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Home , Gratiana (beetle), Gratiana boliviana, Manduca quinquemaculata, Manduca sexta, Solanum viarum, Tupiocoris notatus

Risk assessment of boliviana (Chrysomelidae), a potential biocontrol agent of tropical soda apple, viarum () in the USA

J. Medal,1,2 D. Gandolfo,3 F. McKay3 and J. Cuda1

Summary (Solanaceae), known by the common name tropical soda apple, is a perennial prickly weed native to north-eastern , south-eastern Brazil, Paraguay, and Uruguay, that has been spreading at an alarming rate in the USA during the 1990s. First detected in the USA in 1988, it has already invaded more than 1 million acres (ca. 400,000 ha) of improved pastures and woody areas in nine states. Initial field explorations in South America for potential biocontrol agents were initiated in June 1994 by University of researchers in collaboration with Brazilian and Argentinean scientists. The leaf (Chrysomelidae) was evaluated as a potential biocontrol agent of tropical soda apple. The only known hosts of this are S. viarum and Solanum palinacanthum. Open field experiments and field surveys were conducted to assess the risk of G. boliviana using Solanum melongena () as an alternative . In an open field (choice-test) planted with tropical soda apple and eggplant there was no feeding or oviposition by G. boliviana adults on eggplant. Surveys conducted (1997–2002) of 34 unsprayed fields of eggplant confirmed that this crop is not a host of G. boliviana. Based on these results, the Florida quarantine host-specificity tests, the open field tests in Argentina, and the lack of unfavourable host records in the scientific literature, we concluded that G. boliviana is safe to release for biocontrol of tropical soda apple. A petition submitted for field release to the Technical Advisory Group (TAG) for Biological Control Agents of Weeds was unanimously approved on April 2002, and an APHIS permit for field release was issued in May 2003. Field releases in Florida were initiated on 14 May 2003.

Keywords: Gratiana boliviana, risk assessment, Solanaceae, weed biocontrol.

Introduction 1997). Currently, the infested area is estimated at more than one million acres (Medal et al. 2002a). Tropical Tropical soda apple is a perennial weed, native to South soda apple was first reported in the USA in Glades America, that has been spreading throughout Florida at County, Florida in 1988 (Coile 1993, Mullahey & an alarming rate during the 1990s. The pasture land Colving 1993). This weed is also present in Alabama, infested in 1992 was estimated as approximately Georgia, Louisiana, Mississippi, North Carolina, South 150,000 acres (1 acre = ca. 0.4 ha)(Medal et al. 1996, Carolina, Tennessee, Texas, and Puerto Rico (Bryson Mullahey et al. 1993), and this infested area increased & Byrd Jr. 1996, Dowler 1996, Mullahey et al. 1997), to more than 750,000 acres in 1995–96 (Mullahey et al. although infestations in these states have not reached high levels. The potential range of tropical soda apple in the United States can extend even further based on 1 University of Florida – Department of Entomology & Nematology. studies of the effects of temperature and photoperiod POB 110620. Gainesville, Florida 32611. USA. 2 INTA-Cerro Azul, Misiones Province, Argentina. conducted by Patterson (1996) in controlled environ- 3 USDA-ARS South American Biological Control Laboratory. Hurl- mental chambers. This invasive exotic weed was placed ingham, Argentina. on the Florida and Federal Noxious Weed Lists in 1995, Corresponding author: J. Medal, University of Florida – Department of Entomology & Nematology. POB 110620. Gainesville, Florida 32611, and is listed as one of the most in USA . Florida by the Florida Exotic Council (1999).

