnivory was sufÞciently common that it might underlie the “Lygus enigma.” In observations of 84 individuals over a total of 56.7 h, we did not observe any predation events.Observations conducted in the laboratory under continuous magniÞcation also yielded no evidence of predation, suggesting that we were not failing to detect predation events on small or cryptic prey in the Þeld.Thus, L. hesperus expresses predatory behavior at most very infrequently and develops essentially as an herbivore in California cotton.We did, however, Þnd that adult male L. hesperus spend more of their time resting and spend less time on the vulnerable reproductive structures of the cotton plant compared with nymphal stages or adult females.Further work on the Lygus enigma will examine the differential ease of sampling different L. hesperus stages and the possibility that they contribute unequally to crop damage.

KEY WORDS omnivory, diet selection, selection, direct observations, cotton

OMNIVORY, THE HABIT OF feeding both as a herbivore and et al.1996, Janssen et al.2003) and Lygus a predator, is now recognized to be widespread among (Wheeler 1976, 2001). taxa (Coll and Guershon 2002).This result has It is important for applied insect ecologists to un- been supported by detailed studies (Polis derstand omnivory for at least two reasons.First, when 1991) and by a growing understanding of the natural omnivores function as predators they can be impor- history of some broadly omnivorous taxa, such as the tant as biological control agents.This is especially true Hemiptera (Wheeler 2001, Coll and Guershon 2002). in disturbed or annual agroecosystems, where omni- Furthermore, theoretical work (McCann et al.1998, vores may be able to support themselves on plant- Lalonde et al.1999, Williams and Martinez 2000, van based resources and thereby maintain their popula- Rijn et al.2002) and microcosm experimentation (Fa- tions during periods when the target pest is absent or gan 1997, Holyoak and Sachdev 1998) have over- rare (Karban et al.1994; Walde 1995; Settle et al.1996; turned earlier predictions (May 1973, Pimm 1982) that McMurtry and Croft 1997; Coll 1998; Eubanks and omnivores should destabilize food webs and should Denno 1999, 2000; van Rijn et al.2002).Second, when therefore be rare in nature.In some agricultural eco- omnivores function as herbivores they can be impor- systems, such as cotton, many of the commonest ar- tant as crop pests.The impact of omnivore feeding on thropod taxa are omnivorous.This is true for many the host plant may vary as a function of the availability species that are generally considered to be “beneÞ- of prey, necessitating the use of more com- cials,” including (Jervis et al.1996) and plex decision rules to manage their populations effec- predatory hemipterans (Coll 1998), lacewings (Lim- tively (Alomar and Albajes 1996, Agrawal et al.1999, burg and Rosenheim 2001), and phytoseiids (Mc- Agrawal and Klein 2000; also see Reding et al.2001, Murtry and Croft 1997), and also for some species that Lucas and Alomar 2002).Indeed, some omnivorous are generally considered to be herbivorous “pests,” taxa may switch between functioning as important such as some thrips (Trichilo and Leigh 1986, Wilson biological control agents when prey are abundant and important crop pests when prey are rare or absent 1 Corresponding author: e-mail, [email protected]. (Alomar and Albajes 1996, McGregor et al.2000).

0046-225X/04/1362Ð1370$04.00/0 ᭧ 2004 Entomological Society of America October 2004 ROSENHEIM ET AL.:OMNIVORE OR HERBIVORE? 1363

