Proceedings of the XIV International Symposium on Biological Control of Weeds, pp 77-81 F.A.C. Impson, C.A. Kleinjan and J.H. Hoffmann (eds). 2-7 March 2014, Kruger National Park, South Africa.

Biological control of viarum in , USA: A successful project

Julio Medal*1, Richard Gaskalla1, Kenneth Hibbard1, Bobbie Jo Davis1, Raghavan Charudattan2, William Overholt2, Rodrigo Díaz2, Amy Roda4, Nikary Bustamante2, Stephen Hight3, Philip Stansly2, Diana Ohashi5, Robinson Pitelli6, Aldo Santana6, José Henrique Pedrosa7, Edgard Bredow7, Marcelo Vitorino8, Liliam Beal8, André Buss8, Charles Wikler9 and James Cuda2

1Florida Department of Agriculture and Consumer Services, DPI. Gainesville, FL. USA 2University of Florida, USA 3USDA-ARS, Tallahassee, FL. USA; 4USDA-APHIS Miami, FL. USA 5INTA–Cerro Azul, Misiones, 6Universidade Estadual Paulista, Jaboticabal, São Paulo, Brazil 7Universidade Federal do Paraná6, Curitiba, Paraná, Brazil 8Universidade Regional de Santa Catarina, Blumeanu, Santa Catarina, Brazil 9Universidade do Centro-Oeste, Iratí, Paraná state, Brazil

Keywords: boliviana, defoliating , pasture weed,

Abstract

Solanum viarum (Solanaceae) is an invasive native to South America that has invaded Florida grasslands and natural ecosystems. In 1988, it was first reported in Florida, USA. Currently, 600,000 ha are infested in Florida due to favorable environmental conditions and lack of natural enemies (herbivores and pathogens). This invader has spread rapidly in the majority of Florida counties and also in Alabama, Georgia, South Carolina, Texas, and Puerto Rico. was placed on the Florida and Federal Noxious Weed Lists in 1995. Control costs for Florida ranchers were estimated at $6.5 to 16 million annually. The plant is a reservoir for at least six crop viruses and major pests utilize the plant as an alternate . Solanum viarum also reduces biodiversity in natural areas by displacing native vegetation. Management practices in Florida pastures primarily involve herbicide applications and mowing which provide temporary weed suppression at an estimated annual cost of US$61 and US$47 per ha, respectively. However, application of these control methods is not always feasible in rough terrain or inaccessible areas. In June 1994, the first exploration for natural enemies was conducted in South America by University of Florida and Brazilian researchers. Host specificity tests with potential biocontrol candidates were initiated in 1998. The South American leaf-feeder beetle (Chrysomelidae) was approved for field release in Florida in 2003 and 250,723 were released from 2003 to 2011 by the Biocontrol Implementation Team which included ranchers and state and federal agencies. Post-release monitoring through Florida indicates the beetle is causing substantial defoliation, reducing stand densities and decreasing fruit production of S. viarum in Central and South Florida with no negative effects on non-target species. This is the first successful biocontrol project of a Solanum species in North America, since attempts with other Solanum species are still ongoing or incomplete.

1. Introduction movement. The infested acreage in Florida was estimated at approximately 6,000 hectares in 1990, increasing to more Solanum viarum Dunal (Solanaceae), commonly than 250,000 hectares in 1995, and it currently infests over known as tropical soda apple in the USA, is native to 600,000 hectares. Solanum viarum has spread rapidly and southeastern Brazil, northeastern Argentina, Paraguay and has been observed in the majority of Florida counties and Uruguay. It was first reported in Glades County, Florida in also in Alabama, Georgia, Louisiana, Mississippi, North 1988. The pathway of introduction is unknown, but it may Carolina, South Carolina, Texas and Puerto Rico (Bryson have been accidentally introduced with cattle carrying and Byrd Jr., 1996; Dowler, 1996, Mullahey et al., 1993, undigested seeds that were imported from Brazil (Medal, 1998; Medal et al., 2003, 2010a). This weed has become 2005). In its introduced range spread is mainly by shipping naturalized in southern Mexico and Nicaragua (Medal of cattle between states and by hay, sod and wildlife personal observation), Honduras (Díaz et al., 2008), the

Corresponding author: [email protected] 77 Medal et al.

