Natural Enemies of Brazilian Peppertree

Natural Enemies of Brazilian Peppertree (Sapindales: Anacardiaceae) from Argentina: Their Possible Use for Biological Control in the USA Author(s): Fernando Mc Kay, Marina Oleiro, Guillermo Cabrera Walsh, Daniel Gandolfo, James P. Cuda and Gregory S. Wheeler Source: Florida Entomologist, 92(2):292-303. 2009. Published By: Florida Entomological Society DOI: 10.1653/024.092.0213 URL: http://www.bioone.org/doi/full/10.1653/024.092.0213

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. 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 native 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 biodiversity 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 ornamental, 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, probably 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 and other Anacardiaceae species in Northeastern Argen- tina (CO, Corrientes; CH, Chaco; F, Formosa; ER, Entre Ríos; M, Misiones; SF, Santa Fé).

Astronium balansae Engl., Lithrea molleoides were placed in 2 different ﬁeld sites next to dis- (Vell.) Engl., Schinus fasciculatus (Griseb.) Schi- eased S. terebinthifolius plants. Diseased plants nus lentiscifolius March., S. longifolius (Lindl.) have wrinkled and shrunken young leaves. Two Speg., Schinus molle L. and Schinus weinmanni- branches of each test plant were tied to branches folius Engl. Voucher specimens of the plants and of living Brazilian peppertree plants that showed insects collected are deposited at the USDA-ARS- disease symptoms. SABCL, Hurlingham, Argentina. Tecmessa elegans Schaus (Lepidoptera: Not- odontidae). No-choice larval survival was evalu- Preliminary Host-range Testing ated on 12 plant species in the Anacardiaceae: A. balansae, L. molleoides, Mangifera indica L. Experiments were conducted on plant species in (mango), P. vera, P. integerrima, Schinopsis bal- the Anacardiaceae and the Sapindaceae for their ansae Engl., S. areira, S. lentiscifolius, S. molle, taxonomic relatedness to S. terebinthifolius and and S. terebinthifolius, and the Sapindaceae Car- economic importance. Special attention was paid diospermum grandiflorum Sw. and Serjania gla- to the pistachio species, Pistacia vera L., Kerman brata Kunth. Tests were conducted in a growth cultivar, (pistachio) and Pistacia integerrima Stew- chamber (25 ± 2°C: 60-80% RH; 16:8 L:D). In each art ex. Brandis (a species commonly used as root- replicate (5 to 10), 5 newly emerged larvae were stock of P. vera), which are chemically similar to placed in 0.7-L plastic containers with perforated Brazilian peppertree (Campello & Marsaioli 1975) lids and moist tissue paper. The larvae were fed and commercially important Anacardiaceae, espe- bouquets of freshly excised leaves with their peti- cially in California (Siegel et al. 2008). oles inserted in 3.6-mL water picks with water. Apocnemidophorus blandus (Pascoe) (Co- Fungus Associated with Distorted Leaves leoptera: Curculionidae). The adult feeding preference of this weevil was studied in a choice test Selected potted test plants (L. molleoides, S. in outdoor conditions at the SABCL. Two potted areira, P. integerrima and S. terebinthifolius) plants of 5 species (S. terebinthifolius, S. areira, Mc Kay et al.: Natural Enemies of Brazilian Peppertree 295