In this study, our focus is on the expression of lenati, and an adult honey , Apis mellifera L. (J.A.R. omnivory by Lygus hesperus Knight (Hemiptera: Miri- and D.D.Limburg, unpublished data); at least for the dae). L. hesperus is a key pest of several crops in North , the L. hesperus was presumably acting as a America, including cotton, , seed , .Finally, and perhaps most importantly, beans, pome fruits, and some vegetables (Leigh and Hagler and Naranjo (1994) and Naranjo and Hagler Goodell 1996).Although the majority of the literature (1998) concluded that L. hesperus in Arizona cotton describing the and of Lygus spp.has was one of the top two predators of the eggs of the pink focused on their role as herbivores, it has long been bollworm, Pectinophora gossypiella (Saunders), and recognized that Lygus also feed as predators or scav- the sweetpotato whiteßy, Bemisia tabaci (Gennadius). engers of insect carrion (reviewed by Wheeler 1976, Approximately one-quarter of all Þeld-collected 2001).As noted by Wheeler (1976), however, few of nymphal and adult L. hesperus scored positive in gut these studies provide quantitative Þeld data evaluating content immunoassays for having recently (Ͻ1d) the role of Lygus as predators; instead, the majority of consumed one of these prey.Thus, L. hesperus in the Þeld studies simply report casual observations of Arizona cotton seems to express predation on a level predation by Lygus spp.Perhaps most importantly, roughly similar to, and in some cases exceeding, other few studies have quantiÞed the contribution of pre- taxa that are widely recognized as important generalist dation to the total diet of Lygus. predator biological control agents, including O. tris- Producers and pest management specialists working ticolor, spp., Nabis spp., and Z. renardii. Such in California cotton have for many years discussed a strong expression of omnivory by L. hesperus would informally an “enigma” that surrounds the manage- suggest that the impact of L. hesperus on cotton might ment of L. hesperus: the relationship between the be modulated by the availability of arthropod prey as perceived density of L. hesperus and crop damage an alternate food .Such a potential for a (abscission of ßower buds, called “squares”) seems to shifting impact on the host plant would be important be highly variable.Some Þelds in which the standard for L. hesperus management decisions. sweep-net sampling produces high counts of L. hes- Studies of the battery of enzymes produced by L. perus sustain little damage, whereas other Þelds with hesperus have provided further support for the view much lower counts of L. hesperus sustain heavy dam- that they function as omnivores.Cohen (1996) age.This enigmatic observation has never been stud- showed that L. hesperus produces and phos- ied scientiÞcally, and indeed the few studies relating pholipase A2, an enzyme that indicates an advanced L. hesperus density to crop damage do not suggest that state of to predation.Agusti and Cohen the enigma is real; instead L. hesperus density and crop (2000) and Zeng and Cohen (2000, 2001) studied a damage can be strongly correlated (Leigh et al.1988). long-term laboratory colony of L. hesperus originally Nevertheless, the perception of a Lygus enigma per- derived from Arizona (A.C.Cohen, personal com- sists in the grower .One goal of our study munication), and reported enzymatic activity proÞles was to examine the possibility that a highly omnivo- that were generally consistent with an omnivorous rous L. hesperus population might be switching be- diet, although hyaluronidase activity, which is partic- tween plant and prey feeding, creating hard-to-pre- ularly characteristic of predatory taxa, was not de- dict swings in the intensity of their impact on the host tected. plant. The goal of our study was to quantify the foraging A series of Þeld studies conducted in California and behavior, microhabitat use, and diet of L. hesperus Arizona created an expectation that the L. hesperus foraging naturally in upland cotton, hirsu- populations that we studied in California cotton would tum L., grown in the San Joaquin Valley of California. indeed function as omnivores.First, Eveleens et al. Because we wanted to deÞne the range of prey con- (1973) studied predation on Spodoptera exigua (Hu¨ b- sumed by L. hesperus, we used focal observations.Our ner) in California cotton by using outplanted egg most fundamental question was, How frequently does masses.They reported that L. hesperus was observed L. hesperus act as a predator of other several times feeding on egg masses, although it was a present in cotton? To address the possibility that pre- minor predator compared with the hemipteran pred- dation events on very small prey (e.g., eggs of ators Geocoris pallens Ståhl, Orius tristicolor (White), or whiteßies) might be missed in some Þeld Nabis americoferus Carayon, and the lacewing Chry- observations, we also conducted laboratory observa- soperla carnea Stephens.Second, in a similar study, tions of foraging by L. hesperus under continuous ste- Bisabri-Ershadi and Ehler (1981) examined predation reomicroscopic magniÞcation. on Spodoptera praefica (Grote) eggs in California al- falfa Þelds and again observed L. hesperus attacking Materials and Methods eggs, although they expressed uncertainty regarding how important it might be relative to what they con- Field Observations. Focal observations of individ- sidered to be the “major” predators O. tristicolor, Geo- ual Lygus (N ϭ 84) were conducted from June through coris spp., and Nabis spp.Third, observations made September 2001 on upland cotton in the southern San during whole-plant searches of cotton plants in the Joaquin Valley.California cotton Þelds can harbor San Joaquin Valley of California revealed instances of both L. hesperus and the generally much less common L. hesperus acting as a predator of a coccinellid larva, Lygus elisus Van Duzee (Sevacherian and Stern 1972). a coccinellid , an egg mass of Zelus renardii Ko- Although the nymphal stages and adult females of 1364 ENVIRONMENTAL ENTOMOLOGY Vol.33, no.5 these species are difÞcult to distinguish deÞnitively, net, were conducted, and Lygus spp.nymphs and male L. hesperus can be readily distinguished from adults were counted in the Þeld.A leaf sample, com- male L. elisus by using a combination of the following prising 50 leaves collected from the Þfth mainstem characters: dark lines or spots on the propleuron, black node from the top of the plant, was taken to quantify pigment in the wing membrane, and the rostrum ex- the densities of the dominant herbivores cotton , tending beyond the hind coxae (Mueller et al.2003). Aphis gossypii Glover; spider mites, Tetranychus spp.; Using these characters, 14 of the 14 males that we and western ßower thrips, Frankliniella occidentalis observed and collected were assigned to L. hesperus. (Pergande).The leaves were stored in 70% ethanol We suggest, therefore, that our results apply to L. until they were processed in the laboratory by hand- hesperus, although a small number of L. elisus also may washing them over a Þne sieve (75 by 75-␮m open- have been observed. ings) to extract the foliar arthropods.The arthropods Observations were made during daylight hours were stored in 70% ethanol and identiÞed and counted only.Fields, including seven commercial plantings using a stereomicroscope.A second leaf sample com- and two smaller plantings at experimental stations, prising an additional twenty leaves taken from the Þfth were chosen on the basis that they supported popu- mainstem node was taken to quantify the density of lations of L. hesperus and had not received whiteßy nymphs.These leaves were kept cool and applications for 3 wk before the observations.Indi- examined in the laboratory within 48 h to count and vidual L. hesperus were chosen for observation by identify whiteßy nymphs.To quantify the predator walking slowly though the Þeld inspecting all visible community, whole plant searches (N ϭ 10 plants) portions of the cotton plants for any L. hesperus stage. were conducted.The plants were chosen randomly The aim was to observe equal numbers of nymphs, and cut below their cotyledonary scars and then car- adult males, and adult females at each site; however, ried to the edge of the Þeld where all plant parts were spatial and temporal variation in the age structure and inspected to count immature and adult predators. ratio of Lygus populations, and in particular the Laboratory Observations. Laboratory observations difÞculty of Þnding L. hesperus nymphs early in the were conducted in early October 2001 on Þeld-col- growing season, often made this impossible to achieve. lected nymphal (N ϭ 10) and adult (N ϭ 18) L. Observers worked in teams of two and attempted to hesperus foraging on individual cotton leaves.The L. record continuously the behavior of an individual L. hesperus and cotton leaves were collected from cotton hesperus over the course of an hour.One person Þelds in the San Joaquin Valley supporting populations watched the L. hesperus and the other person re- of whiteßies or that had not received pesticide corded data on a hand-held computer (Psion Orga- treatments in the previous 3 wk. L. hesperus were nizer II, Psion PLC, London, United Kingdom) oper- collected with a sweep net and stored in a cooler or ating behavioral event recording software (The refrigerator.The top Þve nodes of cotton plants were Observer 3.0, Noldus Information b.v., cut and stored with their stems in water in the labo- Wageningen, The Netherlands).By minimizing our ratory.Both the and the plant material were movements during an observation period, we were used within 24 h of collection. able to avoid disturbing the focal L. hesperus. Although Individual L. hesperus were observed continuously the goal was to observe individual insects for an hour, under a stereomicroscope for1hbyconÞning them in this was not always possible because some individuals an arena created by afÞxing half of a petri dish (3.5 cm were lost in ßight.Continuous recordings were made in diameter) to the undersurface of a cotton leaf with of 1) the plant part on which the L. hesperus was an adhesive putty (Tac ÔN Stik, ElmerÕs Products, Co- present (top of leaf, bottom of leaf, petiole, stem, lumbus, OH).We placed the arenas over portions of growing tip of plant, square, ßower, and boll); 2) L. the leaves that harbored high concentrations of po- hesperus activity (rest, walk, and feed); 3) the identity tential prey for L. hesperus (aphids and whiteßies) and of food items consumed or probed (including plant generally excluded extraßoral nectaries.The arena parts and arthropod prey); and 4) any contacts with was mounted on a small plate that was then placed on other arthropods (natural enemies or prey).Feeding top of a small mass of putty so that it could be tilted was recorded if the individual remained still with its to provide the best lateral view of the mouthparts of stylets inserted into the substrate ( and Backus the foraging bug. L. hesperus were allowed to accli- 2002).When possible, L. hesperus were collected after mate to the foraging arena for 30 min before obser- being observed to determine their nymphal stage and, vations were begun.We used the same hardware and for adults, their sex. software as described above for the Þeld observations Our initial expectation was that L. hesperus behavior to record behavioral data, but the magniÞed view of might be inßuenced by the plant growth stage or by Lygus behavior allowed us to distinguish a few addi- the resident community of arthropods.At each site, tional behavioral categories.Thus, we recorded L. we therefore measured the number of mainstem hesperus activity (resting, walking, probing, grooming, nodes for each of 10 plants and sampled the arthropod and feeding) and identity of food items probed or community by using three sampling techniques: consumed (leaf blade, leaf vein, extraßoral nectary, sweep netting, leaf samples, and whole-plant visual aphids, and whiteßies).We paid special attention to searches.Ten sweep-net samples, each sample com- the details of the feeding behavior of the L. hesperus. prising 50 sweeps across the upper canopy of a single A “contact” was recorded when the L. hesperus row of cotton with a standard 38-cm-diameter canvas touched another arthropod. “Probing” was recorded if October 2004 ROSENHEIM ET AL.:OMNIVORE OR HERBIVORE? 1365

