Predation of Striped Lynx , salticus (Araneae: Oxyopidae), on Tarnished Plant Bug, Lygus lineolaris (Heteroptera: Miridae): A Laboratory Evaluation

O. P. YOUNG AND T. C. LOCKLEY Southern Field Crop Insect Management Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Stoneville, Mississippi 38776

Ann. Entomol. Soc. Am. 79: 879-883 (1986) ABSTRACT Oxyopes salticus Hentz is an important member of the predatory community within and adjacent to row crops in the United States. Lygus lineolaris (Palisot de Beauvois) is a major pest of crops in most areas of North America. A laboratory experiment was conducted to determine relationship of predatory success to size of the spider and size of the plant bug. Predation success was inversely related to prey size across all predator sizes. After exposure for 24 h, all spider size classes had high predation values (36-92%) for small (first-second instar) plant bug nymphs, intermediate values (32-68%) for medium-sized (third instar) nymphs, and low predation values (8-52%) for large (fifth instar) nymphs. Significant increases in predation from 24 to 48 h occurred only with small exposed to small- and medium-sized plant bugs. Low predation success may be due both to difficulty in prey capture and to satiation after one or more successful prey captures.

KEY WORDS Lygus lineolaris, Oxyopes salticus, predation, prey size

A RECENT REVIEW of the literature has empha- 1980). The apparent need for a nonchemical con- sized the potential role of spiders in the biological trol strategy for TPB has led the staff of the South- control of insect pests (Riechert & Lockley 1984). ern Field Crop Insect Management Laboratory to A prime candidate for consideration in this regard consider various , including O. salticus, is the striped (SLS), Oxyopes salticus as agents of biological control. Hentz (Young & Lockley 1985). This species can Field observations have indicated recently that be the most numerous beneficial in cot- SLS in cotton may preferentially feed upon mem- ton fields and may constitute as much as 90% of bers of Hemiptera, with the TPB representing the all spiders collected in some samples (Laster & most frequently captured prey (Lockley & Young Brazzel 1968). O. salticus may also be the most 1986). To further evaluate the potential impact of abundant spider in border habitats adjacent to cot- SLS on TPB populations, we have evaluated in the ton fields (e.g., Stadelbacher & Lockley 1983). The laboratory the effect of predator and prey sizes on known prey of this species include such economi- prey capture rates. cally important pests as alfalfa weevil, Hypera postica (Gyllenhal); soybean looper, Pseudoplusia includens (Walker); tobacco bud worm and corn Materials and Methods earworm, Heliothis spp.; southern green stink bug, Spiders and plant bugs were obtained by D-Vac Nezara viridula (L.); and tarnished plant bug sampling from an old-field habitat dominated by (TPB), Lygus lineolaris (Palisot de Beauvois) Erigeron canadensis (Compositae) during early (Young & Lockley 1985). July 1984 in Washington County, Miss. In the lab- TPB is a pest of particular concern to cotton oratory, both SLS and TPB were segregated by growers in the southeastern and south-central size, placed in containers, and maintained in en- United States. This insect can cause up to a 40% vironmental chambers at 25°C, 80% RH, and a yield loss by feeding on flower buds (squares) and 14:10 (L:D) photoperiod. producing several types of immediate and long- TPB nymphs were separated into three size term damage to the plant (Scales & Furr 1968, classes, small, medium, and large (corresponding Pack & Tugwell 1976). Most TPB feeding activity to particular stadia, as determined by wing pad in cotton occurs in early to mid season (June to development), and were maintained in containers mid-July); attempts to reduce TPB populations with (3.8 liter) with green beans, Phaseolus vulgaris L. insecticides at that time can allow large late-season Small nymphs were defined as first and second Heliothis populations by reducing the associated instars, with an average pronotum width of 0.55 ± predator/parasite populations (Lambert et al. 0.07 mm (n = 10), medium nymphs as third instar

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Table 1. Prey consumption by nine predator/prey size Table 2. Prey consumption by three size categories categories i no. of prey i no. of prey Size class consumed t test Predator/prey consumed after t test (LSD) after 24 h (LSD) size relation 24 h Spider Large/small 4.6 Small 15 1.27 Medium/small 4.4 Medium 15 3.07 Large/medium 3.4 Large 15 3.53 Medium/medium 2.8 Large/large 2.6 TPB nymph Medium/large 2.0 Small 15 3.60 Small/small 1.8 Medium 15 2.60 Small/medium 1.6 Large 15 1.67 Small/large 0.4 Means within predator or prey grouping with the same letter Means with the same letter are not significantly different (P > are not significantly different (P > 0.05). 0.05).