Caribbean, Africa, India, Nepal, China (Coile, 1993; Raghavan Charudattan, Julio Medal (University of Florida) Chandra and Srivastava, 1978), and in August 2010 it was and Robinson Pitelli (Universidade Estadual Paulista, first reported in New South Wales, Australia Jaboticabal campus, São Paulo state, Brazil). Sixteen (www.dpi.nsw.gov.au/weeds/ tropical soda apple), and species of were found attacking the weed during this could pose a threat to other Pacific Ocean countries. two-week survey (Medal et al., 1996). Subsequent surveys Solanum viarum was placed on the Florida and Federal in Brazil revealed several other potential insects that may be Noxious Weed Lists in 1995. suitable as biocontrol agents of S. viarum including an undescribed Platyphora species (Coleoptera: Solanum viarum invades perennial grass pastures and Chrysomelidae) and a leaf and root feeder, Epitrix probably natural ecosystems and is unpalatable to livestock (Medal et or near parvula (Coleoptera: Chrysomelidae) (Medal et al., al., 2012). It can overrun pasture very rapidly and in only a 1996; Olckers et al., 2002; Medal et al., 2012). Four of the few years reduces forage production and decreases 16 species found during the initial 1994 survey, were livestock carrying capacity. Control costs of S. viarum for identified as potential biological control agents of Florida ranchers were estimated at US$6.5 to US$16 S. viarum: the defoliating Chrysomelid leaf beetles, million annually (Thomas, 2007). An economic analysis Gratiana boliviana Spaeth (Medal et al., 1996, 2002, 2007); from surveys conducted with the Florida Cattlemen’s Gratiana graminea Klug (Medal et al., 2010b): Metriona Association in 2006 and 2010 indicated that the biological elatior Klug (Medal et al., 1996; Gandolfo et al., 2008); and control program for S. viarum was reducing the Florida the flower bud weevil Anthonomus tenebrosus Boheman management costs of this weed by 50%. The estimated (Coleoptera: Curculionidae) (Medal et al., 2011). Host reduction in costs was US$3.25 to US$8.0 million or a specificity tests on these were initiated in 1998 by J. Medal permanent reduction of US$108 to US$266 million in total (University of Florida) in collaboration with the USDA savings (Salaudeen et al., 2012a, b). The ecological cost Biological Control Laboratory in Hurlingham, Buenos caused by S. viarum replacing pasture grasses and native Aires province, Argentina, the USDA Biological Control vegetation in conservation areas is difficult to estimate. Laboratory in Stoneville, Mississippi, and the Universidade These serve as hosts for several crop viruses Estadual Paulista, Jaboticabal, Brazil. (cucumber mosaic virus, leaf-roll virus, potato virus Y, etch virus, mosaic virus, tomato mottle Comprehensive host range studies with G. boliviana virus) and the potato fungus Alternaria solani Sorauer adults and first instar larvae were conducted from January (Pleosporales: Pleosporaceae) (McGovern et al., 1994a, 1998 to April 2000 at the quarantine facility of the Florida 1994b; McGovern et al., 1996). In addition, major insect Department of Agriculture and Consumer Services, pests use S. viarum as an alternative host, including the Biological Control Laboratory in Gainesville. A total of , Leptinotarsa decemlineata (Say) 123 plant species in 35 families were included in the feeding (Coleoptera: Chrysomelidae); green peach aphid, Myzus and oviposition preference tests (choice and no-choice). persicae (Sulzer) (Hemiptera: Aphididae); southern green The plants tested included 53 species in the Solanaceae stink bug, (L.) (Hempitera: ); (Medal et al., 2002). Open-field host specificity tests tomato hornworm, quinquemaculata (Haworth) exposing several hundred G. boliviana adults to the (: ); tobacco hornworm, Manduca cultivar ‘Black Beauty’ in Argentina (Gandolfo et sexta (L.) (Lepidoptera: Sphingidae); tobacco budworm, al., 2007), and surveys of 32 unsprayed eggplant fields in Helicoverpa virescens (Fabricius) (Lepidoptera: Argentina, Brazil, Paraguay and Uruguay during a three- Noctuidae); tomato pinkworm, Keiferia lycopersicella year period, corroborated that G. boliviana is not a of (Walsingham) (Lepidoptera: Gelechiidae); silverleaf in South America. Gratiana boliviana was whitefly, Bemisia tabaci biotype B (Bellows and Perring) unanimously approved by the Technical Advisory Group (Hemiptera: Aleyrodidae), and the soybean looper, (TAG) members in April 2002, and USDA-APHIS-PPQ Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae), granted a permit for field release in Florida in May 2003. In (Habeck et al., 1996; Medal et al., 1999; Sudbrink et al., total, 250,723 beetles were released from 2003 to 2011. 2000). Although the beetles became established throughout Florida, they are most evident in the central and southern Management of S. viarum in Florida was traditionally regions (below latitude 29º N) causing significant based on mechanical mowing and chemical herbicides. The defoliation (30-100%) and reducing fruit production from herbicide application rate varied according to the infestation 40-60 fruits per plant to zero, or to a few small or deformed level. The most common herbicides were triclopyr fruits per plant (Overholt et al., 2009, 2010; Medal and (Remedy) and 2-4D, but more recently these have been Cuda, 2010; Medal et al., 2010a, b; Medal et al., 2012; Díaz replaced by a more efficient and cheaper alternative, et al., 2014). amynopyralid (Milestone) (Mullahey, 1996; Ferrell et al., 2006; Sellers et al., 2010). Herbicides or mowing provide Several post-release studies have been conducted to only temporary weed suppression at an estimated cost of determine the impact of G. boliviana on the density of S. US$61 and $47 per ha, respectively (Thomas, 2007). viarum plants and indirect effects on fruit production and all However, application of these control methods is not always the surveys show that G. boliviana is reducing fruit feasible in rough terrain or inaccessible areas. production and plant density in central and south Florida. There are clear indications that biological control of In June 1994, the first exploration for S. viarum natural S. viarum by G. boliviana has become a key management enemies in South America was conducted by Jeff Mullahey,