M. indica, P. vera, Kerman cultivar, and P. inte- unfolding leaves of young shoots of medium-sized gerrima) of comparable height (1.5-2 m tall) and young plants (1-2.5 m tall). Shoot tips of infested canopy size were placed in a circle in random or- S. terebinthifolius plants appeared wilted, with der, inside a 7.2-m3 walk-in cage. Eighty adult the leaf surface somewhat wrinkled, and in most weevils were released in the center of the cage cases clear yellow dots were found that corre- and allowed to feed for 60 d. sponded to the oviposition marks. In preliminary rearing attempts, we observed that larvae and RESULTS adults preferentially colonized the shoots containing the most villous leaves. Exploration Blotch Leaf Miner. The larvae of a leaf-mining gracillariid moth were observed feeding on the In total, 37 phytophagous insects and one dis- leaflets of S. terebinthifolius at several sites in Ar- ease were found associated with S. terebinthifo- gentina. Three other species of Gracillariidae lius and other Anacardiaceae species in north- (Gracillaria sp., nr. Parornix sp. and Phyllonoryc- eastern Argentina (Table 1). The insects belonged tor sp.) were reported from earlier surveys con- to the orders Hemiptera (1 species), Thysanoptera ducted in Brazil (Krauss 1963; F. Bennett, Univ. (1 species), Coleoptera (20 species), Lepidoptera of Florida unpublished report). However, speci- (12 species), and Hymenoptera (3 species) (Table mens from Argentina do not match any known 1). Of these, 9 species were recorded on S. terebin- Gracillariidae and this species will be assigned to thifolius in earlier surveys in Brazil (F. Bennett, a recently created genus (D. Davis et al. Smithso- Univ. of Florida, unpublished report; Krauss nian Institution NMNH, unpublished data). 1962; Davis & Krauss 1962, 1963; D’ Araújo et al. Females lay eggs singly on the adaxial surface 1968; Medal et al. 1999; Martin et al. 2004; Schef- of leaflets, either on the main or secondary leaflet fer & Grissell 2003). Field observations, bionomic veins. The neonate larva bores into the plant epi- data, and comments on those species deemed to dermis and makes a short mine (0.93 ± 0.08 mm; have potential as biological control agents are in- mean ± SD; n = 21) parallel to the leaf vein. After cluded below. this initial slender mine, the larval mine turns 90° and continues forming an increasingly wider Fungal Associate blotch mine in the leaf blade. The initial two thirds of a fully developed blotch mine are dark Schinus terebinthifolius plants with distorted brown and the most distal third is light green. and pock-marked leaves were observed at several One fully developed mine may remove up to 40% sites. This condition is caused by an unidentified of the leaflet photosynthetic tissue. Occasionally fungus associated with cellular distortion and hy- 2, but generally 1 blotch is found per leaflet. Ma- pertrophy (M. Rayamajhi, USDA/ARS, personal ture larvae leave the blotch through a slit in the communication). Similar symptoms were ob- light colored part and spin a silk cocoon on the served on field-collected leaves of the congeneric adaxial surface of the leaves. Although larvae of species S. weinmannifolius and S. lentiscifolius. different developmental stages were present The disease incidence of S. terebinthifolius plants year-round, the highest numbers of larvae and co- was not abundant, but fairly common. Noticeably, coons were found during the winter (Jun-Aug). young plants seem to be more susceptible. Prelim- Although most Nearctic Gracillariidae probably inary host specificity experiments showed that undergo some kind of resting phase, those feeding symptoms were only found on S. terebinthifolius on evergreen leaves apparently experience no and L. molleoides (Table 2). However, potted L. true diapause but fed whenever temperatures or molleoides plants were grown under shade and other conditions permit, producing 1 to 3 genera- high humidity, conditions in which this plant is tions per year (Davis 1987). Similarly, the Neotro- rarely seen in the field. These conditions might pical Brazilian peppertree Gracillariidae moth have been conducive to transmission of this dis- described here apparently is present year-round. ease because under natural field conditions the Occasionally large numbers of larvae were found symptoms were never seen on L. molleoides in the same stage suggesting their populations re- plants, even when they were growing near in- spond in a synchronized