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In addition to invading pasture lands and reducing (University of Florida) in collaboration with R. Pitelli carrying capacity (Mullahey et al. 1993), tropical (Universidade Estadual Paulista, Jaboticabal campus, soda apple is a host of at least six viruses that affect Brazil), and D. Gandolfo (USDA-ARS South American vegetable crops including , , and pepper Biological Control Laboratory, Hurlingham, Buenos (McGovern et al. 1994a, McGovern et al. 1994b, Aires province, Argentina). Host-specificity tests and McGovern et al. 1996). Tropical soda apple is also an field surveys were conducted from 1997 to 2002 to alternative host of several major insect pests such as the determine the suitability of the Gratiana , Bemisia argentifolii Bellows and boliviana Spaeth (Chrysomelidae) for biological Perring (Homoptera: Aleyrodidae), a worldwide pest of control of tropical soda apple. In this article we report many field, horticultural, and ornamental crops; the the results of an open-field experiment conducted with Colorado beetle, Leptinotarsa decemlineata G. boliviana exposed to tropical soda apple and (Say) (Coleoptera: Chrysomelidae), a major foliage eggplant (choice test) in Misiones, Argentina, and a feeder of potato in North America; the tomato horn- survey of eggplant fields in South America to assess the worm quinquemaculata (Haworth) (Lepidop- specificity and safety of G. boliviana as a biocontrol tera: ), and the tobacco hornworm, Manduca agent of tropical soda apple in the USA. sexta (L.), major pests of tomato and tobacco; and several other polyphagous such as the southern green stink bug, (L.) (: Material and methods ); the tobacco budworm, Helicoverpa virescens (Fabr.) (: Noctuidae); and the Field experiment in Argentina suckfly, notatus (Distant) (Heteroptera: An open-field experiment (choice) was conducted at ) (Medal et al. 1999, Sudbrink et al. 1999, the Instituto Nacional de Tecnología Agropecuaria Habeck et al. 1996). Although it is very difficult to esti- (INTA)-Agriculture Experimental Station in Cerro mate the real (direct and indirect) economic losses due Azul, Misiones province, Argentina. A natural popula- to this invasive weed, Mullahey (unpublished data) tion of G. boliviana was monitored in a field planted estimated the annual production loss to Florida with tropical soda apple and eggplant (cultivars: Black ranchers in 1993 at US$11 million. Beauty and Long Purple). The tropical soda apple Native to Brazil, Paraguay, north-east Argentina, tested were transplanted from fields close to the area, and Uruguay (Nee 1991), tropical soda apple has spread and the were grown from seeds obtained from into other parts of South and Central America a commercial supplier of local varieties. They were (confirmed growing in Nicaragua, but its presence in planted in pots held in a greenhouse and then trans- Honduras and Costa Rica is unconfirmed). This weed planted to the field on December 6, 1999 when approx- has also spread into other regions including the Carib- imately 10–15 cm in height. Fifty plants of each of the bean (confirmed in Puerto Rico), Africa, India, Nepal, two species tested (total:100 plants) were randomly and China (Chandra & Srivastava 1978, Coile 1993). assigned in five replicates of 20 (10 of each species). All The rapid spread in south Florida can be partially attrib- plants were thoroughly examined once a week (from uted to the plant’s high reproductive potential (Akanda January 5 to April 3, 2000) and feeding, number of et al. 1996, Pereira et al. 1997), and effective seed , and oviposition on the plants were recorded. dispersal by cattle and wildlife, such as deer, feral hogs, raccoons, and that feed on fruits (Mullahey et al. 1993, Bryson et al. 1995, Brown et al. 1996). One trop- Field surveys in Argentina, Brazil, ical soda apple plant can produce an average of 41,000 Paraguay, and Uruguay to 50,000 seeds with a germination rate of at least 75% Thirty-four eggplant fields inside the area of distri- (Mullahey et al. 1993, Pereira et al. 1997). Infested bution of G. boliviana were surveyed from January areas are increasing rapidly, making this a national 1997 to March 2002 in Argentina (16), Brazil (16), problem rather than just a Florida problem. Paraguay (1), and Uruguay (1). These fields were not Management practices for tropical soda apple in treated with pesticides during the growing season, or Florida pastures are based on herbicide applications were fields where fungicides and/or insecticides were combined with mechanical (mowing) practices (Mislevy applied to eggplants only at the beginning of the et al. 1996, Sturgis & Colvin 1996, Akanda et al. 1997, growing cycle. The number of eggplants in the fields Mislevy et al. 1997). These control tactics provide surveyed varied from 6 to approximately 1200. All temporary weed suppression, and costs are estimated at plants were thoroughly examined above ground for US $75.00 per acre to control dense infestations of trop- insects when the field had fewer than 100 plants. When ical soda apple (Mullahey et al. 1996). In addition to there were more than 100 plants, a sample of 50 to100 being expensive, application of chemicals is not always plants was randomly selected to have representatives feasible in rough terrain or inaccessible areas. from most of the areas in each field. Insect specimens A biological control project on this highly invasive found on plants were collected, identified, or sent to non-native weed was initiated in 1997 by J. Medal specialists for identification or confirmation.