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Biological control of Solanum viarum tool that can be integrated with other available management techniques including pathogens, mechanical removal, chemical herbicides, and cattle/hay/sod movement regulations to reduce S. viarum populations. The results of the post-release monitoring study in Okeechobee County, Florida on which these findings are based are presented here.

2. Materials and Methods To evaluate the effects of the leaf-feeder beetle Gratiana boliviana on a dense stand of Solanum viarum plants (more than 1,000 plants in early reproductive stage in a field approximately 0.5 ha), 500 two-three week old adult beetles, separated in 20 groups of 25 insects each, were Plate 2. Two months after the Gratiana boliviana release in randomly released over the foliage of the plants (Plate 1) on Okeechobee County, Florida. 26 October 2004 11 August 2004 in Okeechobee County in Central Florida (N 27º 41’ 15”, W 81º 01’ 71”). Plant defoliation was 4. Conclusions and Recommendations visually estimated two months after the beetle field release (26 October 2004), and the number of fruits on 20, The South-American leaf feeder beetle, Gratiana randomly selected, S. viarum plants were recorded at the boliviana, introduced and released in Florida from 2003 to time of the beetle release and again two months later. 2011, successfully established in Florida, and post-release evaluations throughout Florida indicate it is causing significant defoliation, decreasing plant density and reducing reproduction. Up to now, no non-target effects have been observed even in closely related plants in the same family, growing in the proximity of, or mixed with, the target weed. An integrated management approach including all the tactics available should be used to suppress S. viarum. No control technique should be excluded. Large weed population densities may be initially managed with mechanical mowing or herbicide applications before the S. viarum fruit set to prevent the enormous fruit/seed production and to reduce new re-infestations. Once the S. viarum population is reduced, biological control should be used to maintain the weed at low levels. Research efforts should continue to find cold tolerant biological control agents for those northern geographical regions where Plate 1. Releasing Gratiana boliviana in Okeechobee G. boliviana has not been able to establish. Studies to County, Florida. 11 August 2004 determine the economic benefits of the various management practices should now be pursued.

3. Results and Discussion Acknowledgements Defoliation of Solanum viarum two months after the The Solanum viarum biological control program was release of 500 Gratiana boliviana beetles was 100% financially supported by the United States Department of throughout the field (see Plate 2). The defoliation, Agriculture, Plant Health Inspection Service; the combined with the impact of 2 months of flooded conditions Florida Department of Agriculture and Consumer Services, produced by rain after hurricane Jeanne, resulted in the Division of Plant Industry; the University of Florida; and in complete replacement of S. viarum by the improved grass, part by the South-West Florida Water Management District. bahiagrass, Paspalum notatum Flugge (Poaceae). Fruit The authors thank Julieta Brambila (USDA-APHIS) and production per plant was negligible. Significant defoliation Cory Penca (FDACS-DPI) for providing useful suggestions levels and decreases in fruit production were found in other to improve this manuscript. post-release monitoring studies in Sumter and Polk counties, Florida (Medal, 2005; Medal et al., 2008, 2010), References and other counties through the state (Overholt et al., 2009, 2010). These findings show that G. boliviana is having a Bryson, C.T., Byrd Jr., J.D., 1996. Tropical soda apple in negative impact on S. viarum plant populations (Medal et Mississippi. In: J. J. Mullahey (ed.). Proceedings al., 2012; Díaz et al., 2014). Tropical Soda Apple Symposium, January 9-10, 1996. Bartow, Florida. Univ. of Florida-IFAS.

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