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Arthropod community associated with tropical soda apple and natural enemies of Gratiana boliviana (Coleoptera: Chrysomelidae) in Florida.

Tropical soda apple, Solanum viarum Dunal (Solanaceae), is a 1.5-m-tall perennial shrub native to tropical regions of South America. First reported in Florida in 1988, tropical soda apple rapidly became a major weed in pastures and conservation areas across the southeastern United States (Mullahey 1996). In pastures, tropical soda apple competes with forages resulting in reduced stocking rates (Mullahey et al. 1998). Florida ranchers spent an average of $44 per acre on chemical and mechanical control costs on tropical soda apple in 2006 (Thomas 2007). Additionally, this plant is an alternate host of several diseases of solanaceous crops (McGovern et al. 1994; Adkins et al. 2007).

A biological control program of tropical soda apple was initiated in 1994, and several natural enemies were collected in Brazil, Argentina and Paraguay (Medal et al. 1996), including Gratiana boliviana Spaeth (Coleoptera: Chrysomelidae). This host specific beetle was first released into Florida in May 2003, and by 2008 approximately 180,000 beetles had been released (Overholt et al. 2009). Experiments conducted in central Florida demonstrated that beetle populations increased during the summer and remained very low during the coldest months of the year from Dec to mid-Mar (Overholt et al. 2010). Beetle populations were more abundant on plants located in open pastures compared to those in shaded hammocks (Diaz et al. 2011). In a four-year study, Overholt et al. (2010) demonstrated that tropical soda apple densities decreased by 90% two yr after beetle release. Survival from egg to adult in closed cages was 51% compared to 15% in open cages (Manrique et al. 2011), thus revealing the impact of biotic factors on G. boliviana populations. Because of the presence in Florida of many solanaceous plants, we inventoried the herbivores associated with tropical soda apple with the hypothesis that many would expand their host ranges to include the novel resource. Additionally, because of the importance of G. boliviana as a biological control agent of tropical soda apple, we inventoried its natural enemies in Florida.

Arthropods were collected from 2004 to 2011 at two G. boliviana mass rearing facilities in Fort Pierce, Florida and from several natural infestations on ranches or conservation areas in central and south Florida. Collection methods for insect herbivores and predators included hand catching, aspiration, rearing, and the use of beating cloths. Lepidopteran larvae found feeding on tropical soda apple were reared in the laboratory until adult emergence and then identified. Parasitoids were reared from G. boliviana pupae, and field observations of predation were made. Entomopathogens of G. boliviana were identified using light microscopy by Dr. Drion Boucias at the University of Florida, and arthropods were identified by personnel at the Florida Department of Agriculture and Consumer Services, Division of Plant Industry (DPI), Gainesville, Florida, and the Systematic Entomology Laboratory, United States Department of Agriculture, Beltsville, Maryland. All arthropods collected from tropical soda apple from 1994 to 2011 are included in the DPI database.

A total of seven mite species and 75 species of insect herbivores were collected from tropical soda apple in Florida (Table 1). The host specificity of these species ranged from Solanum specialists to generalists and included major pests of agricultural crops as well as ornamental plants. The high diversity of insect herbivores found in this study is explained in part by the presence of close tropical soda apple relatives in Florida, including 27 species in the genus Solanum and 31 species in other genera of Solanaceae (Wunderlin & Hansen 2008). Based on field observations, tropical soda apple is an attractive host for many agriculturally important insect pests such as Leptinotarsa decimlineata (Say) and L. juncta (Germar) (Chrysomelidae), Manduca sexta L. (Sphingidae), Bemisia tabaci (Gennadius) (Aleyrodidae), Aphis gossypii Glover (Aphididae) and Lineodes integra Zeller (Pyralidae) (Table 1), and therefore may serve as a reservoir on which pest populations may increase before moving into crops.