subsequent analyses, only analyses for the 24-h data (0.96 ± 0.12 mm, n = 10), and large nymphs as are presented. This nonrandom distribution of dead fifth instar (1.68 ± 0.28 mm, n = 10). Nymphs prey suggests some effect(s) of predator or prey that were between two size classes were not used. size on prey mortality, and can be examined in SLS adults and spiderlings were separated into several ways. Arranging in numerical order the small, medium, and large size classes based on car- values for the mean number of prey killed in each apace width. Small spiderlings with an average predator/prey category indicates that the signifi- carapace width of 0.58 ± 0.04 mm (n = 10) were cant groupings are not based on the size of just the defined as presumptive third instar. Medium spi- predator or the prey (Table 1). For example, the derlings (0.81 ± 0.07 mm, n = 10) were presump- three categories with the highest number of prey tive fifth and sixth instars. The large size category killed include both medium- and large-sized pred- consisted of penultimate (ninth instar) females and ators and both small- and medium-sized prey. To penultimate (eighth instar) males (1.34 ± 0.29 mm, determine whether both predator and prey size n = 10). Spiders between two size classes were not are equally important in determining prey mor- used. Each spider was placed in a petri dish (15 tality, all data were grouped by size class (Table by 100 mm) and offered one TPB nymph (about 2). For TPB nymphs, there were significant dif- one-half size of spider) 2 days before the begin- ferences in the mean number killed in each size ning of the experiment. class, regardless of predator size. For SLS, only the The experiment protocol consisted of exposing number of prey killed by small spiders was signif- five TPB nymphs of a particular size to a single icantly different from that killed by the other two SLS in a container (15 by 100 mm petri dish) with sizes, suggesting that small spiders may have dif- food (green bean) for the nymphs, and counting ficulty preying upon members of at least one of the number of surviving nymphs after 24 and 48 the sizes of TPB. This can perhaps best be illus- h. Five replicates were included of each of the trated by presenting the data as percent predation nine combinations of size classes of predator and by each size class of predator on each size class of prey, for a total of 45 SLS and 225 TPB nymphs. prey (Fig. 1). Small spiders are relatively poor To monitor the mortality of TPB nymphs under predators on large TPB nymphs, even when both experimental conditions and in the absence of SLS, are confined in a container for 48 h. five nymphs and a green bean were placed in a The experimental protocol was designed to test petri dish, two replicates for each of the three size the hypothesis that predation rate by SLS was cor- classes. related with the size of the prey. Eight ranking SAS programs (SAS Institute 1982) were utilized sequences were tested, four involving increasing for various analyses of variance (ANOVA), and for or decreasing prey size within each size category obtaining correlation coefficients and the Student's of predator and four involving increasing or de- t distribution. creasing predator size within each size category of prey. The highest significant positive correlation was in a scheme wherein decreasing prey size Results within increasing predator size was highly corre- There were nine possible predator/prey com- lated with increasing mortality of prey (r = +0.733; binations of three size classes of predator and three n = 45; P < 0.0001). size classes of prey. The distribution of dead prey among these nine combinations was not random after 24 or 48 h ([24 h: F = 0.1; df = 8; P < 0.0001; Discussion ANOVA] [48 h: F = 17.8; df = 8; P < 0.0001; Limitations of the Data. Records of prey cap- ANOVA]). Because there were no significant dif- ture by nonwebspinning spiders historically have ferences between 24- and 48-h values in this or been difficult to obtain. Many hours of field obser- November 1986 YOUNG & LOCKLEY: O. salticus PREDATION ON L. lineolaris 881

