Parasitism and Predation on Egg Masses of the Southern Green Stink Bug, Nezara viridula (L.) (Heteroptera: Pentatomidae), in Tomato, Okra, Cowpea, Soybean, and Wild Radishl,2 B. M. Shepard, K. D. Elsey 3, A. E, Muckenfuss and H. D. Justo, Jr. Clemson University, Coastal Research and Educalion Center 2865 Savannah Highway Charleston, SC 29414 USA J. Agric. Entomol. 11(4): 375-381 (October 1994) ABSTRACT Predation and parasitism of eggs oCthe southern green stink bug, Nezara uiridula (L.), were assessed by placing egg masses in tomato, okra, cowpea, soybean, and wild radish during 1991 and 1992. Percent parasitism and predation of N. uiridula egg masses were variable among years and crops, but parasitism was higher than predation in tomato for both years. Average percent parasitism and predation were approximately equal in okra, soybean and cowpea in 1990 and in wild radish in 1991. During 1990, predation was higher than parasitism in soybean toward the end of the growing season but parasitism was higher early in the season in okra and cowpea. Parasitism of egg masses in wild radish reached a peak of nearly 100% during May 1991 and declined to about 30% toward the end of the sampling period. Season long parasitism of N. uirldula egg masses in soybean and okra was higher than predation in 1991. The major patasiic from all crops was Trissolcus basalis (Wollaston). KEY WORDS Nezara viridula, predation, parasitism, tomato, okra, cowpea, soybean, wild radish. Trissolcus basalis. The southern green stink bug, Nezara viridula (L.), is widely distributed throughout the world and is a major pest on many fruit, vegetable, nut and grain crops (DeWitt & Godfrey 1972, Todd & Herzog 1980). It also attacks many wild hosts that serve as reservoirs until agricultural crops are available (Jones & Sullivan 1982), Nezara viridula ecology and behavior were reviewed by Todd (19S9) and reviews by Jones (1988) and Luck (1981) contained references to parasites important in N. viridula control. The major species that attacks N. uiridula in the United States is the egg parasite, TrissolclLs basalis (Wollaston) (Hymenoptera: Scelionidae) Jones (1988). Nishida (1966) glued eggs of laboratory reared N. vi.ridula to leaves of Asystasia coromandeliana Nees in Hawaii and found that parasitism by T. basalis ranged from 14 to 55% and predation by the ant Pheidole megacepha./a (F.) ranged from 2 to 100%. Besides this study, attacks by both 1 Accepted for publication 15 June 1994. 2 Technical contribution No. 4009 of the South Cnrolina Agricultuml Experiment Station, Clemson University, Clemson se. 3 U. S. Vegetable Laborulory, ARS, USDA, 2875 Suvllnnnh HighwHY, Clmrlel:ltoll, South Cllrolinu 2901101. 375 376 J. AW;c. Entomol. Vol. ll, No.4 (1994) predators and parasites on eggs of N. uiridula located in difTerent host plants have not been measured, although Yeargan (1979) monitored the action of parasites and predators on eggs of Acrosternum hilare (Say) and related pentatomid species in soybean and alfalfa. Predators have been reported as important N. uiridula mortality factors (Kiritani 1964, Nishida 1966, Starn et al. 1987). Using an enzyme linked immunosorbent assay (ELISA), Ragsdale et al. (1981) identified 27 species of insects and spiders that attacked eggs and nymphs of N. ui.ridula in soybean. In a separate study in Charleston, se, T. basalis attacked an average of 53.1 ± 1.9% of eggs per egg mass (n = 260) and predators attacked 78.0 ± 1.6% (n = 451) (H. D. Justo, personal communication). The average number of eggs per egg mass as determined from a subs ample of the egg masses used in this study was 73.7 ± U.8 (n = 120). This present study was undertaken to determine the seasonal incidence of parasitism and predation of eggs of N. uiridula in tomato, Lycopersicum esculentum Mill.; okra, Abelmoschus esculentus (L.); cowpea, Vigna unguiculata (L.) Walp.; soybean, Glycine max (L.) Merr.; and wild radish, Raphanus rapha.nistrum, L., in coastal South Carolina. Materials and Methods Field tests were carried out at Clemson University's Coastal Research and Education Center from 6 June to 26 October 1990 and from 10 April to 19 September 1991 to evaluate parasitism and predation on eggs of N. viridula in tomato, okra, cowpea, soybean. Wild radish was included in 1991. During 1990, 'Sunny' variety tomatoes were transplanted to the field on 3 August, 'Clemson Spineless' okra was planted on 30 April, 'Mississippi Silver' cowpea was planted on 11 May, and 'Young' soybean was planted on 14 May. In 1991 the same varieties of tomato and okra as in 1990 were planted on 19 March and 27 May, respectively. 