A total of one mite species, 19 species of spiders and 30 species of predatory insects were found on tropical soda apple (Table 2). Predators observed feeding on G. boliviana larvae and pupae included Geocoris punctipes (Say) (Lygaidae), Sinea sp. (Reduviidae), Perillis bioculatus (Fabricius), Stiretrus anchorago (Fabricius) (Pentatomidae), Tupiocoris notatus (Distant) (Miridae), Solenopsis invicta Buren (Formicidae), and the spider Peucetia viridans (Hentz) (Oxyopidae). The mirid species found in this study are facultative predators, and they comprised up to 95% of the predators found on tropical soda apple in central Florida (Manrique et al. 2011). Pupal parasitoids of G. boliviana included Conura side (Walker) (Chalcidae), Brasema sp. (Eupelmidae), and Aprostocetus nr. cassidis (Eulophidae). Because C. side also attacks lepidopteran larvae (Mitchell et al. 1997) and because of the taxonomic uncertainty of Brasema sp. and Aproctocetus nr. cassidis, we cannot conclude that any specialist natural enemies attack G. boliviana in Florida. The exploitation of G. boliviana by these parasitoids was reported three yr after its release in Florida (K. Hibbard, unpublished data). This relatively short time to host exploitation is similar to that which has been documented in other weed biological control programs (Hill & Hulley 1995; Kula et al. 2010, but see Christensen et al. 2011). Two parasitoids have been reported attacking the native Gratiana pallidula (Boheman) in Arkansas, i.e., a eulophid, Tetrastichus, and a chalcid, Conura sanguineiventirs (Cresson) (Rolston et al. 1965). However, these were not found attacking G. boliviana in Florida. Entomopathogens recovered from G. boliviana included Nosema sp. (Microspora: Nosematidae), Mattesia oryzaephili Ormieres (Negregarinorida: Lipotrophidae), and a short gram-negative bacteria. The abundance of parasitoids and entomopathogens of G. boliviana was higher inside the mass rearing facilities compared to field conditions where predators (ants, spiders and mirids) were more abundant (Diaz et al. 2011).

SUMMARY

Arthropods associated with the exotic weed tropical soda apple were collected in Florida. We found that tropical soda apple is a suitable host for several insect pests of agricultural and ornamental plants. Additionally, we report several predators, parasitoids and entomopathogens of Gratiana boliviana, a biological control agent of tropical soda apple.

REFERENCES CITED

ADKINS, S., KAMENOVA, I., ROSSKOPF, E. N., AND LEWANDOWSKI, D. J. 2007. Identification And Characterization Of A Novel tobamovirus from tropical soda apple in Florida. Plant Dis. 91: 287-293.

CHRISTENSEN, R. M., PRATT, P. D, COSTELLO, S. L., RAYAMAJHI, M. B., AND CENTER, T. D. 2011. Acquired natural enemies of the weed biological control agent Oxyops vitiosa (Colepotera: Curculionidae). Florida Entomol. 94: 1-8.

DIAZ, R., AGUIRRE, C., WHEELER, G. S., LAPOINTE, S. L., ROSSKOPF, E., AND OVERHOLT, W. A. 2011. Differential performance of tropical soda apple and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae) in open and shaded habitats. Environ. Entomol. 40: 1937-1447.

HILL, M. P., AND HULLEY, P. E. 1995. Host-range extension by native parasitoids to weed biocontrol agents introduced to South Africa. Biol. Cont. 5: 297-302.

KULA, R. R., BOUGHTON, A. J., AND PEMBERTON, R. W. 2010. Stantonia pallida (Ashmead) (Hymenoptera: Braconidae) reared from Neomusotina conspurcatalis Warren (Lepidoptera: Cambridae), a classical biological control agent of Lygodium microphyllum (Cav.) R. Br. (Polypodiales: Lygodiaceae). Proc. Entomol. Soc. Washington. 112: 61-68.