L. hesperus contacted a potential prey with its beak. “Feeding” was recorded if we observed the beak to e pierce the substrate and stay there for Ͼ5 s.After the observation, all stages of all arthropods in the foraging Lygus sample arena were counted. density/sweep Data Analysis. The unit of replication for our anal- ysis of L. hesperus behavior in the Þeld was the indi- vidual bug observed; thus, each focal observation con- d tributed a single datum to our Þnal data set.Four 1.0 3.8 0.6 1.9 2.5 0.6 0.5 0 2.0 1.5 2.8 7.7 0.6 1.1 1.9 0.70.51.2 1.8 0.2 4.4 3.3 0.3 3.1 1.41.0 1.5 2.4 5.4 7.7 observations were excluded because they were Ͻ1 Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ min.Nonparametric Wilcoxon/KruskalÐWallis tests

Predator were used to determine whether nymphs, adult males, density/plant and adult females differed in plant substrates used, activity budget, or feeding preferences.All summary statistics are presented as the means Ϯ 1 SE. c Results Field Observations. We observed L. hesperus (N ϭ 84; total observation time 56.7 h) under Þeld condi- tions that varied with respect to the growth stage of 1.0 0.2 0.3 4.3 0.4 20.7 1.7 12.3 0.1 0.2 0.4 2.6 0.1 0.4 1.1 11.5 0.2 0.2 0.3 2.9 0.1 0.1 0.2 3.8 were conducted Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ the plant and the densities of potential herbivore prey, Lygus spp., and potential predators of Lygus (Table 1).

Herbivore densities/leaf Contrary to our expectations, which were shaped by an extensive literature describing Lygus spp.as om- L. hesperus nivores, we never observed L. hesperus to attack or consume any arthropod prey.Thus, our observations suggest that L. hesperus functions predominantly as a herbivore in California cotton and that any predatory b 0.6 3.4 6.4 0.7 2.4 1.3 0.7 2.5 0.1 0.7 20.0 0.1 0.40.60.4 1.5 1.9 13.0 0 1.0 0 0 0 1.8 1.2 1.5 2.8 0.50.6 0.6 0.7 0.4 0 0 1.0 4.6 0.3 0.4 0 0.4 0.6activity 7.3 that might be expressed was too infrequent to Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ be detected by our sampling. nodes

mainstem Although none of our Þeld sites harbored outbreak Cotton plant

10 plants searched per site). densities of herbivores, the Lygus we observed did

ϭ have opportunities to interact with potential prey, N because our Þeld sites supported signiÞcant popula- tions of key cotton herbivores (Table 1).We observed 10), each of which comprised Þfty sweeps. Total

ϭ L. hesperus to make physical contact with different time (h) observation N arthropods (aphids, whiteßies, and thrips), but in each case these contacts seemed to occur strictly acciden- tally as L. hesperus moved across the plant surface.For a example, we often observed L. hesperus walking while

) derived from a sample of 50 leaves collected from the Þfth mainstem node.Whiteßy counts are for nymphal stages of sweetpotato whiteßy periodically touching the plant substrate with the tip of their beaks; in a few cases, L. hesperus engaged in observed this activity placed their beaks on tops of aphids.Nev- 20 randomly selected plants. ertheless, this contact did not result in arrestment of Lygus ϭ F. occidentalis N L. hesperus or the initiation of an attack.We never No. observed L. hesperus respond to any arthropod with N M F unkpredatory Aphids Whiteßies behavior Mites Thrips (e.g., stalking and Nymphs striking); Adults in- 1SEfor

spp.counted per sweep net sample ( stead, the L. hesperus either ignored the arthropods or Ϯ retreated upon contact.On two occasions we saw Z.

Lygus renardii stalking our focal L. hesperus, but no attacks were recorded. Although we did not see L. hesperus feed as pred- ators, we did observe extensive feeding on plant sub- strates, and different stages of L. hesperus showed differences in feeding and other behaviors (Tables 2 and 3).Adult males spent a signiÞcantly greater pro- portion of their time resting than did adult females (␹2 ϭ 5.1, P ϭ 0.02; Table 2), but males and females both Mainstem node counts are means F, adult females; M, adult males; N, nymphs; unk, adults of unknown sex. Mean no.predators per whole cotton plant, as measured by whole plant searches ( Mean no.nymphal and adult Counts of aphids, mites, and thrips (primarily

