Natural Enemies of Brazilian Peppertree (Sapindales: Anacardiaceae) from Argentina: Their Possible Use for Biological Control in the Usa
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292 Florida Entomologist 92(2) June 2009 NATURAL ENEMIES OF BRAZILIAN PEPPERTREE (SAPINDALES: ANACARDIACEAE) FROM ARGENTINA: THEIR POSSIBLE USE FOR BIOLOGICAL CONTROL IN THE USA FERNANDO MC KAY1, MARINA OLEIRO1, GUILLERMO CABRERA WALSH1, DANIEL GANDOLFO1*, JAMES P. CUDA2 AND GREGORY S. WHEELER3 1South American Biological Control Laboratory, USDA-ARS, Hurlingham, Argentina E-mail: [email protected] *Deceased 2Entomology & Nematology Department, Institute of Food & Agricultural Sciences, University of Florida, P.O. Box 110620, Gainesville, Florida 32611-0620 3Invasive Plant Research Laboratory, USDA/ARS, University of Florida, 3225 College Avenue, Ft. Lauderdale, Florida 33314 ABSTRACT Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) is a perennial tree na- tive to Argentina, Brazil, and Paraguay. The plant was introduced into the USA before 1900. Originally grown as an ornamental, Brazilian peppertree is now considered an noxious plant in Hawaii and Florida, where it is ranked among the most important threats to biodi- versity in natural areas. Recent surveys conducted in northeastern Argentina recovered one fungus associated with distorted leaves and 36 phytophagous insects collected on Brazilian peppertree. A leaf-feeding notodontid moth, a new species of gracillariid leaf blotch miner, and a stem-boring weevil have been selected for further studies to determine their potential as biological control agents of Brazilian peppertree in the USA. The results of these surveys are summarized herein and descriptions are included of the insects that are considered most promising for biological control of this weed. Key Words: foreign exploration; classical biological control; Schinus terebinthifolius; host range; invasive weed; Florida Everglades RESUMEN Schinus terebinthifolius Raddi, (Anacardiaceae) es un árbol perenne nativo de Argentina, Brasil, y Paraguay. Introducido en los Estados Unidos antes de 1900, como especie ornamen- tal, S. terebinthifolius es considerada una planta nociva en los estados de Florida y Hawaii, donde amenaza la biodiversidad de áreas naturales. Inspecciones de campo recientes en el noreste de Argentina revelaron la presencia de un hongo asociado a hojas deformadas y 36 artrópodos fitófagos recolectados de S. terebinthifolius. Un Notodontidae desfoliador, un Gracillariidae minador de las hojas, y un Curculionidae minador del tallo han sido seleccio- nados para realizar estudios que determinen su potencial como agentes de control biológico de S. terebinthifolius en los Estados Unidos. El presente trabajo resume el resultado de las inspecciones de campo y las descripciones de los artrópodos considerados más promisorios para el control biológico de S. terebinthifolius en los Estados Unidos. Translation by the authors. Brazilian peppertree (Schinus terebinthifolius considered an invasive species in Florida, Califor- Raddi, Anacardiaceae) is a Neotropical species nia, Texas, and Hawaii (Randall 2000; HSASC whose native range extends along the Atlantic 2001; FLEPPC 2005; USDA, NRCS 2009). In its coast of Brazil, from Recife south to Rio Grande do exotic range, the tree decreases the biodiversity of Sul, and west to north-eastern Argentina and ad- infested natural areas by aggressively invading a jacent Paraguay (Barkley 1944, 1957, unpub- variety of coastal and upland habitats (Mytinger lished data). This species has been introduced to & Williamson 1987; Gann et al. 2001). In Florida, many countries around the world as an ornamen- infestations of Brazilian peppertree are estimated tal (Morton 1978; Panetta & McKee 1997). Cur- to occupy over 283,400 ha in central and south rently, Brazilian peppertree is listed as a prohib- Florida (Wunderlin & Hansen 2003; Cuda et al. ited plant and a noxious weed in Florida, and is 2006). Brazilian peppertree constitutes not only a Mc Kay et al.: Natural Enemies of Brazilian Peppertree 293 threat to natural areas but also to agriculture and and causes on average 30% mortality to Brazilian cattle production in Florida and Hawaii (Morton peppertree seeds (Wheeler et al. 2001). However, 1978; Ewel 1986; Yoshioka & Markin 1991). In the continuous spread of Brazilian peppertree mo- Florida, it is an important alternate host for the tivated the search for additional natural enemies exotic diaprepes root weevil, Diaprepes abbrevi- against this weed. Explorations were conducted in ates (L.), a serious pest of citrus and ornamentals northern Argentina, an area that had not been sur- (McCoy et al. 2003). This species produces allelo- veyed previously, and seems to be the most likely pathic compounds that suppress the growth of center of origin of the Schinus genus, with 