MANRIQUE, V., DIAZ, R., HIGHT, S. D., AND OVERHOLT, W. A. 2011. Evaluation of mortality factors using life table analysis of Gratiana boliviana, a biological control agent of tropical soda apple in Florida. Biol. Control. 59: 354-360.

MCGOVERN, R. J., POLSTON, J. E., AND MULLAHEY, J. J. 1994. Solanum viarum: Weed reservoir of plant viruses in Florida. Int. J. Pest Manag. 40: 270-273.

MEDAL, J. C., CHARUDATTAN, R., MULLAHEY, J. J., AND PITELLI, R. A. 1996. An exploratory insect survey of tropical soda apple in Brazil and Paraguay. Florida Entomol. 79: 70-73.

MITCHELL, E. R., HU, G. Y., AND OKINE, J. S. 1997. Diamondback moth (Lepidoptera: Plutellidae) infestation and parasitism by Diadegma insulare (Hymenoptera: Ichneumonidae) in collards and adjacent cabbage fields. Florida Entomol. 80: 54-62

MULLAHEY, J. J. 1996. Tropical soda apple (Solanum viarum Dunal), a biological pollutant threatening Florida. Castanea 61: 255-260.

MULLAHEY, J. J., SHILLING, D. G., MISLEVY, P., AND AKANDA, R. A. 1998. Invasion of tropical soda apple (Solanum viarum) into the U.S.: Lessons learned. Weed Tech. 12: 733-736.

OVERHOLT, W. A., DIAZ, R., HIBBARD, K. L., RODA, A. L., AMALIN, D., FOX, A. J., HIGHT, S. D., MEDAL, J. C., STANSLY, P. A., CARLISLE, B., WALTER, J. H., HOGUE, P. J., GARY, L. A., WIGGINS, L. F., KIRBY, C. L., AND CRAWFORD, S. C. 2009. Releases, distribution and abundance of Gratiana boliviana (Coleoptera: Chrysomelidae), a biological control agent of tropical soda apple (Solanuma viarum, Solanaceae) in Florida. Florida Entomol. 92: 450-457.

OVERHOLT, W. A., DIAZ, R., MARKLE, L., AND MEDAL, J. C. 2010. The effect of Gratiana boliviana (Coleoptera: Chrysomelidae) herbivory on growth and population density of tropical soda apple (Solanum viarum) in Florida. Biocontrol Sci. Techn. 20: 791-807.

ROLSTON, L. H., MAYES, R., EDWARDS, P., AND WINGFIELD, M. 1965. Biology of the eggplant tortoise beetle (Coleoptera: Chrysomelidae). J. Kans. Entomol. Soc. 38: 362-366.

THOMAS, M. 2007. Impact of tropical soda apple on Florida's grazing land. The Florida Cattleman's and Livestock J. 71: 33.

WUNDERLIN, R. P., AND HANSEN, B. F. 2008. Atlas of Florida Vascular Plants (http://www.plantatlas.usf. edu/).[S. M. Landry and K. N. Campbell (application development), Florida Center for Community Design and Research.] Institute for Systematic Botany, Univ. South Florida, Tampa, Florida.

R. DIAZ (1), K. HIBBARD (2), A. SAMAYOA (1) AND W. A. OVERHOLT (1)

(1) Biological Control Research and Containment Laboratory, Indian River Research and Education Center, University of Florida, Fort Pierce, FL

(2) Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Fort Pierce, FL
TABLE 1. HERBIVOROUS ARTHROPODS ASSOCIATED WITH TROPICAL SODA APPLE,
SOLANUM VIARUM, IN FLORIDA.