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Fig. 1. Percentage of L. lineolaris nymphs killed by O. salticus after 24 and 48 h, as determined for three sizes of predator and three sizes of prey. vations typically produce very few records of prey a container 80 mm high by 85 mm wide (Howell capture by spiders that are either actively search- & Pienkowski 1971). Feeding tests have also been ing or in hiding. This situation led Whitcomb conducted with either a serial presentation of prey (1967) to introduce potential prey onto plants and or an ad lib. presentation. The distribution of TPB to lie on the ground for the next 6 h recording prey prey in cotton is not random, with more than one captures. In a total of 390 h of such observations, TPB nymph usually occurring on a flower bud or after releasing 1,605 potential lepidopterous larval in the immediate vicinity (O.P.Y., unpublished prey, he was able to obtain only 63 records of prey data). Thus, a SLS is likely to meet groups of prey, capture by spiders. Perhaps Bilsing (1920) stated rather than solitary individuals. It is for these rea- the problem most accurately when he indicated sons that we believe it appropriate to conduct that the study of active hunting spiders was almost feeding tests with SLS under our chosen laboratory impossible unless observations were conducted in conditions, and that the results of this experiment laboratory cages. Spiders have proven to be quite have relevancy to the real world of hunting spi- adaptable to cage environments and there is con- ders. siderable literature devoted to observations and Experimental Results. SLS can be character- experiments conducted under artificial conditions ized as a diurnal foliage-inhabiting hunting spider (Foelix 1982). To our knowledge there is no re- with relatively keen eyesight that can either search search involving hunting spiders that documents actively for prey or assume a prey-catching pos- substantial differences in behavior between labo- ture and wait in ambush for its victims (Brady ratory and field situations. 1964). These characteristics suggested that indi- Feeding tests with hunting spiders have been viduals of this species would be able to successfully conducted in a variety of cage sizes, with differ- obtain food under the conditions of this experi- ences in feeding success apparently not related to ment. Behavioral observations of both predator and the size of the container. In one experiment in prey during the experiment revealed that SLS had which the smallest container was 13 mm high by no difficulty in detecting the presence of TPB. Im- 42 mm wide, spiders (including SLS) were no more mediately before prey capture, spiders would con- or less successful in capturing prey than when in tinually change body orientation so as to be facing 882 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 79, no. 6 a moving bug that was within 3-5 cm. In addition, nymphs in July would be exposed to small- and when a spider of any size attacked and seized a medium-sized SLS. These predator sizes are not as bug, the bug was always killed and eaten (n = capable as large SLS in killing large TPB nymphs. >10). These observations are particularly impor- Considering the entire generation of TPB in cot- tant when considering the low predation values for ton, early season nymphs of any size and mid- and small SLS on large TPB. Of the five replicates with late-season nymphs of small size probably suffer this size combination of predator and prey, three relatively high levels of predation from SLS. Large produced no TPB mortality in 48 h and two pro- TPB nymphs of mid- and late season probably have duced one dead TPB each after 24 h with no ad- lower predation losses, as they are too large for ditional deaths after 48 h (Fig. 1). Low predation successful predation by SLS. This sequence as- values for this size combination, thus, may be due sumes a considerable degree of instar synchrony to both a failure to attack in three cases and satia- within both TPB and SLS populations; unfortu- tion after successful attack in two cases. In either nately, the validity of the assumption is unknown. event, however, the net result was the same: com- We postulate a similar sequence of TPB/SLS pared with the other size combinations, small spi- interactions in cotton field margins. Early-season ders did not kill many large bugs. generations (April-May) of TPB in margins would Extrapolation to Field Situations. O. salticus be exposed to medium and large SLS, the most in Mississippi is univoltine and overwinters as im- capable predator size classes (Fig. 1). When TPB matures. Adults mate in April or May, construct adults disperse from cotton fields back into the egg sacs, and die in May or June. Immatures de- margins in July-August and reproduce, their prog- velop to adults in August, with young immatures eny would be initially exposed to large adult SLS. appearing again in September and October (Red- Later generations of TPB in September-October mond 1967). Population levels of this spider in would only be exposed to small SLS, and would cotton may peak in late June to late July and again suffer relatively low predation levels. in mid-September to early October (Robbins 1982, We, therefore, suggest that certain periods in Scott et al. 1983a). Most of the spiders in cotton the population cycle of TPB can be more vulner- are the smaller and immature forms (Whitcomb able to SLS predation than other periods. Whether & Bell 1964). this is indeed the case awaits further field obser- L. lineolaris in Mississippi is multivoltine and vations. overwinters as adults. Populations increase in early season on wild host plants, and peak population levels in cotton occur in late June to late July (Rob- Acknowledgment bins 1982, Scott et al. 1983b). Only one generation The technical assistance of D. Boykin is appreciated, of TPB is typically produced in cotton before either as is the manuscript review provided by T. R. Ashley, insecticide applications lower population levels or J. C. Bailey, J. E. Powell, S. H. Roach, and G. L. Snod- dispersal to late-season wild host plants occurs. grass. Mating and dispersing adults are most common in early and late season on cotton, with nymphs most common in midseason (O.P.Y., unpublished data). References Cited The following sequence of events can be pos- Bilsing, S. W. 1920. Quantitative studies in the food tulated concerning the exposure in cotton of var- of spiders. Ohio J. Sci. 20: 215-260. ious-sized TPB prey to various-sized SLS preda- Brady, A. R. 1964. The lynx spiders of North Amer- tors. Cotton in the Delta area of Mississippi is ica, north of Mexico (Araneae: Oxyopidae). Bull. Mus. usually planted in April, with plant material ap- Comp. Zool. 131: 429-518. pearing above ground in May. Spiders are among Foelix, R. F. 1982. Biology of spiders. Harvard Univ., the first arthropods to move into a freshly sprouted Cambridge. row crop (Shepard et al. 1974), and SLS popula- Howell, J. O. & R. L. Pienkowski. 1971. Spider pop- tions gradually increase in cotton by dispersal of ulations in alfalfa, with notes on spider prey and late instars and adults. The early instar progeny of effect of harvest. J. Econ. Entomol. 64: 163-168. the few TPB adults dispersing into cotton and ovi- Lambert, L., J. N. Jenkins, W. L. Parrott & J. C. positing in May are exposed to large SLS, the most McCarty. 1980. Evaluation of thirty-eight foreign and domestic cotton cultivars for tarnished plant bug successful size class of predator (Fig. 1). Peak pop- resistance. Miss. Agric. For. Exp. Stn. Res. Rep. 5(1): ulations of dispersing adult TPB would be expect- 1-4. ed in cotton during the presquare and square pe- Laster, M. L. & J. R. Brazzel. 1968. A comparison riods, about mid-June to mid-July. Early instar TPB of predator populations in cotton under different would also begin appearing at about that time, control programs in Mississippi. J. Econ. Entomol. whereas SLS adults would be dying and small, ear- 61: 714-719. ly instar SLS would begin appearing. Thus, small Lockley, T. C. & O. P. Young. 1986. Prey of the TPB nymphs would be exposed primarily to small striped lynx spider, Oxyopes salticus (Araneae: Ox- SLS, the least successful size of predator. TPB yopidae), on cotton in the Delta area of Mississippi. nymphs develop much faster than SLS spiderlings J. Arachnol. 14: (in press). (Ridgway & Gyrisco 1960), such that large TPB Pack, T. M. & P. Tugwell. 1976. Clouded and tar- nished plant bugs on cotton: a comparison of injury November 1986 YOUNG & LOCKLEY: O. salticus PREDATION ON L. lineolaris 883