Table 1. Descriptive data for cotton field sites in California’s San Joaquin Valley where focal observations of fed on a similar array of plant substrates, including a b c d e Field site (county) Dates (2001) Jones 4 (Kings) 20Ð26 Sept. 9 4 5 0 14.30 22.8 Jones 9 (Kings) 11Ð13 Sep 7 3 2 0 9.16 24.0 Sheely 6Ð4 (Fresno) 4Ð6 Sept. 2 2 6 0 9.77 18.0 Newton 6 (Kings) 22Ð24 Aug. 2 6 2 2 8.59 21.5 Sheely 6Ð3 (Fresno)Sheely 8Ð1 (Fresno)Shafter 43 (Kern) 2 Aug. 3 Aug. 16 Aug. 0 3 4 0 3 2 0 1 2 1 0 1 1.76 5.03 2.60 17.3 18.7 19.5 Sheely 32 (Fresno)Shafter 43 (Kern) 24 July 25 July 0 0 0 0 0 0 11 2 3.92 0.98 17.5 17.9 Westside (Fresno) 23 July 1 0 0 1 0.59 18.7 found on 20 leaves collected from the Þfth mainstem node. vegetative and reproductive plant structures, and also 1366 ENVIRONMENTAL ENTOMOLOGY Vol.33, no.5

Table 2. Activity budget of L. hesperus observed in the field on ent-rich plant foods (fruiting structures), whereas upland cotton males were primarily engaged in searching for recep- Nymphs Adult males Adult females tive females. (N ϭ 24) (N ϭ 22) (N ϭ 20) Laboratory Observations. To address the possibility Rest 74.69 Ϯ 4.27a 75.65 Ϯ 4.52a 58.76 Ϯ 5.58b that we were failing to detect L. hesperus predation on Walk 12.95 Ϯ 2.21a 16.01 Ϯ 2.68a 21.37 Ϯ 4.34a small or cryptic arthropod prey in the Þeld, we ob- Feed 10.78 Ϯ 3.95a 7.65 Ϯ 2.66a 18.15 Ϯ 5.07a served Þeld-collected L. hesperus (10 nymphs, nine adult males, and nine adult females) under continuous Data (mean Ϯ 1 SE) represent percentages of time engaged in resting, walking, or feeding.Means within a row followed by different magniÞcation in the laboratory for a period of 1 h.To letters indicate signiÞcant differences (P Ͻ 0.05, Wilcoxon/KruskalÐ ensure that frequent encounters would occur be- Wallis test). tween L. hesperus and potential prey, we selected cotton leaves harboring large populations of aphids Ϯ Ϯ imbibed extraßoral (Table 3).Nymphs were (20.1 6.3 per enclosure) and whiteßy eggs (194.3 not observed feeding on extraßoral nectar, but oth- 79.1 per enclosure). Whiteßy crawlers, nymphs, and erwise they showed a pattern of feeding similar to that pupae were also present (6.9 Ϯ 2.2 per enclosure). observed for adults.We emphasize, however, that our Despite frequent contacts between L. hesperus and sampling likely underestimated nymphal feeding on whiteßy eggs, L. hesperus were not observed probing squares and young bolls, because nymphs often hid or feeding on any stage of whiteßy.Frequent encoun- under the bracts that subtended squares and bolls, ters also were observed between L. hesperus and making it very difÞcult for us to determine whether aphids (N ϭ 21). Lygus responded to the majority of they were feeding or simply resting.Because we only these contacts (16/21 ϭ 76%) by retreating.The re- recorded feeding when we could see the beak in maining Þve L. hesperusÐaphid contacts comprised contact with the plant substrate, we probably overes- one case where the L. hesperus showed no response, timated resting and underestimated feeding by one case where the L. hesperus touched the aphid with nymphs. its beak but did not pierce it, and three cases where the Different stages of L. hesperus allocated their time L. hesperus probed, punctured, and killed the aphid, dissimilarly to microhabitats within the cotton plant but then immediately retreated without feeding.Thus, (Table 4).Adult females and especially adult males in no case did we observe L. hesperus to consume an spent more time on the upper surfaces of leaves than aphid.In two cases, we also observed L. hesperus to did nymphs (␹2 ϭ 19.5, P Ͻ 0.0001). Males, in partic- probe dead aphids and then retreat without feeding. ular, were often observed resting at the upwind edges of leaves in the very top of the plant canopy, with their We did observe L. hesperus feeding on the cotton antennae extended upward and over the edge of the leaf while conÞned in our laboratory arenas: L. hes- leaf.We speculate that these males were sampling the perus fed on the leaf blade and veins and took meals for pheromone plumes produced by calling fe- from the foliar extraßoral nectary. L. hesperus engaged Ϯ males.Adult females and nymphs were not observed in 1.8 0.6 feeding bouts per hour and spent a total Ϯ to exhibit this distinctive behavior.Adult males also of 6.6 2.2 min feeding per hour of observation. Thus, spent signiÞcantly less time on fruiting structures than although L. hesperus did feed on the cotton leaf in the did either adult females or nymphs (␹2 ϭ 12.6, P ϭ laboratory, and although we did observe some will- 0.002). The overall pattern of microhabitat use is con- ingness to probe at least one herbivore (the cotton sistent with the interpretation that nymphs and adult aphid), we again produced no evidence of consump- females were primarily engaged in feeding on nutri- tion of prey by L. hesperus.

Table 3. Percentage of total feeding time allocated by L. hesperus to different plant substrates on upland cotton

Nymph Male Female (N ϭ 15) (N ϭ 12) (N ϭ 15) Vegetative parts 61.68 Ϯ 12.46a 48.84 Ϯ 13.04a 45.48 Ϯ 10.70a Top of leaf 11.94 Ϯ 8.20 6.31 Ϯ 4.10 3.88 Ϯ 3.50 Bottom of leaf 23.20 Ϯ 10.49 4.06 Ϯ 3.09 16.14 Ϯ 9.22 Petiole 4.66 Ϯ 4.01 26.96 Ϯ 10.19 1.82 Ϯ 1.34 Stem 7.64 Ϯ 3.95 4.72 Ϯ 4.72 5.37 Ϯ 5.37 Tip of plant 10.68 Ϯ 7.34 11.26 Ϯ 7.71 5.39 Ϯ 2.92 Vegetative bud 3.56 Ϯ 3.56 5.53 Ϯ 3.71 12.87 Ϯ 8.18 Reproductive parts 38.36 Ϯ 12.46a 32.14 Ϯ 12.40a 41.32 Ϯ 11.03a Square 18.22 Ϯ 9.67 19.75 Ϯ 9.96 19.52 Ϯ 8.94 Flower 13.43 Ϯ 9.08 10.20 Ϯ 8.26 15.14 Ϯ 8.25 Boll 6.67 Ϯ 6.67 2.19 Ϯ 2.19 6.67 Ϯ 6.67 Nectaries 0 a 9.01 Ϯ 8.30ab 13.20 Ϯ 5.42b Foliar nectary 0 0.68 Ϯ 0.68 3.88 Ϯ 3.05 Circumbracteal nectary 0 8.33 Ϯ 8.33 6.96 Ϯ 4.65 Subbracteal nectary 0 0 2.35 Ϯ 2.35