way to environmental fected S. terebinthifolius plants. Further studies cues. are underway to examine the identity and speci- In our field surveys, leaf blotches produced by ficity of this fungal associate species. this species were found on, S. fasciculatus, S. lentiscifolius, S. longifolius, S. terebinthifolius and S. Leaf Feeders weinmannifolius. A similar, but unidentified, blotch mine was found on leaflets of Astronium Paraleucothrips n. sp. (Thysanoptera: Thripi- balansae. Results so far indicate a preference for dae). A new species of thrips was found damaging the Schinus spp. but host specificity tests are cur- shoots of S. terebinthifolius. Large numbers of rently underway to confirm the safety of this in- light orange larvae and adults were found on the sect as a biological control agent. These studies 296 Florida Entomologist 92(2) June 2009 RGEN- A ORTHEASTERN N Abundance (up to 200 specimens per site) (up to 50 specimens per site) (up to 40 specimens per site 1 Stage NACARDIACEAE SPECIES IN collected A AND OTHER ) Distorts leavesLeaf pit gallsLeaf feeder N A; feederFruit Stem borerA N; E; Common Leaf feeder Common A Common/abundant L ALeaf feeder Uncertain Uncertain Leaf feeder Common/abundant ALeaf feederCollected on flowers ACollected on flowers ACollected on leavesCollected by beating A A Rare Collected on flowers A ACollected on flowers A rare Very Locally abundant A rare Very Rare rare Very Rare rare Very rare Very CHINUS TEREBINTHIFOLIUS S ( S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. molleoides L. lentiscifolius S. longifolius S. molle S. terebinthifolius S. weinmannifolius S. molle S. terebinthifolius S. molle S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. or near RAZILIAN PEPPERTREE or near B n. sp. sp. sp. 1 sp. 2 sp. sp. Calophya terebinthifolii Paraleucothrips Lithraeus atronotatus Compsibidion vanum Ommata Apocnemidophorus blandus balansae A. terebinthifolius S. pipitziA. rufescensA. Compsus sobrinus Conotrachelus Centrinus argentinensisEntimus imperialisHadromeropsis molleoides L. Linogeraeus Linogeraeus molleiodes L. terebinthifolius S. terebinthifolius S. . ATURAL ENEMIES COLLECTED ON TINA 1. N A, adults; E, eggs; L, larva; N, nymph; P, pupa. 1 UnknownPsyllidae Unknown Thripidae Bruchidae Cerambycidae Curculionidae ABLE Natural enemies Host plant site or mode Attack Fungal associate Hemiptera Thysanoptera Coleoptera T Mc Kay et al.: Natural Enemies of Brazilian Peppertree 297 ORTHEAST- N Abundance (up to 80 specimens per site) (up to 20 specimens per site) (up to 60 specimens per site) (up to 300 specimens per site) (up to 40 specimens per site) (up to 80 specimens per site) NACARDIACEAE SPECIES IN A 1 Stage collected AND OTHER ) Collected by beatingCollected on flowersCollected on flowers ACollected on flowers ACollected on flowers ALeaf feeder A ALeaf feeder rare Very rare Very Stem galls rare Very A rare Very Leaf miner A rare Very Leaf blotch miner L Locally abundant P L; L Common Leaf feeder Common/locally abundant Common/locally abundant Leaf miner Common/locally abundant LLeaf feederLeaf feeder L L Common LLeaf tier Common Common Rare Very L Common/locally abundant Leaf feederLeaf feederLeaf feederLeaf feeder L E; L L L Locally abundant Rare Rare Rare CHINUS TEREBINTHIFOLIUS S ( S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. terebinthifolius S. weinmannifolius S. molleoides L. terebinthifolius S. fasciculatus S. lentiscifolius S. longifolius S. terebinthifolius S. weinmannifolius S. molleoides L. terebinthifolius S. weinmannifolius S. terebinthifolius S. weinmannifolius S. terebinthifolius S. S. weinmannifolius S. RAZILIAN PEPPERTREE B ) E. utilis E. (= or near sp. sp. sp. . ATURAL ENEMIES COLLECTED ON Nicentrus Xystus 1 sp. 2 sp. 3 sp. varia Percolaspis auricapillaThermesia Crasimorpha infuscata 1 sp. terebinthifolius S. terebinthifolius S. Aceclostria musStigmella obrontundaPaectes Eutelia abscondens elegansTecmessa balansae A. terebinthifolius S. terebinthifolius S. terebinthifolius S. Nystalea ebaleaCitheronia laocoon strigilisProtoambylyx Episimus unguiculus terebinthifolius S. terebinthifolius S. terebinthifolius S. ) N RGENTINA A ONTINUED ERN 1. (C A, adults; E, eggs; L, larva; N, nymph; P, pupa. 1 Chrysomelidae Clytrinae Gelechiidae Gracillariidae 1 Unknown genus sp. Mimallonidae Nepticulidae Noctuidae Notodontidae Saturniidae Sphingidae Tortricidae ABLE Natural enemies Host plant site or mode Attack Lepidoptera T 298 Florida Entomologist 92(2) June 2009