'Carolina Cream' cowpea and 'Coker 485' soybean were planted on 9 May. Each field was approximately 0.25 ha except for the wild radish that occurred in naturally established clumps along borders of surrounding fields. Egg masses were obtained from a colony of N. viridula reared at the U. S. Vegetable Laboratory, Charleston, SC. Egg masses were stored at -50·C until ready for placement in the field. Powell & Shepard (1982) had determined that N. viridula eggs stored at -50°C were suitable hosts for the parasite T. basalis. Ten freezer-stored egg masses were placed randomly in each field weekly by gluing (Elmer's glue) the egg masses to small strips of cardboard and stapling the strips to the undersides of leaves. At the end of each week, missing egg masses were recorded and those remaining were removed, placed in small plastic petri dishes and held in an insect rearing room at 24 ± 5°C with a photoperiod of L:D 14:10 to allow parasites to emerge. Missing egg masses were considered to be preyed upon. Parasitism was calculated as a percentage of the remaining masses, either whole or partially eaten. SHEPARD et al.: Parasitism and Pl'edation on N. uiridula Egg masses 377 Results and Discussion 1990 Tests. Predation and parasitism on N. viridula egg masses varied widely between crops and growing seasons. More than 95% of the parasites found in all crops during both seasons were T. basalis with Ooencyrtus submeta.llicus (Howard) (Hymenoptera: Encyrtidae) present in low numbers. In a crop of fall tomatoes in 1990 there was no predation on N. viridula egg masses (n = 50) but parasitism reached 70% on two sampling dates (Fig. 1A). Percent parasitism and predation of egg masses (n = 70) in okra are shown in Fig. lB. Parasitism reached over 80% early in the season. During the latter two sampling dates predators consumed about 50% of the egg masses while T. basalis attacked from 0-20%. There was little difference in the season-long mean levels of parasitism (37%) compared to predation (33%) in okra. Parasitism of egg masses (n = 50) in cowpea reached 70% in early August but declined to zero as the season progressed (Fig. Ie). Conversely, predation at the beginning of the season was near zero and increased to 50% toward the end of the season. The shifts in importance between the two natural enemy groups were evident in several of the crops and it was clear that both parasites and predators were important in impacting natural populations of N. uiridula. In soybean, predators were the most important group of natural enemies attacking egg masses (n = 70) during the last four sampling dates (Fig. 10), but as in all crops in 1990, parasitism was highest on the first sampling date. On 29 August, predation reached 80% but parasitism was not detected. 1991 Tests. Seasonal incidence of egg mass (n = 90) parasitism and predation in tomato is shown in Fig. 2A. As in 1990, parasitism was higher than predation and the latter was detected only during the last 3 wks of the season and then at levels usually below 20%. Parasitism was low (about 10%) during the first 3 wks, peaked at 90% during mid-May and declined as the season progressed. Natural enemy action on N. viridula egg masses (n = 70) placed in okra was lower than in soybean or wild radish. Parasitism was highest (about 55%) during the first sampling period (15 July) and generally declined thereafter (Fig. 2B). Season-long average percent predation (11%) was lower than parasitism (34%). The action of predators and parasites on egg masses (n = 90) in soybean is illustrated in Fig. 2C. Average seasonal parasitism (82%) was higher than predation (41%). Parasitism increased to nearly 100% on 8 August and remained high throughout the season. The action of predators was less impressive but increased to about 70% toward the end of the season. The season~long percent predation and parasitism on N. viridula egg masses (n = 100) in wild radish are shown in Fig. 2D. The action by these natural enemy groups on this wild host plant is about equal to that in soybean. Parasitism reached a peak of nearly 100% during the week of 9 May and predators took about 80% of the N. viridula egg masses during their peak activity toward the end of May. J. Agric. Entomol. Vol. 11, No.4 (1994) 378 IGO • 0 90 100 fottoc:ke::l by P'ecetor, Poro,illled A. Tomato eo ·· " 0 co .5" c ~ ~ 0. • 90 0 /~ eo 50 ·0 JO 20 ·· ... 70 ~ 60 co '" c ~ 0. 50 / •0 30 '0 0 0 9/21 10/5 10/19 7/26 Week 01 Sample 100 • C 90 .\Uc.cl.ed 1;)/ P'PC;:IOfS PoroStlilN "'" ~ c · ~ "- 9J 0 ",\loc·cd Dr ,::Jred<ltor~ 0 PO'G~II"'l~ So,)'becn · eo C> 50 ,~ ..! '0· 30 / 70 - 0 " 0 50 0 • '00 C Co.... peo /~ 60 10 9/6 eo 70 20 8/23 8/9 Week 01 Sample 80 0 /0 20 10 · 6 O"ro J\. 