Means Ϯ 1 SE within a row followed by different letters indicate signiÞcant differences (P Ͻ 0.05, Wilcoxon/KruskalÐWallis test). October 2004 ROSENHEIM ET AL.:OMNIVORE OR HERBIVORE? 1367

Table 4. Percentage of total time spent by L. hesperus on different plant substrates on upland cotton

Nymph Male Female (N ϭ 24) (N ϭ 22) (N ϭ 20) Top of leaf 8.16 Ϯ 2.78a 48.40 Ϯ 7.85b 28.17 Ϯ 6.39b Other vegetative structures 55.20 Ϯ 8.41a 41.81 Ϯ 7.17a 34.44 Ϯ 6.32a Bottom of leaf 25.96 Ϯ 6.33 17.44 Ϯ 6.09 17.62 Ϯ 5.60 Petiole 18.07 Ϯ 5.58 9.27 Ϯ 2.82 9.07 Ϯ 2.91 Stem 7.52 Ϯ 2.51 8.05 Ϯ 4.41 4.61 Ϯ 2.37 Tip 3.70 Ϯ 2.54 7.05 Ϯ 3.89 3.15 Ϯ 1.97 Fruit 36.61 Ϯ 9.11a 9.73 Ϯ 3.79b 37.28 Ϯ 8.14a Square 11.53 Ϯ 5.61 3.41 Ϯ 1.75 16.68 Ϯ 5.85 Flower 12.53 Ϯ 6.87 0.70 Ϯ 0.44 12.85 Ϯ 6.99 Boll 12.58 Ϯ 6.89 5.61 Ϯ 3.59 7.76 Ϯ 4.94

Means Ϯ 1 SE within a row followed by different letters indicate signiÞcant differences (P Ͻ 0.05, Wilcoxon/KruskalÐWallis test).

