Clemson University, Coastal Research and Educalion Center 2865 Savannah Highway. Charleston, SC USA
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1 Parasitism and Predation on Egg Masses ofthe Southern Green Stink Bug, Nezara viridula (L.) (Heteroptera: Pentatomidae), in Tomato, Okra, Cowpea, Soybean, and Wild Radishl,2 B. M. Shepard, K. D. Elsey3, A. E, Mukenfuss and H. D. Justo, Jr. Clemson University, Coastal Researh and Edualion Center 2865 Savannah Highway Charleston, SC USA J. Agri. Entomol. 11(4): (Otober 1994) ABSTRACT Predation and parasitism of eggs octhe southern green stink bug, Nezara uiridula (L.), were assessed by plaing egg masses in tomato, okra, owpea, soybean, and wild radish during 1991 and Perent parasitism and predation of N. uiridula egg masses were variable among years and rops, but parasitism was higher than predation in tomato for both years. Average perent parasitism and predation were approximately equal in okra, soybean and owpea in 19 and in wild radish in During 19, 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 owpea. Parasitism of egg masses in wild radish reahed a peak of nearly 1% during May 1991 and delined to about 3% toward the end of the sampling period. Season long parasitism of N. uirldula egg masses in soybean and okra was higher than predation in The major patasii from all rops was Trissolus basalis (Wollaston). KEY WORDS Nezara viridula, predation, parasitism, tomato, okra, owpea, soybean, wild radish. Trissolus 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 rops (DeWitt & Godfrey 1972, Todd & Herzog 198). It also attaks many wild hosts that serve as reservoirs until agriultural rops are available (Jones & Sullivan 1982), Nezara viridula eology and behavior were reviewed by Todd (19S9) and reviews by Jones (1988) and Luk (1981) ontained referenes to parasites important in N. viridula ontrol. The major speies that attaks N. uiridula in the United States is the egg parasite, TrissollLs basalis (Wollaston) (Hymenoptera: Selionidae) Jones (1988). Nishida (1966) glued eggs of laboratory reared N. vi.ridula to leaves of Asystasia oromandeliana Nees in Hawaii and found that parasitism by T. basalis ranged from 14 to 55% and predation by the ant Pheidole megaepha./a (F.) ranged from 2 to 1%. Besides this study, attaks by both 1Aepted for publiation 15 June Tehnial ontribution No. 49 of the South Cnrolina Agriultuml Experiment Station, Clemson University, Clemson se. 3 U. S. Vegetable Laborulory, ARS, USDA, 2875 Suvllnnnh HighwHY, Clmrlel:ltoll, South Cllrolinu
2 376 J. AW;. Entomol. Vol. ll, No.4 (1994) predators and parasites on eggs of N. uiridula loated in difterent host plants have not been measured, although Yeargan (1979) monitored the ation of parasites and predators on eggs of Arosternum hilare (Say) and related pentatomid speies in soybean and alfalfa. Predators have been reported as important N. uiridula mortality fators (Kiritani 1964, Nishida 1966, Starn et al. 1987). Using an enzyme linked immunosorbent assay (ELISA), Ragsdale et al. (1981) identified 27 speies of insets and spiders that attaked eggs and nymphs of N. ui.ridula in soybean. In a separate study in Charleston, se, T. basalis attaked an average of 53.1 ± 1.9% of eggs per egg mass (n = 26) and predators attaked 78. ± 1.6% (n = 451) (H. D. Justo, personal ommuniation). The average number of eggs per egg mass as determined from a subsample of the egg masses used in this study was 73.7 ± U.8 (n = 1). This present study was undertaken to determine the seasonal inidene of parasitism and predation of eggs of N. uiridula in tomato, Lyopersium esulentum Mill.; okra, Abelmoshus esulentus (L.); owpea, Vigna unguiulata (L.) Walp.; soybean, Glyine max (L.) Merr.; and wild radish, Raphanus rapha.nistrum, L., in oastal South Carolina. Materials and Methods Field tests were arried out at Clemson University's Coastal Researh and Eduation Center from 6 June to 26 Otober 19 and from 1 April to 19 September 1991 to evaluate parasitism and predation on eggs of N. viridula in tomato, okra, owpea, soybean. Wild radish was inluded in During 19, 'Sunny' variety tomatoes were transplanted to the field on 3 August, 'Clemson Spineless' okra was planted on 3 April, 'Mississippi Silver' owpea was planted on 11 May, and 'Young' soybean was planted on 14 May. In 1991 the same varieties of tomato and okra as in 19 were planted on 19 Marh and 27 May, respetively. 'Carolina Cream' owpea and 'Coker 485' soybean were planted on 9 May. Eah field was approximately.25 ha exept for the wild radish that ourred in naturally established lumps along borders of surrounding fields. Egg masses were obtained from a olony of N. viridula reared at the U. S. Vegetable Laboratory, Charleston, SC. Egg masses were stored at -5 C until ready for plaement in the field. Powell & Shepard (1982) had determined that N. viridula eggs stored at -5 C were suitable hosts for the parasite T. basalis. Ten freezer-stored egg masses were plaed randomly in eah field weekly by gluing (Elmer's glue) the egg masses to small strips of ardboard and stapling the strips to the undersides of leaves. At the end of eah week, missing egg masses were reorded and those remaining were removed, plaed in small plasti petri dishes and held in an inset rearing room at 24 ± 5 C with a photoperiod of L:D 14:1 to allow parasites to emerge. Missing egg masses were onsidered to be preyed upon. Parasitism was alulated as a perentage of the remaining masses, either whole or partially eaten.