are being complemented with ﬁeld host range surveys (F. M., unpublished data). Tecmessa elegans. This moth was described by Schaus (1901) from specimens collected in Castro, ORTHEAST- Paraná state, Brazil without reference to host N plant. Tecmessa elegans is known to occur in Ar- gentina on Lithrea brasilinensis and Lithrea sp. and in Brazil on Lithrea sp. (“aroeira”) (D’Araújo et al. 1968; Pastrana 2004) and S. terebinthifolius

Abundance (F. Bennett, Univ. of Florida, unpublished report). In the present study, eggs and larvae of T. elegans were found at 7 sites in northeastern Ar- gentina (Corrientes and Misiones provinces) feed- (up to 200 specimens per site) (up to 200 specimens per site) (up to 50 specimens per site) ing on S. terebinthifolius and the closely related

NACARDIACEAE SPECIES IN species S. weinmannifolius, which constitute new

A host records for this species in Argentina. Tec- 1 messa elegans adults (wingspan: 3 cm) are creamy white in color with 3 sinuous narrow dark lines

Stage across each forewing. They lay chalky white eggs collected

AND OTHER in compact clusters of varying number (10-80 ) eggs). There are 5 instars; the first 3 are gregari- ous, and the last 2 are generally solitary. Larval color changes progressively from burgundy in the early instars to alternate yellow and burgundy rings in the latter instars. The larvae of T. elegans are voracious leaf-feeders. The first instars skele- tonize the leaflets usually feeding on the abaxial surface. As larvae develop, they eat most of the leaf except the larger veins. In the field, although

Leaf feederLeaf feeder feederFruit A L; E; A L; E; Common/locally abundant A P; Common/locally abundant not very Common/locally abundant common, it is possible to find S. terebin- CHINUS TEREBINTHIFOLIUS

S thifolius plants with some of their branches to- ( tally defoliated by T. elegans, indicating the potential damage that could be caused by large populations of this moth. Mature larvae spin a de- bris-encrusted cocoon buried a few centimeters in soil where they pupate. Egg incubation period is approximately 10 d. The larval stage varies be-

S. weinmannifolius S. longifolius S. molle S. terebinthifolius S. weinmannifolius S. tween 20 and 25 d, and the time between cocoon formation and adult emergence is approximately RAZILIAN PEPPERTREE 20 d. The presence of eggs and larvae of T. elegans B in the field extends approximately from Dec to Apr. Several natural enemies were found emerging from different life stages of T. elegans. Eupelmi- dae (Chalcidoidea) wasps (Anastatus sp.) emerged from the eggs. Tachinid ﬂies (Lespesia spp.) and 2 different wasps, Glyptapanteles sp. (Braconidae) and 1 Ichneumonidae (Diradops sp.) were reared from mature larvae. In some cases, the Ichneu- monidae parasitoids were responsible for up to 90% of the larval mortality.

. In the no-choice tests, neonate T. elegans sur- ATURAL ENEMIES COLLECTED ON

Heteroperreyia hubrichi jorgenseniH. Megastigmus transvaalensis terebinthifolius S. areira S. lentiscifolius S. vival and development to the adult stage was re- ) N corded on all of the native Argentinean Anacardi- aceae (A. balansae, L. molleoides, S. balansae, S.

RGENTINA areira, S. lentiscifolius, S. molle, and S. terebinthi- A folius) and also on the economically important P. ONTINUED

ERN vera and P. integerrima (Table 2). Only M. indica

1. (C and the Sapindaceae species C. grandiﬂorum and S. glabrata were not suitable hosts as all larvae A, adults; E, eggs; L, larva; N, nymph; P, pupa. 1 Pergidae