symptoms and damage on fruit parts. Ark. Agric. 1983b. Population dynamics of cotton arthropods as- Exp. Stn. Rep. Ser. 226: 1-17. sociated with optimum pest management and cur- Redmond, K. R. 1967. Toxicological and biological rent insect control strategies. J. Ga. Entomol. Soc. 18: studies of the striped lynx spider, Oxyopes salticus 518-530. Hentz. M.S. thesis, Mississippi State Univ., State Col- Shepard, M., G. R. Carner & S. C. Turnipseed. 1974. lege. Seasonal abundance of predaceous arthropods in soy- Ridgway, R. L. & C. C. Cyrisco. 1960. Effects of beans. Environ. Entomol. 3: 985-988. temperature on the rate of development of Lygus Stadelbacher, E. A. & T. C. Lockley. 1983. The spi- lineolaris (Hemiptera: Miridae). Ann. Entomol. Soc. ders of Geranium dissectum L. in Washington Am. 53: 691-694. County, Mississippi. J. Ga. Entomol. Soc. 18: 398- Riechert, S. E. & T. C. Lockley. 1984. Spiders as 402. biological control agents. Annu. Rev. Entomol. 29: Whitcomb, W. H. 1967. Field studies of predators of 299-320. the second-instar bollworm, Heliothis zea (Boddie) Robbins, J. T. 1982. The influence of peripheral and (Lepidoptera: Noctuidae). J. Ga. Entomol. Soc. 2: 113- infield vegetation on the development of selected pest 118. and beneficial arthropod populations in cotton. M.S. Whitcomb, W. H. & K. Bell. 1964. Predaceous in- thesis, Mississippi State Univ., State College. sects, spiders, and mites of Arkansas cotton fields. SAS Institute. 1982. SAS user's guide: statistics. SAS Ark. Agric. Exp. Stn. Bull. 690: 1-84. Institute, Cary, N.C. Young, O. P. & T. C. Lockley. 1985. The striped Scales, A. L. & R. E. Furr. 1968. Relationships be- lynx spider, Oxyopes salticus (Araneae: Oxyopidae), tween the tarnished plant bug and deformed cotton in agroecosystems. Entomophaga 30: 329-346. plants. J. Econ. Entomol. 61: 114-118. Scott, W. P., J. W. Smith & C. R. Parencia, Jr. 1983a. Received for publication 1 November 1985; accepted Effect of boll weevil (Coleoptera: Curculionidae) 9 June 1986. diapause control insecticide treatments on preda- ceous arthropod populations in cotton fields. J. Econ. Entomol. 76: 87-90.