3 SHEPARD et al.: Parasitism and Pl'edation on N. uiridula Egg masses 377 Results and Disussion 19 Tests. Predation and parasitism on N. viridula egg masses varied widely between rops and growing seasons. More than 95% of the parasites found in all rops during both seasons were T. basalis with Ooenyrtus submeta.llius (Howard) (Hymenoptera: Enyrtidae) present in low numbers. In a rop of fall tomatoes in 19 there was no predation on N. viridula egg masses (n = 5) but parasitism reahed 7% on two sampling dates (Fig. 1A). Perent parasitism and predation of egg masses (n = 7) in okra are shown in Fig. lb. Parasitism reahed over 8% early in the season. During the latter two sampling dates predators onsumed about 5% of the egg masses while T. basalis attaked from -%. There was little differene in the season-long mean levels of parasitism (37%) ompared to predation (33%) in okra. Parasitism of egg masses (n = 5) in owpea reahed 7% in early August but delined to zero as the season progressed (Fig. Ie). Conversely, predation at the beginning of the season was near zero and inreased to 5% toward the end of the season. The shifts in importane between the two natural enemy groups were evident in several of the rops and it was lear that both parasites and predators were important in impating natural populations ofn. uiridula. In soybean, predators were the most important group of natural enemies attaking egg masses (n = 7) during the last four sampling dates (Fig. 1), but as in all rops in 19, parasitism was highest on the first sampling date. On 29 August, predation reahed 8% but parasitism was not deteted Tests. Seasonal inidene of egg mass (n = ) parasitism and predation in tomato is shown in Fig. 2A. As in 19, parasitism was higher than predation and the latter was deteted only during the last 3 wks of the season and then at levels usually below %. Parasitism was low (about 1%) during the first 3 wks, peaked at % during mid-may and delined as the season progressed. Natural enemy ation on N. viridula egg masses (n = 7) plaed in okra was lower than in soybean or wild radish. Parasitism was highest (about 55%) during the first sampling period (15 July) and generally delined thereafter (Fig. 2B). Season-long average perent predation (11%) was lower than parasitism (34%). The ation of predators and parasites on egg masses (n = ) in soybean is illustrated in Fig. 2C. Average seasonal parasitism (82%) was higher than predation (41%). Parasitism inreased to nearly 1% on 8 August and remained high throughout the season. The ation of predators was less impressive but inreased to about 7% toward the end of the season. The seasonlong perent predation and parasitism on N. viridula egg masses (n = 1) in wild radish are shown in Fig. 2D. The ation by these natural enemy groups on this wild host plant is about equal to that in soybean. Parasitism reahed a peak of nearly 1% during the week of 9 May and predators took about 8% of the N. viridula egg masses during their peak ativity toward the end of May.
4 378 J. Agri. Entomol. Vol. 11, No.4 (1994) "o.5" IGO 5. JO 1 fotto:ke::l by P'eetor, Poro,illled A. Tomato eo 7 eo / 9/21 1/5 1/19 Week 1 Sample o 5... '". 3 '.litled Dj' Predoto's ParasItized J\ /. 6 O"ro / 7/26 8/9 8/23 9/6 Week 1 Sample 1.\U.l.ed 1;)/ P'PC;:IOfS C PoroStlilN / " '" 5 ' \ "- 3 / 1 7/25 5/5 ':,'eel" ' Sonp'l:' C Co... peo 8/22 ' 7 - ",\lo d Dr,::Jred<ltor 9J PO'GII"'l eo eo "C> 5,..! \ e/a 8/22 9/ ""ek oi S::»mpl So,)'ben 9/21 Fig. 1. Perent parasitism and predation on N. uiridula egg masses plaed in tomato (A), oha (B), owpea (C), and soybean (D). Charleston, SC. 19.