ABLE died within the first 72 h of testing. However, Natural enemies Host plant site or mode Attack Hymenoptera Torymidae T Mc Kay et al.: Natural Enemies of Brazilian Peppertree 299 these conservative tests can produce false posi- During field surveys, H. jorgenseni was found not tive results that might lead to rejection of a safe only on its known natural host but also on S. len- agent (Marohasy 1998; Hill 1999). Additional tiscifolius and S. longifolius. Large numbers of tests will also be conducted including larval feed- eggs and larvae of H. jorgenseni were found in the ing choice tests, and oviposition choice tests in field between Mar and Jun. Although H. jorgens- walk-in cages, and open field conditions. More- eni was never found on S. terebinthifolius in the over, this insect needs to be tested against the field, it was possible to rear it on this plant in the species of Anacardiaceae in North America. Re- laboratory and obtain an F1 generation (D. G. & sults obtained will enable assessment of whether M. O., unpublished data). This species is not being the risk posed by T. elegans on non-target species developed for biological control of Brazilian pep- is acceptable. pertree. Aceclostria mus Vuillot (Lepidoptera: Mimal- lonidae). This sack-bearing caterpillar was occa- Gall makers sionally found feeding on leaves of S. terebinthifolius and S. weinmannifolius. It was also found oc- Crasimorpha infuscata Hodges (Lepidoptera: casionally on A. balansae and L. molleoides. The Gelechiidae). Previously reported on S. terebin- Mimallonidae comprise a small family restricted thifolius in Brazil (Krauss 1962, 1963; Davis & to the Neotropical region. The larvae feed mainly Krauss 1962), stem galls produced by this moth on leaves of Myrtaceae and Anacardiaceae (Pas- were found in the terminal branches of S. terebin- trana 2004). Records show that A. mus was col- thifolius and S. weinmannifolius, which consti- lected in Argentina on Schinus sp. (probably S. tute new host records for this species in Argen- fasciculatus), and on S. terebinthifolius in Para- tina. Galls (3-5 cm long; 0.7-0.9 cm wide) show 1 guay (Pastrana 2004). Unfortunately, the low or 2 emergence windows covered with silk, ob- numbers found in the field and the presence of Ta- served as dark, rounded marks near the ends of chinidae parasitizing up to 30% of the larvae lim- the gall. Inside each gall a single grayish larva de- ited our possibilities to rear and evaluate this spe- velops until pupation. Released in Hawaii numer- cies in the laboratory. However, based on the ous times, this moth apparently never estab- available literature and field data, we consider lished (Hight et al. 2002). that further studies should be pursued. Heteroperreyia hubrichi. This defoliating saw- Stem borers fly has been intensively studied as a biological control candidate of Brazilian peppertree in Bra- Apocnemidophorus blandus. This weevil was zil and in quarantine facilities in Hawaii and recorded on S. terebinthifolius in earlier surveys Florida (Medal et al. 1999; Vitorino et al. 2000; conducted in Brazil (F. Bennett, Univ. of Florida, Hight et al. 2003). This species was known to oc- unpublished report) and was also known from cur in Uruguay on Schinus polygama (Cav.) Ca- Paraguay and Uruguay without host plant brera, and in Argentina (Entre Ríos and Santa Fé records (Wibmer & O’Brien 1986). In Mar 2004, provinces) without reference to host plant (Smith A. blandus was found feeding on S. terebinthifo- 1990). In surveys conducted in Argentina during lius in northern Argentina. In the ensuing sur- 2004 and 2005, larvae of H. hubrichi were found veys, A. blandus was found at several sites feed- at several sites in northeastern Argentina feeding ing not only on S. terebinthifolius but also on the on S. terebinthifolius and on the closely related related species A. balansae, L. molleoides, S. len- species S. weinmannifolius. These findings con- tiscifolius, S. longifolius, S. molle and S. wein- stituted new host records for this species. Eggs mannifolius, which constitute new host records and larvae of H. hubrichi were found from Apr to for this species. Adults of A. blandus are 0.7 to 1 late Jun and again from Oct to Nov. According to cm in length, with the prothorax and anterior our surveys, H. hubrichi has 2 generations per part of the elytra covered for the most part by year in northeastern Argentina. Permits to re- white scales and with 2 small but distinct protu- lease H. hubrichi in Hawaii have not been re- berances covered by black scales on the posterior quested because host specificity studies showed third of the elytra. In the field, adults were found that it may pose risks to the native Hawaiian resting or feeding on the adaxial surface of leaves, sumac Rhus sandwicensis A. Gray (Hight et al. and immediately dropped off the plants when dis- 2003). Even though H. hubrichi was found to be turbed. The feeding damage is generally concen- sufficiently host specific for release in Florida trated on the margin of the leaves. When feeding, (Medal et al. 1999; Cuda et al. 2005), the presence the adult weevils may totally perforate the leaves, of toxins in the larvae have prevented the issu- or leave the epidermis undamaged. When this ance of a release permit (J. P. C., unpublished damage is old, this layer takes on a whitish color- data). ation that resembles the general color of the in- According to Smith (1990), another sawfly spe- sect which might help to conceal its presence. cies Heteroperreyia jorgenseni (Jörgensen) was re- No A. blandus larvae have been found in the corded on S. molle in Argentina and Paraguay. field. Adults collected in the field and kept in out- 300 Florida Entomologist 92(2) June 2009 door cages containing potted S. terebinthifolius biological control as long as its oviposition behav- plants did not