Discussion cotton simply as a potential pest, rather than as an insect that might also contribute signiÞcantly to bio- We knew at the outset of our study that L. hesperus, logical control of other herbivores in the community. like other Lygus spp., is an omnivore, consuming both Our focal observations also demonstrated some- plant-based foods and arthropod prey.Omnivory in L. thing that is unremarkable but nonetheless important hesperus has been documented in both the laboratory and Þeld (reviewed by Wheeler 1976, 2001), including and as yet unrecognized in the development of sam- Þeld studies conducted in California cotton and alfalfa pling or management plans for L. hesperus: nymphs, (Eveleens et al.1973, Bisabri-Ershadi and Ehler 1981). adult males, and adult females exhibit different be- Our own informal observations made over several haviors (Tables 2Ð4).Nymphs and females spend sub- years of work in California cotton support this con- stantially more time on reproductive structures of the clusion (J.A.R.andD.D.Limburg, unpublished data). cotton plants (squares, ßowers, and bolls), where the What had not been established, however, was the economically damaging feeding occurs, whereas adult frequency with which L. hesperus consume prey rel- males spend more time on the top of leaves, presum- ative to the frequency with which they engage in ably searching for receptive females.This simple re- herbivory.We have demonstrated in this study that L. sult, coupled with recent research on L. hesperus in hesperus in California cotton acts as a predator only Arizona cotton reported by Ellsworth (2000) and Ells- very infrequently, so infrequently that we recorded worth and Barkley (2003), suggesting that nymphal zero predation events in focal observations of 84 L. stages may be particularly important in generating hesperus individuals conducted over a 56.7-h period. crop damage, has refocused our attempts to explain This result does not seem to be an artifact of failing to the Lygus enigma on the role of L. hesperus stage- detect predation on small, cryptic prey: laboratory speciÞc behavior. observations made under continuous magniÞcation Reconciling Studies on L. hesperus Feeding Biol- also produced no evidence of predatory activity. ogy. How can we reconcile our primary result that L. This result is important for two reasons.First, it hesperus functions almost exclusively as an herbivore suggests that the impact of L. hesperus on its cotton with previous reports by Hagler and Naranjo (1994) host plant is unlikely to be modulated strongly by the and Naranjo and Hagler (1998) that L. hesperus is a availability of arthropod prey as alternate food re- major predator of pink bollworm and sweetpotato sources.Thus, the enigmatic observation of a highly whiteßy eggs, on a par with the important biological variable relationship between the perceived density of control agents O. tristicolor, Geocoris spp., and Nabis L. hesperus and crop damage does not seem to be spp.? Although Arizona and California populations of caused by L. hesperus omnivory.It may simply be that L. hesperus have access to different suites of potential what seems to be the preferred prey of L. hesperus, prey, Arizona L. hesperus have been shown to be major eggs of (Wheeler 1976, 2001) or nymphs predators of sweetpotato whiteßy eggs (Hagler and of whiteßies (Hagler et al.2004), are so rare in typical Naranjo 1994, Naranjo and Hagler 1998) and nymphs commercial cotton Þelds during the mid-season that L. (Hagler et al.2004), whereas California L. hesperus hesperus rarely express their predatory habit.Lepi- given access to the same stages of sweetpotato white- dopteran eggs were sufÞciently rare that they were ßy in both the Þeld and the laboratory did not express never detected in any of our samples of cotton leaves. any predatory behavior.We will address Þve nonmu- Whiteßies, including B. tabaci and the greenhouse tually exclusive possibilities for these divergent ob- whiteßy, Trialeurodes vaporariorum (Westwood), can servations, beginning with the one that we think is be important pests in California cotton, but generally most likely. only build to high densities late in the season, when First, it is possible that Arizona and California L. the cotton crop is no longer sensitive to L. hesperus hesperus are fundamentally similar, and express dif- damage (University of California 1996).Second, the ferent amounts of predatory behavior because they almost strict status of L. hesperus as an herbivore sug- are foraging in environments that differ substantially gests that we can manage L. hesperus in California in the density of suitable prey.The pink bollworm is 1368 ENVIRONMENTAL ENTOMOLOGY Vol.33, no.5 not established in CaliforniaÕs San Joaquin Valley conducted during daylight hours only.Given that Ly- (University of California 1996), and thus this major gus spp.are active both during the day and night, prey item is absent; as discussed above, other eggs of might L. hesperus be acting as a predator primarily (or Lepidoptera are generally only found in California at exclusively) at night? This “Dr.Jekyll and Mr.Hyde ” low densities.Although whiteßies are often present in hypothesis seemed to receive support in a recent study mid-season cotton, and they were present at our study of Lygus lineolaris (Palisot de Beauvois) by Pfannen- sites, they generally do not reach high densities until stiel and Yeargan (2002).These authors reported that the late summer or fall, after the cotton crop is no L. lineolaris and other “minor” predators of Helicov- longer sensitive to damage by L. hesperus. The Þelds erpa zea (Boddie) eggs in soybean and corn were that we sampled never harbored high densities of active as predators only nocturnally.However, they whiteßy nymphs (Table 1).Although our laboratory present data for these minor predators treated as a trials did use higher densities of whiteßy eggs and group, and when the data for L. lineolaris are viewed nymphs (nearly 200 eggs and seven nymphs on aver- in isolation there is no trend toward nocturnal pre- age per 3.5-cm-diameter circular enclosure), these dation: approximately equal sampling intensity during densities are still very low compared with those used the day and night revealed eight predation events in the laboratory studies reported by Hagler et al. during the day and six during the night (R.S.Pfan- (2004) (837 eggs, 704 nymphs, and 43 adults on aver- nenstiel, personal communication).Furthermore, age per 3.5-cm-diameter circular enclosure). To pro- previous Þeld studies of L. hesperus have documented vide a preliminary evaluation of whether California L. predation during daylight hours (Eveleens et al.1973; hesperus would express levels of predation typical of Bisabri-Ershadi and Ehler 1981; J.A.R.andD.D.Lim- Arizona populations, we sent L. hesperus collected in burg, unpublished data), and we are unaware of any Fresno County during September 2003 to James R. omnivores that shift between predation and herbivory Hagler, who tested them using the same assay proce- on a diel cycle.Thus, current evidence supports the dures and similarly high whiteßy densities (764 eggs, interpretation that California L. hesperus act as pred- 279 nymphs, and 50 adults on average per 3.5-cm- ators only infrequently, but not only at night. diameter circular arena) as reported in Hagler et al. A fourth possibility is that our observations of L. (2004).Four California L. hesperus were observed for hesperus were problematical in other ways.They may a total of 2 h, yielding a total of 60 plant feeding events have been too short or too intrusive to document and eight predation events (six on nymphs and two on predation adequately.Although we cannot rule out adults; J.R.Hagler, personal communication).These this possibility, it seems unlikely given our success in predation rates are very similar to those reported in quantifying predation and herbivory by other omniv- Hagler et al. (2004) (e.g., they report an average of 2.4 orous predators in cotton, including O. tristicolor, Geo- nymphs preyed upon per hour).Although preliminary coris spp., Nabis spp., and Z. renardii, by using the same in nature, these observations are consistent with the techniques that we used here (Cisneros and Rosen- interpretation that California and Arizona populations heim 1998; Rosenheim et al.1999; J.A.R.andD.D. of L. hesperus have similar underlying potentials to act Limburg, unpublished data).Focal observations re- as predators, with Arizona populations expressing this vealed 33 predation events by O. tristicolor (over potential more often because of their much more 69.4-h total observation time), 24 predation events by frequent encounters with prey. Geocoris spp.(over 75.1h), 18 predation events by Second, it is possible that intraspeciÞc genetic vari- Nabis spp.