Order: Family Species

Acari: Acaridae Undetermined
Acari: Eriophyidae Aceria sp.
 Aculops lycopersici (Massee)
Acari: Tarsonemidae Tarsonemus sp.
Acari: Tenuipalpidae Brevipalpus californicus (Banks)
 Tetranychus evansi Baker and Pritchard
Acari: Winterschmidtiidae Czenspinskia transversostriata (Oudemans)
Coleoptera: Anthicidae Acanthinus argentinus (Pic)
Coleoptera: Cerambycidae Styloleptus biustus (LeConte)
Coleoptera: Chrysomelidae Diabrotica undecimpunctata Barber
 Disonycha glabrata (Fabricius)
 Epitrix fasciata Blatchley
 Erepsocassis rubella (Boheman)
 Gratiana boliviana Spaeth (1)
 Leptinotarsa decimlineata (Say) (1)
 Leptinotarsa juncta (Germar) (1)
 Plagiometriona clavata (Fabricius)
Coleoptera: Curculionidae Faustinus cubae (Boheman)
Coleoptera: Elateridae Conoderus rudis Brown
Coleoptera: Languriidae Loberus sp.
Coleoptera: Latridiidae Undetermined
Coleoptera: Phalacridae Undetermined
Coleoptera: Tenebrionidae Bothrotes canaliculatus (Say)
Diptera: Agromyzidae Liriomyza trifolii (Burgess)
Diptera: Cecidomyiidae Undetermined
Diptera: Chloropidae Undetermined
Diptera: Ephydridae Leptopsilopa similis (Coquillett)
Diptera: Lauxaniidae Camptoprosopella verticalis (Loew)
Diptera: Muscidae Atherigona orientalis Schiner
Hemiptera: Aleyrodidae Bemisia tabaci (Gennadius) (1)
 Trialeurodes abutilonea (Haldeman)
Hemiptera: Alydidae Stenocoris tipuloides (DeGeer)
Hemiptera: Anthocoridae Xylocoris vicarius (Reuter)
Hemiptera: Aphididae Aphis gossypii Glover (1)
Hemiptera: Cercopidae Clastoptera xanthocephala Germar
 Prosapia bicincta (Say)
Hemiptera: Cicadellidae Planicephalus flavicosta (Stal)
Hemiptera: Coccidae Pulvinaria urbicola Cockerell
Hemiptera: Coreidae Anasa scorbutica (Fabricius)
 Leptoglossus sp.
 Phthia picta (Drury)
Hemiptera: Delphacidae Delphacodes sp.
Hemiptera: Dictyopharidae Undetermined
Hemiptera: Lygaeidae Ischnodemus brunipennis (Germar)
 Paromius longulus (Dallas)
 Pseudopachybrachius vinctus (Say)
Hemiptera: Membracidae Entylia carinata (Foster)
Hemiptera: Miridae Collaria oculata (Reuter)
 Cyrtopeltis modesta (Distant) (1)
 Dicyphus minimus Quaintance (1)
Hemiptera: Pentatomidae Arvelius albopunctatus (De Geer)
 Euschistus obscurus (Palisot de Beauvois)
 Euschistus quadrator Rolston
 Euschistus servus (Say)
 Mormidea lugens (Fabricius)
 Proxys punctulatus (Palisot de Beauvois)
Hemiptera: Pseudococcidae Maconellicoccus hirsutus (Green)
 Palmicultor browni nr. (Williams)
 Planococcus citri (Risso)
Hemiptera: Pyrrhocoridae Dysdercus sp.
Hemiptera: Rhopalidae Niesthrea sidae (Fabricius)
Hymenoptera: Halictidae Augochloropsis metallica (Fabricius)
Lepidoptera: Arctiidae Estigmene acrea (Drury)
 Hypercompe scribonia (Stoll)
 Hyphantria cunea (Drury)
Lepidoptera: Gelechiidae Undetermined
Lepidoptera: Noctuidae Enigmogramma basigera (Walker)
 Heliothis subflexa (Guenee)
 Heliothis virescens (Fabricius)
 Mocis latipes (Guenee)
 Mocis sp.
 Plathypena scabra (Fabricius)
 Pseudoplusia includens (Walker)
 Spodoptera eridania (Cramer)
 Spodoptera latifascia (Walker)
 Spodoptera ornithogalli (Guenee)
Lepidoptera: Nymphalidae Heliconius charithonia (L.)
Lepidoptera: Pyralidae Lineodes integra Zeller (1) Pilemia
 periusalis (Walker)
Lepidoptera: Sphingidae Manduca sexta L. (1)
Lepidotera: Tortricidade Platynota flavedana Clemens
Orthoptera: Tettigoniidae Undetermined