293 Proceedings of the XI International Symposium on Biological Control of Weeds

Results should have little negative effect on non-target organ- isms. No adverse impacts are expected on the six solana- Field experiment in Argentina ceous species listed as threatened or endangered in In the open-field planted with tropical soda apple Hawaii and Puerto Rico (US Fish and Wildlife Service and eggplants in an area with a natural population of 1997). Indirect beneficial effects on wildlife populations tropical soda apple and G. boliviana growing in the may be expected due to recolonization by native plants proximity, there was no feeding or oviposition by G. that have been displaced by the rapidly growing and boliviana adults on either of the two eggplant cultivars highly competitive tropical soda apple plants. (Black Beauty and Long Purple) during their vegetative The eggplant fields surveyed in South America, and and reproductive stages of growth. Almost all tropical the host range tests conducted in quarantine in the USA soda apple plants that were thoroughly examined once and in South America (Gandolfo et al., 1999, Medal et a week (from January 5 to April 3, 2000), showed some al., 2002b) indicated that G. boliviana is safe to release. leaf-feeding damage (5–20% of the leaf area) by G. Occasional temporary feeding might occur on some boliviana. A total of 16 G. boliviana adults, 26 larvae very closely related Solanum species such as Solanum and 21 were found on tropical soda apple plants, torvum Sw. (on the Federal Noxious Weed list, intro- but no G. boliviana stages were found on the eggplants. duced from West Africa) and on S. elaeagnifolium Cav. (an important weed in agricultural areas in North Field surveys in Argentina, Brazil, America) (Medal et al. 2000, Medal et al. 2001). Based Paraguay, and Uruguay on the surveys of 34 unsprayed eggplant fields reported here, noticeable damage to eggplant seems unlikely. In the field surveys of insects attacking eggplant in Further field and laboratory experiments conducted in 34 fields, no G. boliviana were found feeding on this Argentina (Gandolfo et al., unpublished data) and the crop (Table 1). Insects found feeding on eggplant lack of unfavourable host records in the scientific liter- included mainly the leaf-feeding beetle Diabrotica ature also corroborate the specificity and safety of G. speciosa Germar (Coleoptera: Chrysomelidae), the boliviana. Therefore, control of tropical soda apple by green peach aphid Myzus persicae (Sulz.) (Heteroptera: this leaf beetle is not expected to have any significant, Aphididae), the tobacco hornworm long-term negative impacts on non-target organisms. Paphus (Lepidoptera: Sphingidae), and an unidentified The petition to release the South-American tortoise species of spider-mite (Acari: Tetranichidae). Four of beetle G. boliviana for the control of tropical soda apple the eggplant fields in Argentina and Brazil were exam- in the USA was approved and a permit was issued by ined at least once a month for insects during their vege- the USDA-APHIS in May 2003. Field releases in tative and reproductive stages of development. Larvae, Florida were initiated on 14 May 2003. pupae and adults of G. boliviana were found on tropical soda apple plants that were growing intermixed, or close to (sometimes a few metres away) the eggplant Acknowledgements fields. The South American growers that have been growing eggplant for many years have also never found We thank Don Sudbrink, Shaharra Usnick, formerly G. boliviana attacking their crops. with the USDA-ARS in Stoneville, Mississippi, and Judy Gillmore (University of Florida) for their collabo- Discussion ration conducting host-specificity tests. This research was funded by the USDA-APHIS, and by the Florida The field release of a non-indigenous leaf feeding insect Department of Agriculture and Consumer Services, to control tropical soda apple in the continental USA Division of Plant Industry.

Table 1. Eggplant fields surveyed in Argentina, Brazil, Paraguay and Uruguay. Location Plants checked/total plants Date G. gratiana Argentina Misiones (13 fields) 6–100/6–800 Feb 98/Jan 00 0 Buenos Aires (3 fields) 20/20 Dec 98/March 00 0 Brazil Sâo Paulo (7 fields) 40–100/40–1200 Jan 97/June 98 0 (9 fields) 7–100/7–640 Nov 98/March 01 0 Paraguay Itapua (1 field) 40/40 January 2000 0 Uruguay Canelone (1 field) 100/600 April 1999 0

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