(over 66.0h), and 34 predation events by ation exists for the expression of omnivory by L. hes- Z. renardii (over 78.3 h) (J.A.R. and D. D. Limburg, perus. That is, Arizona populations may be closer to unpublished data).We emphasize that Hagler and the “predator end” of the omnivory spectrum and Naranjo(1994) and Naranjo and Hagler (1998) con- California (San Joaquin Valley) populations may be cluded that predation by L. hesperus was on a par with closer to the “herbivore end.” Although we are aware exactly these hemipterans in their Arizona cotton of no studies speciÞcally quantifying intraspeciÞc ge- Þelds.Clearly, populations of L. hesperus in California netic variation in the expression of predation by om- cotton do not exhibit predation to the same extent as nivores, genetic variation in food resource use is cer- these other hemipterans. tainly widespread in insect taxa (Futuyma and Finally, given that it is enzyme-linked immunosor- Peterson 1985).However, the preliminary data just bent assay-based gut assays of L. hesperus that have discussed (J.R.Hagler, personal communication) are suggested a major predatory role for a Lygus species in not consistent with the hypothesis that California L. Arizona cotton Þelds, it is possible that any of the hesperus populations are fundamentally restricted to various interpretational problems associated with this an herbivorous lifestyle.A side by side comparison of method of quantifying predation may be operating Arizona-derived and California-derived L. hesperus (reviewed by Hagler et al.1992, Naranjo and Hagler populations in a controlled experimental setting 1998).Nevertheless, Arizona populations of L. hespe- would offer the most deÞnitive means of testing this rus show high levels of predatory activity in petri dish hypothesis. assays when conÞned with sweetpotato whiteßy A third hypothesis to explain the apparent discrep- nymphs (Hagler et al.2004), and as discussed above, ancy between our results and those of Hagler and preliminary data for L. hesperus collected from Cali- Naranjo (1994) and Naranjo and Hagler (1998) con- fornia cotton suggest that they express a similar level cerns a limitation of our study: our observations were of predation when given access to the extremely high October 2004 ROSENHEIM ET AL.:OMNIVORE OR HERBIVORE? 1369 whiteßy densities that characterize some Arizona cot- tory and integrated pest management.Thomas Say Pub- ton Þelds (J.Hagler, personal communication).Thus, lications in Entomology.Entomological Society of Amer- L. hesperus may express an almost purely herbivorous ica, Lanham, MD. feeding habit in California cotton simply because they Coll, M. 1998. Living and feeding on plants in predatory rarely encounter highly preferred prey (e.g., lepidop- Heteroptera, pp.89Ð129. In M.Coll and J.R.Ruberson teran eggs) and require extremely high encounter [eds.], Predatory Heteroptera: their ecology and use in rates with less preferred prey (e.g., whiteßy nymphs) biological control.Thomas Say Publications in.Entomol- ogy.Entomological Society of America, Lanham, MD. before they will act frequently as predators. Coll, M., and M. Guershon. 2002. Omnivory in terrestrial arthropods: mixing plant and prey diets.Annu.Rev.En- Acknowledgments tomol.47: 267Ð297. Ellsworth, P. C. 2000. Lygus control decision aids for Ari- We thank Erin Duffy, Jillian Hodgen, Matthew Judd, and zona cotton, pp.269Ð280. In J.C.Silvertooth [ed.],Cot- Michael Kabler for Þeld assistance.We thank James R.Hagler ton, a College of Agriculture Report.Series P-121.Publ. for conducting the preliminary feeding trials for California L. No.AZ1170.University of Arizona, College of Agricul- hesperus exposed to the high whiteßy densities sometimes ture, Tucson, AZ. http:// cals.arizona.edu /crops/cotton/ observed in Arizona cotton.We also thank the many pro- insects/lygus/lyg00cr.pdf. ducers and California advisors who granted Ellsworth, P. C., and V. Barkley. 2003. Making late season permission to conduct Þeldwork.We thank Allen Cohen, decisions to terminate use against Lygus, pp. Peter Ellsworth, James Hagler, Larry Godfrey, Peter Goodell, 204Ð217. In J.C.Silvertooth [ed.],Cotton, A College of Shannon Mueller, Robert Pfannenstiel, and Charles Sum- Agriculture and Life Sciences Report.Publ.No.AZ1312. mers for helpful discussions on Lygus biology, clariÞcations University of Arizona, College of Agriculture and Life of published studies, and sharing of preprints or unpublished Sciences, Tucson, AZ. http://cals.arizona.edu/pubs/ data.Jason Harmon and Steve Naranjo made constructive crops/az1312/az13125c.pdf. comments on an earlier draft of this article.This work was Eubanks, M. D., and R. F. Denno. 1999. The ecological supported by grants from the California State Support Board consequences of variation in plants and prey for an om- of Cotton Incorporated and the University of California nivorous insect.Ecology 80: 1253Ð1266. Statewide Integrated Pest Management program. Eubanks, M. D., and R. F. Denno. 2000. Host plants mediate omnivore-herbivore interactions and inßuence prey sup- References Cited pression.Ecology 81: 936Ð947. Eveleens, K. G., R. Van Den Bosch, and L. E. Ehler. 1973. Agrawal, A. A., and C. N. Klein. 2000. What omnivores eat: Secondary outbreak induction of beet armyworm by ex- direct effects of induced plant on herbivores perimental insecticide applications in cotton in Califor- and indirect consequences for diet selection by omni- nia.Environ.Entomol.2: 497Ð503. vores.J.Anim.Ecol.69: 525Ð535. Fagan, W. F. 1997. Omnivory as a stabilizing feature of nat- Agrawal, A. A., C. Kobayashi, and J. S. Thaler. 1999. Inßu- ural .Am.Nat.150: 554Ð567. ence of prey availability and induced host-plant resis- Futuyma, D. J., and S. C. Peterson. 1985. Genetic variation tance on omnivory by western ßower thrips.Ecology 80: in the use of resources by insects.Annu.Rev.Entomol.30: 518Ð523. 217Ð238. Agusti, N., and A. C. Cohen. 2000. Lygus hesperus and Lygus Hagler, J. R., A. C. Cohen, D. Bradley-Dunlop, and F. J. lineolaris (Hemiptera: Miridae), phytophages, zooph- Enriquez. 1992. Field evaluation of predation on Lygus ages, or omnivores: evidence of feeding sug- hesperus (Hemiptera: Miridae) using a species- and stage- gested by the salivary and midgut digestive enzymes.J. speciÞc monoclonal antibody.Environ.Entomol.21: 896Ð Entomol.Sci.35: 176Ð186. 900. Alomar, O., and R. Albajes. 1996. Greenhouse whiteßy (Ho- Hagler, J. R., and S. E. Naranjo. 1994. Determining the fre- moptera: Aleyrodidae) predation and tomato fruit injury quency of heteropteran predation on sweetpotato white- by the zoophytophagous predator Dicyphus tamaninii ßy and pink bollworm using multiple ELISAs.Entomol. (Heteroptera: Miridae), pp.155Ð177. In O.Alomar and Exp.Appl.72: 59Ð66. R.N.Wiedenmann [eds.],Zoophytophagous Heterop- Hagler, J. R., C. G. Jackson, R. Isaacs, and S. A. Machtley. tera: implications for life history and integrated pest man- 2004. Foraging behavior and prey interactions by a agement.Thomas Say Publications in Entomology.En- tomological Society of America, Lanham, MD. of predators of various lifestages of Bemisia tabaci. J.In- Bisabri-Ershadi, B., and L. E. Ehler. 1981. Natural biological sect Sci.(in press). control of western yellow-striped armyworm, Spodoptera Holyoak, M., and S. Sachdev. 1998. Omnivory and the sta- praefica (Grote), in hay alfalfa in northern California. bility of simple food webs.Oecologia (Berl.).117:413Ð Hilgardia 49: 1Ð23. 419. Cisneros, J. J., and J. A. Rosenheim. 1998. Changes in the Janssen, A., E. Willemse, and T. van der Hammen. 2003. foraging behavior, within-plant vertical distribution and Poor host plant quality causes omnivore to consume pred- micro-habitat selection of a generalist predator: an age ator eggs.J.Anim.Ecol.72: 478Ð483. analysis.Environ.Entomol.27: 949Ð957. Jervis, M. A., N.A.C. Kidd, and G. E. Heimpel. 1996. Para- Cline, A. R., and E. A. Backus. 2002. Correlations among AC sitoid adult feeding behaviour and biological control Ða electronic monitoring waveforms, body postures, and review.Biocontrol News Info.17:11NÐ26N. stylet penetration behaviors of Lygus hesperus Karban, R., D. Hougen-Eitzmann, and G. English-Loeb. (Hemiptera: Miridae).Environ.Entomol.31: 538Ð549. 1994. Predator-mediated apparent between Cohen, A. C. 1996. Plant feeding by predatory Heteroptera: two herbivores that feed on grapevines.Oecologia evolutionary and adaptational aspects of trophic switch- (Berl.). 97: 508Ð511. ing, pp.1Ð17. In O.Alomar and R.N.Wiedenmann [eds.], Lalonde, R. G., R. R. McGregor, and D. R. Gillespie. 1999. Zoophytophagous Heteroptera: implications for life his- Plant-feeding by arthropod predators contributes to the 1370 ENVIRONMENTAL ENTOMOLOGY Vol.33, no.5