Order: Family Importance

Acari: Acaridae
Acari: Eriophyidae
 pest of tomato
Acari: Tarsonemidae pest of crops
Acari: Tenuipalpidae pest of citrus
 pest of crops
Acari: Winterschmidtiidae
Coleoptera: Anthicidae
Coleoptera: Cerambycidae
Coleoptera: Chrysomelidae pest of crops

 pest of solanaceae

 biocontrol of TSA
 pest of tomato
 pest of Solanum spp.

Coleoptera: Curculionidae pest of Solanum spp.
Coleoptera: Elateridae pest of sweet potato
Coleoptera: Languriidae
Coleoptera: Latridiidae
Coleoptera: Phalacridae
Coleoptera: Tenebrionidae
Diptera: Agromyzidae pest of crops
Diptera: Cecidomyiidae
Diptera: Chloropidae
Diptera: Ephydridae
Diptera: Lauxaniidae
Diptera: Muscidae fruit fly
Hemiptera: Aleyrodidae pest of crops
 pest of crops
Hemiptera: Alydidae
Hemiptera: Anthocoridae
Hemiptera: Aphididae pest of crops
Hemiptera: Cercopidae
 pest of grasses
Hemiptera: Cicadellidae
Hemiptera: Coccidae
Hemiptera: Coreidae
 pest of crops

Hemiptera: Delphacidae
Hemiptera: Dictyopharidae
Hemiptera: Lygaeidae

Hemiptera: Membracidae
Hemiptera: Miridae
 pest of tomato
 pest of tomato
Hemiptera: Pentatomidae pest of Solanaceae
 pest of cotton
 pest of cotton
 pest of cotton

Hemiptera: Pseudococcidae pest of crops

 pest of crops
Hemiptera: Pyrrhocoridae
Hemiptera: Rhopalidae
Hymenoptera: Halictidae
Lepidoptera: Arctiidae pest of crops

Lepidoptera: Gelechiidae
Lepidoptera: Noctuidae

 pest of crops

 pest of soybeans
 pest of crops

 pest of crops
Lepidoptera: Nymphalidae
Lepidoptera: Pyralidae pest of Solanaceae

Lepidoptera: Sphingidae pest of tomato
Lepidotera: Tortricidade
Orthoptera: Tettigoniidae

(1) Field observations in Florida suggested that insect populations
could increase rapidly on tropical soda apple.

TABLE 2. PREDATORS, PARASITOIDS AND ENTOMOPATHOGENS FOUND ON TROPICAL
SODA APPLE PLANTS, SOLANUM VIARUM, OR RECOVERED FROM GRATIANA BOLIVIANA
IN FLORIDA.