60 70 .lItlcc~ed Dj' Predoto's ParasItized 40 30 \ 20 \ 10 0 7/25 5/5 ':,'eel" c' Sonp'l:' 8/22 e/a 8/22 9/ 9/21 ""cek oi S::»mplc Fig. 1. Percent parasitism and predation on N. uiridula egg masses placed in tomato (A), oha (B), cowpea (C), and soybean (D). Charleston, SC. 1990. SHEPARD et a1.: Parasitism and Predation on N. uiridula Egg masses • 0 100 .. ~ 0 " D" '" ~;; w " ;'t:ockea bv ?reaolors PcrOSI~lze(J 'Oil ,. 0 ~j ~ j 'o.O•w• • 30 5/1 'Nt~ • o :'Uac,,"ed t.y P, td::llc.r!i Porcsllll~d B Qk"o ., 0 " ~ '"c'" ~ ~ ·0 JO 20 20 10 <!7 • orrcte 379 ../' '0 • 5/1:: 01 5/29 6/1 6/12 SCi"T\l:Ic Altac:l.ed by Predators ParO'tltleG c. Soybean 100 • 0 AtioCol'ea 0., POIOS,\ 8/'5 "eel. ef Sum:> e 8/29 P,eC(ltor~ :co 90 ".. 0 " ~ ~ '0. o ~••~,~~,_~...,.,J 1/15 9/1 8/'5 Wc:!d 01 Semple 9/2, 1 70 60 '"c'" 50 ~ '0 v ~ 60 " 30 ZO '0 9/\2 Wt.!Ck or Sample Fig. 2. Percent parasitism and predation on N. uiridula egg masses placed in tomato (A), okra (B), soybean (C), and wild radish (D), Charleston, SC, 1991. 380 J. Agric. Entomol. Vol. 11, No.4 (994) In summary, there were shifts in the importance of parasites and predators during the season and between crops. In many cases, as the action of predators increased, action by parasites declined. Obviously, predator attacks may have masked the impact of parasites because predators probably consumed the parasitized egg masses. Also, removal of egg mass by predators probably prevented parasitism in many cases. The most striking example of a clear preference by a natural enemy group was in tomato where parasites dominated and the action of predators was almost absent. OUf results indicate that both predators and parasites may play an important role in regulating populations of N. viridula. The combined action by these groups of natural enemies often attacked 100% of the egg masses placed in some crops. Other research (H. D. Justo, personal communication) has shown that if an egg mass is attacked by natural enemies 53 - 78% of eggs will be destroyed. Acknowledgment We express our sincere appreciation to Dr. Walker A. Jones, USDA-ARS, Biocontrol of Insects Research Unit, Weslaco, Texas, and to Dr. David Tonkyn, Biological Sciences Department, Clemson University, Clemson, South Carolina for their helpful comments. We extend our thanks to Mr. Max DuBose and Ms. Louise Cauthen for their assistance with this study. Dr. P. M. Marsh confirmed our parasite identifications. We thank him for this. References Cited DeWitt, N. B. & G. L. Godfrey. 1972. The literature of arthropods associated with soybean. II. A bibliography of the southern green stink bug, Nezara uiridula (L.). Illinois Nat. Hist. Surv. BioI. Notes 78, 23 pp. Jones, W. A. ]988. A world review of the parasitoids of the southern green stink bug, Nezara uiriduln (L.) (J-leicroptera: Pentatomidae). Ann. Entomo!. Soc. Am. 81: 262 273. Jones, W. A. & M. J. Sullivan. 1982. Role of host plants in population dynamics of stink bug pests of soybean in South Carolina. Environ. Entomo!. 11: 867-875. Kiritani, K. 1964. Natural control of populations of the southern green stink bug, Nezara viridula. Res. Popul. Ecol. (Kyoto) 6: 88-98. Luck, R. F. 1981. Parasitic insects introduced as biological control agents for arthropod pests, pp. 125-184. In D. Pimentel [ed.l, Handbook of pest. management in agriculture, Vol. 2. eRC Press, Boca Raton, Florida 501 pp. Nishida, T. 1966. Behaviol' and mortality of the southern green stink bug, Nezam viridula, in Hawaii. Res. PopuL Eco!. (Kyoto) 8: 78~88. Powell, J. E. & M. Shepard. 1982. Biology of Australian and United States strains or Trissolcus basalis, a parasitoid of the green vegetable bug, Nezara uiridula. Aust. J. Ecol. 7: 181-186. Ragsdale, D. W., A. D. Larson & L. D. Newsom. ]981. Quant.itative assessment of the predators of Nezara viridula eggs and nymphs within a soybean agr'oecosystern using an ELISA. Environ. Entoma!. 10: 402-405. SHEPARD et a1.: Parasitism and Predation on N. uiridula Egg masses 381 Starn, P. A., L. D. Newsom & E. N. Lambremont. 1987. Predation and food as factors affecting survival of Nezara uiridula (L.) (Hemiplera: Pentatomidae) in a soybean ecosystem. Environ. Enlomo!. 16: 1211-1216 Todd, J. W. 1989. Ecology and behavior of Nezara uiridula. Annu. Rev. Enlomol. 34: 273-292. Todd. J. W. & D. C. Herzog. 1980. Sampling phytophagous Pentatomidae on soybean, pp. 438·478. In M. Kogan & D. C. Herzog (cds.], Sampling I\oIethods in Soybean Entomology. Springer-Verlag, New York, 587 pp. Yeargan. K. V. 1979. Parasitism and predation of stink bug eggs in soybean and alfalfa. Environ. Entomo!. 8: 715-719.
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