stability of predator-prey .Oikos 87: damage to apple by Campylomma verbasci (Hemiptera: 603Ð608. Miridae).J.Econ.Entomol.94: 33Ð38. Leigh, T. F., and P. B. Goodell. 1996. Insect management, Rosenheim, J. A., D. D. Limburg, and R. G. Colfer. 1999. pp.260Ð293. In S.J.Hake, T.A Kerby, and K.D.Hake Impact of generalist predators on a biological control [eds.], Cotton production Manual. University of Califor- agent, carnea: direct observations.Ecol. nia, Division of Agriculture and Natural Resources Pub- Appl.9: 409Ð417. lication 3352, Oakland, CA. Settle, W. H., H. Ariawan, E. T. Astutui, W. Cahayana, A. L. Leigh, T. F., T. A. Kerby, and P. F. Wynholds. 1988. Cotton Halo,. D. Hindayana, A. S. Lestari, and Pajarningsih. square damage by the plant bug, Lygus hesperus 1996. Managing tropical rice pests through conservation (Hemiptera: Heteroptera: Miridae), and abscission rates. of generalist natural enemies and alternative prey.Ecol- J.Econ.Entomol.81: 1328Ð1337. ogy 77: 1975Ð1988. Limburg, D. D., and J. A. Rosenheim. 2001. Extraßoral nec- Sevacherian, V., and V. M. Stern. 1972. Sequential sampling tar consumption and its inßuence on survival and devel- plans for Lygus bugs in California cotton Þelds.Environ. opment of an omnivorous predator, larval Chrysoperla Entomol.1: 704Ð710. plorabunda (: ).Environ.Ento- Trichilo, P. J., and T. F. Leigh. 1986. Predation on spider mol.30: 595Ð604. ´ eggs by the western ßower thrips, Frankliniella oc- Lucas, E., and O. Alomar. 2002. Impact of Macrolophus cidentalis (Thysanoptera: Thripidae), an opportunist in a caliginosus presence on damage production by Dicyphus cotton agroecosystem.Environ.Entomol.15: 821Ð825. tamaninii (Heteroptera: Miridae) on tomato fruits.J. University of California. 1996. Integrated pest management Econ.Entomol.95: 1123Ð1129. for cotton in the western region of the United States, 2nd May, R. M. 1973. Stability and complexity in model ecosys- ed.University of California, Division of Agriculture and tems.Princeton University Press, Princeton, NJ. Natural Resources Publication 3305, Oakland, CA. McCann, K., A. Hastings, and G. R. Huxel. 1998. Weak tro- phic interactions and the .Nature van Rijn, P.C.J., Y. M. van Houten, and M. W. Sabelis. 2002. (Lond.) 395: 794Ð798. How plants beneÞt from providing food to predators even McGregor, R. R., D. R. Gillespie, C. G. Park, D.M.J. Quiring, when it is also edible to herbivores.Ecology 83: 2664Ð and M.R.J. Foisy. 2000. Leaves or fruit? The potential for 2679. damage to tomato fruits by the omnivorous predator, Walde, S. J. 1995. Internal dynamics and : Knight (Heteroptera: Miridae).Ento- experimental tests with predator-prey systems, pp.173Ð mol.Exp.Appl.95: 325Ð328. 193. In N.Cappuccino and P.W.Price [eds.],Population McMurtry, J. A., and B. A. Croft. 1997. Life-styles of phyto- dynamics: new approaches and synthesis.Academic, San seiid mites and their roles in biological control.Annu. Diego. Rev.Entomol.42: 291Ð321. Wheeler, A. G., Jr. 1976. Lygus bugs as facultative predators, Mueller, S. C., C. G. Summers, and P. B. Goodell. 2003. A pp.28Ð33. In Proceedings of Workshop at the XV Inter- Þeld key to the most common Lygus species found in national Congress of Entomology, 19Ð28 August 1976, agronomic crops of the central San Joaquin Valley of Washington, DC.University Press of Idaho, Moscow, ID. California.University of California, Division of Agricul- Wheeler, A. G., Jr. 2001. Biology of the plant bugs ture and Natural Resources Publication 8104, Oakland, (Hemiptera: Miridae): pests, predators, opportunists. CA. Cornell University Press, Ithaca, NY. Naranjo, S. E., and J. R. Hagler. 1998. Characterizing and Williams, R. J., and N. D. Martinez. 2000. Simple rules yield estimating the effect of heteropteran predation, pp.171Ð complex food webs.Nature (Lond.)404: 180Ð183. 197. In M.Coll and J.R.Ruberson [eds.],Predatory Wilson, L. J., L. R. Bauer, and G. H. Walter. 1996. ÔPhyto- Heteroptera: their ecology and use in biological control. phagousÕ thrips are facultative predators of twospotted Thomas Say Publications in Entomology.Entomological spider mites (: Tetranychidae) on cotton in Austra- Society of America, Lanham, MD. lia.Bull.Entomol.Res.86: 297Ð305. Pfannenstiel, R. S., and K. V. Yeargan. 2002. IdentiÞcation Zeng, F., and A. C. Cohen. 2000. Comparison of ␣-amylase and diel activity patterns of predators attacking Helicov- and protease activities of a zoophytophagous and two erpa zea (Lepidoptera: ) eggs in soybean and phytozoophagous Heteroptera.Comp.Biochem.Physiol. sweet corn.Environ.Entomol.31: 232Ð241. A.126: 101Ð106. Pimm, S. L. 1982. Food webs.Chapman & Hall, London, Zeng, F., and A. C. Cohen. 2001. Induction of elastase in United Kingdom. zoophytophagous heteropteran, Lygus hesperus Polis, G. A. 1991. Complex trophic interactions in : (Hemiptera: Miridae).Ann.Entomol.Soc.Am.94: 146Ð an empirical critique of food-web theory.Am.Nat.138: 151. 123Ð155. Reding, M. E., E. H. Beers, J. F. Bruner, and J. E. Dunley. 2001. Inßuence of timing and prey availability on fruit Received 8 August 2003; accepted 9 June 2004.