Order: Family Species

Acari: Ascidae Undetermined
Araneae: Anyphaenidae Undetermined
Araneae: Araneidae Acanthepeira sp.
 Acanthepeira stellata (Marx)
 Argiope aurantia Lucas
 Neoscona arabesca (Walckenaer)
 Neoscona sp.
Araneae: Clubionidae Cheiracanthium inclusum (Hentz)
Araneae: Corinnidae Meriola decepta Banks
Araneae: Oxyopidae Oxyopes salticus Hentz
 Peucetia viridans (Hentz)
Araneae: Salticidae Phidippus audax (Hentz)
 Phidippus regius C. L. Koch
 Phidippus sp.
 Thiodina sp.
Araneae: Tetragnathidae Leucauge argyra (Walckenaer)
Araneae: Theridiidae Coleosoma acutiventer (Keyserling)
Araneae: Thomisidae Misumenops bellulus (Banks)
 Misumenops celer (Hentz)
 Misumenops sp.
Coleoptera: Carabidae Calleida decora (Fabricius)
Dictyotera: Mantidae Thesprotia graminis Scudder
Hemiptera: Anthocoridae Xylocoris vicarius (Reuter)
Hemiptera: Lygaeidae Geocoris punctipes (Say) (1)
Hemiptera: Miridae Engytatus modestus (Distant) (1)
 Macrolophus sp. (1)
 Tupiocoris notatus (Distant) (1)
Hemiptera: Pentatomidae Perillis bioculatus (Fabricius) (1)
 Podisus mucronatus Uhler
 Stiretrus anchorago (Fabricius) (1)
Hemiptera: Reduviidae Arilus cristatus (Linnaeus)
 Sinea sp. (1)
Hymenoptera: Braconidae Undetermined
Hymenoptera: Undetermined
 Ceraphronidae
Hymenoptera: Chalcidae Conura side (Walker) (2)
Hymenoptera: Eulophidae Aprostocetus nr. cassidis (2)
Hymenoptera: Eupelmidae Brasema sp. (2)
Hymenoptera: Formicidae Camponotus tortuganus Emery
 Crematogaster sp.
 Cyphomyrmex sp.
 Dolichoderus pustulatus Mayr
 Pseudomyrmex cubaensis (Forel)
 Solenopsis invicta Buren (1)
 Pseudomyrmex gracilis (Fabricius)
Hymenoptera: Pteromalidae Undetermined
Neuroptera: Chrysopidae Undetermined
Odonata: Coenagrionidae Ischnura hastata (Say)
 Ischnura ramburii (Selys)
Orthoptera: Gryllidae Cyrtoxipha sp.
 Oecanthus sp.
Microspora: Nosematidae Nosema sp. (3)
Negregarinorida: Mattesia oryzaephili Ormieres,
 Lipotrophidae Loubes, and Kuhl (3)
Phyllum Bacteria short gram-negative bacteria (3)

Order: Family Functional Group

Acari: Ascidae predator
Araneae: Anyphaenidae predator
Araneae: Araneidae predator
 predator
 predator
 predator
 predator
Araneae: Clubionidae predator
Araneae: Corinnidae predator
Araneae: Oxyopidae predator
 predator
Araneae: Salticidae predator
 predator
 predator
 predator
Araneae: Tetragnathidae predator
Araneae: Theridiidae predator
Araneae: Thomisidae predator
 predator
 predator
Coleoptera: Carabidae predator
Dictyotera: Mantidae predator
Hemiptera: Anthocoridae predator
Hemiptera: Lygaeidae predator
Hemiptera: Miridae facultative predator
 facultative predator
 facultative predator
Hemiptera: Pentatomidae predator
 predator
 predator
Hemiptera: Reduviidae predator
 predator
Hymenoptera: Braconidae parasitoid
Hymenoptera: parasitoid
 Ceraphronidae
Hymenoptera: Chalcidae parasitoid
Hymenoptera: Eulophidae parasitoid
Hymenoptera: Eupelmidae parasitoid
Hymenoptera: Formicidae predator
 predator
 predator
 predator
 predator
 predator
 predator
Hymenoptera: Pteromalidae parasitoid
Neuroptera: Chrysopidae predator
Odonata: Coenagrionidae predator
 predator
Orthoptera: Gryllidae predator
 predator
Microspora: Nosematidae entomopathogen
Negregarinorida: entomopathogen
 Lipotrophidae
Phyllum Bacteria entomopathogen

(1) Predator observed feeding on G. boliviana.

(2) Parasitoid reared from G. boliviana pupae.

(3) Disease recovered from infected G. boliviana.
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Title Annotation:Scientific Notes
Author:Diaz, R.; Hibbard, K.; Samayoa, A.; Overholt, W.A.
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2012
Words:2513
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