5 SHEPARD et a1.: Parasitism and Predation on N. uiridula Egg masses 'Oil ;'t:okea bv?reaolors,. :'Ua,,"ed t.y P, td::ll.r!i PrOSIlze(J orrte B Qk"o Porslllld j j 'Ow "D" w '" " ;; 3 1o.../' <!7 5/1 5/1:: 5/29 6/12 6/1 8/'5 8/29 'Nt 1 SCi"T\l:I "eel. ef Sum:> e., " '" '" JO ' Alta:l.ed by Predators. Soybean o ParO'tltleG '. 1 o,,_...,.,j 1/15 9/1 8/'5 9/2, 9/\2 W:!d 1 Semple ".. " '" '" v " AtioCol'ea., P,eC(ltor 1 POIOS,\ :o ' 3 ZO ' Wt.!Ck or Sample Fig. 2. Perent parasitism and predation on N. uiridula egg masses plaed in tomato (A), okra (B), soybean (C), and wild radish (D), Charleston, SC, 1991.
6 38 J. Agri. Entomol. Vol. 11, No.4 (994) In summary, there were shifts in the importane of parasites and predators during the season and between rops. In many ases, as the ation of predators inreased, ation by parasites delined. Obviously, predator attaks may have masked the impat of parasites beause predators probably onsumed the parasitized egg masses. Also, removal of egg mass by predators probably prevented parasitism in many ases. The most striking example of a lear preferene by a natural enemy group was in tomato where parasites dominated and the ation of predators was almost absent. OUf results indiate that both predators and parasites may play an important role in regulating populations of N. viridula. The ombined ation by these groups of natural enemies often attaked 1% of the egg masses plaed in some rops. Other researh (H. D. Justo, personal ommuniation) has shown that if an egg mass is attaked by natural enemies 53-78% of eggs will be destroyed. Aknowledgment We express our sinere appreiation to Dr. Walker A. Jones, USDA-ARS, Bioontrol of Insets Researh Unit, Weslao, Texas, and to Dr. David Tonkyn, Biologial Sienes Department, Clemson University, Clemson, South Carolina for their helpful omments. We extend our thanks to Mr. Max DuBose and Ms. Louise Cauthen for their assistane with this study. Dr. P. M. Marsh onfirmed our parasite identifiations. We thank him for this. Referenes Cited DeWitt, N. B. & G. L. Godfrey The literature of arthropods assoiated 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-leiroptera: Pentatomidae). Ann. Entomo!. So. Am. 81: Jones, W. A. & M. J. Sullivan Role of host plants in population dynamis of stink bug pests of soybean in South Carolina. Environ. Entomo!. 11: Kiritani, K Natural ontrol of populations of the southern green stink bug, Nezara viridula. Res. Popul. Eol. (Kyoto) 6: Luk, R. F Parasiti insets introdued as biologial ontrol agents for arthropod pests, pp In D. Pimentel [ed.l, Handbook of pest. management in agriulture, Vol. 2. erc Press, Boa Raton, Florida 51 pp. Nishida, T Behaviol' and mortality of the southern green stink bug, Nezam viridula, in Hawaii. Res. PopuL Eo!. (Kyoto) 8: Powell, J. E. & M. Shepard Biology of Australian and United States strains or Trissolus basalis, a parasitoid of the green vegetable bug, Nezara uiridula. Aust. J. Eol. 7: 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'oeosystern using an ELISA. Environ. Entoma!. 1:
7 SHEPARD et a1.: Parasitism and Predation on N. uiridula Egg masses 381 Starn, P. A., L. D. Newsom & E. N. Lambremont Predation and food as fators affeting survival of Nezara uiridula (L.) (Hemiplera: Pentatomidae) in a soybean eosystem. Environ. Enlomo!. 16: Todd, J. W Eology and behavior of Nezara uiridula. Annu. Rev. Enlomol. 34: Todd. J. W. & D. C. Herzog Sampling phytophagous Pentatomidae on soybean, pp In M. Kogan & D. C. Herzog (ds.], Sampling I\oIethods in Soybean Entomology. Springer-Verlag, New York, 587 pp. Yeargan. K. V Parasitism and predation of stink bug eggs in soybean and alfalfa. Environ. Entomo!. 8:
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