22 of the other plant species (Gogue et al. 1974; Morgan & 30 known species (Barkley 1944; Muñoz 2000). The Overholt 2005, Donnelly et al. 2008). Brazilian results of these surveys indicate that Argentine peppertree is also suspected of causing allergic re- Brazilian peppertree populations harbor natural actions and respiratory illnesses in sensitive hu- enemies not previously reported. In this paper we mans from volatiles released by the leaves, flow- present biological notes, distribution, and host ers, and fruit (Morton 1978). Conservation orga- records of selected natural enemies of Brazilian nizations consider Brazilian peppertree a high- peppertree found in Argentina. We also discuss priority target due to its already widespread oc- their potential as biological control agents against currence and great potential to expand its range Brazilian peppertree in the USA. (Randall 1993). Biological control of Brazilian peppertree has a MATERIALS AND METHODS long history; efforts began in Hawaii in the 1950s and resulted in the release of 3 insect species: a Exploration gall-forming caterpillar, Crasimorpha infuscata Hodges (Lepidoptera: Gelechiidae), a defoliating The surveyed area was selected considering caterpillar, Episimus utilis Zimmerman (Lepi- published distribution records of S. terebinthifo- doptera: Tortricidae), and a seed-feeding beetle, lius in Argentina (Muñoz 2000). Extensive explor- Lithraeus atronotatus (Pic) (Coleoptera: atory trips were made along the main roads of the Bruchidae) (Davis & Krauss 1962; Krauss 1962, provinces of Entre Ríos, Corrientes, Misiones and 1963; Hight et al. 2002). Only the last 2 species Formosa, in the northeast of Argentina, between established field populations in Hawaii, but they Mar 2004 and Jan 2007 (Fig. 1). In total, 18 sur- are exerting only negligible control of the weed veys were conducted with 125 sites inspected. population (Hight et al. 2002). In Florida, explo- Most sites were visited twice a year to account for ration for biological control agents of this weed seasonal variations in herbivore presence and was initiated in the 1980s and 1990s. Surveys of abundance. Brazilian peppertree plants occurred the insect fauna associated with Brazilian pep- as large isolated trees in undisturbed areas or as pertree in its adventive Florida range found 115 shrubby stands on disturbed roadsides, where insect species, most of which were generalists or they are periodically cut and grow back from the potential agricultural pests and thus were unsuit- coppiced stumps. Insects were collected by visual able as biological control agents for biological con- inspection, beating sheets, and by rearing in- trol (Cassani 1986; Cassani et al. 1989). fested plant material (e.g., fruits, leaves, limbs, Exploration in the native range of Brazilian galls) for subsequent emergence in the laboratory. peppertree in South America revealed the pres- Insect species were considered to be “very rare”, ence of at least 200 species of natural enemies “rare” or “common” if present in less than 10%, (Bennett et al. 1990; Bennett & Habeck 1991). 10-30%, and more than 30% of the sampled sites, Three insects were selected for further studies in respectively. Species designated as “abundant” Florida: the leaf-feeding sawfly Heteroperreyia hu- were those that were found in high numbers brichi Malaise (Hymenoptera: Pergidae), the sap- when encountered, but were not necessarily com- sucking thrips Pseudophilothrips ichini Hood mon (e.g., “locally abundant”). Natural enemies (Thysanoptera: Phlaeothripidae), and the defoliat- were prioritized according to their perceived po- ing caterpillar E. unguiculus Clarke (= E. utilis, tential for control of Brazilian peppertree. The cri- Rozowski & Brown 2008) (Medal et al. 1999; Hight teria used were their apparent specificity as de- et al. 2002; Martin et al. 2004). To date, none of termined from field observations (see next sec- these biological control candidates has been re- tion), preliminary host specificity studies, pub- leased in Florida. The only known stenophagous lished records and a subjective assessment of the herbivore feeding on Brazilian peppertree in the ability of a species to damage the weed in terms of continental USA is a seed-feeding wasp, Megastig- defoliation, or stunting growth. mus transvaalensis (Hussey) (Hymenoptera: To- rymidae). This adventive wasp, which attacks Field Host Range Rhus spp. in its native range of South Africa, prob- ably entered Florida with the gourmet pink pep- Populations of other members of the Anacardi- percorn trade (Habeck et al. 1989; Scheffer & Gris- aceae sympatric with S. terebinthifolius were in- sell 2003). It has been found in Florida and Hawaii spected on a regular basis. These species included 294 Florida Entomologist 92(2) June 2009 Fig. 1. Main collecting sites of Schinus terebinthifolius