reproduce. Although they fed on iour proves to be sufficiently host specific. The leaves and survived for 1 to 3 months, no eggs available literature records and field host data ac- were found on the leaves, stems, or roots. How- cumulated in Argentina and Brazil (D’Araújo et ever, A. blandus eggs were found inside root frag- al. 1968; Pastrana 2004; F. Bennett, Univ. of Flor- ments buried in wet peat moss in 1-liter plastic ida, unpublished report, G. S. W., unpublished containers. The females exhibited a characteristic data) suggest that this leaf-feeding moth has a behavior as they prepared to oviposit, chewing a narrow field host range. Under restricted condi- small hole in the root, and then depositing a sin- tions, many herbivorous insect species display ex- gle, rounded, yellowish egg. The hole was then tended host ranges (Harris & Zwölfer 1968; Wap- covered with frass concealing the oviposition scar. shere 1989; Cullen 1990; Shepherd 1990; Olckers Two other Apocnemidophorus species, A. pipi- et al. 1995; McCoy et al 2003). The acceptance by tzi (Faust) and A. rufescens (Pascoe), were col- T. elegans of Pistacia species and most of the na- lected on S. terebinthifolius in northeastern Ar- tive Anacardiaceae species included in the first gentina. Previously reported on S. terebinthifolius host-specificity tests could be a result of the arti- in Brazil (F. Bennett, Univ. of Florida, unpub- ficial conditions in cages. Future studies that clar- lished report), A. pipitzi was also known to occur ify the present results should include: additional in Argentina and Uruguay with no host records multiple-choice oviposition tests (walk-in cage), available (Wibmer & O’Brien, 1986). In the open-field trials involving releases of T. elegans in present study, A. pipitzi and A. rufescens were plots containing Pistacia and other non-target also found on S. molle and L. molleoides, which Anacardiaceae species, and extensive field sur- constitute new locality and host records for these veys. species. Both A. pipitzi and A. rufescens were fre- Three other prospective biological control quently found coexisting with A. blandus on the agents, the leaf-mining Gracillariidae and the same plants, but in lower numbers. These adult stem-boring weevils, A. blandus and A. pipitzi weevils are leaf feeders and produce rounded also feed and develop on several native Argentine feeding marks similar to those described for A. Anacardiaceae. These species also accepted the blandus. Recently, A. pipitzi was colonized in economically important Pistacia species for ovipo- Florida under quarantine from adults collected in sition (leaf-mining Gracillariidae), and feeding Paraguay (also a new locality record), and the lar- (Apocnemidophprus weevils) at least under some vae appear to be stem borers. experimental designs. Again, additional field tri- In preliminary feeding trials, adults of A. als and walk-in cage tests should be conducted to blandus fed on S. terebinthifolius, S. areira and determine if these are potential biological control both Pistacia species offered, showing no prefer- candidates. ence for any of the species (Table 2). The adult The unpublished biological data accumulated feeding on pistachio, an important crop in the San by these authors and others on Brazilian pepper- Joaquin valley in California (Duke 1989; Siegel et tree suggest that it may be difficult to find a com- al. 2008) may preclude the use of this insect as a pletely monophagous species among the natural biological control agent in the USA. In addition, enemy fauna on Brazilian peppertree. The terpe- the fact that in the field, A. blandus was collected noid chemical compounds obtained from the on most of the Anacardiaceae species coexisting leaves and bark of S. terebinthifolius are very with S. terebinthifolius may indicate an unaccept- similar to those isolated from Pistacia species ably broad host range. The field collections of A. (G. S. W., unpublished data). In fact, they are pipitzi have been more limited due to its relative even more similar than those isolated from other scarcity but suggest that the ecological host range species of Schinus (Campello & Marsaioli 1975). of this species is not restricted solely to S. terebin- This evidence, and the oligophagous habits of thifolius. However, additional studies such as ovi- the Brazilian peppertree fauna, could prompt a position and larval development tests are needed discussion of the potential threat posed by these to evaluate the potential of all these weevil spe- prospective agents to cultivated Pistacia species cies as biological control agents for S. terebinthifo- in the US. None of these natural enemies found lius. on Brazilian peppertree are recorded pests of Pistacia plantations in Argentina. Moreover pis- DISCUSSION tachio is cultivated in areas with climatic conditions (hot, dry summers and cool winters) very After 3 years of intensive surveys in north- different from the ones that are suitable for Bra- eastern Argentina combined with our preliminary zilian peppertree and its natural enemies (tropi- host-range studies, it is possible to obtain a prior- cal conditions with high humidity). Due to these itized list of potential biological control agents for differences in climatic requirements it seems un- Brazilian peppertree. likely that the environmental conditions overlap The leaf-feeding moth T. elegans is still consid- between the Pistacia plantations in the US and ered a potential candidate for S. terebinthifolius these insects. Mc Kay et al.: Natural Enemies of Brazilian Peppertree 301

Although the present work targets the most BENNETT, F. D., AND HABECK, D. H. 1991 Brazilian pep- promising known natural enemies associated with pertree—Prospectives for biological control in Flori- S. terebinthifolius populations in Argentina, sur- da, pp. 23-33 In T. D. Center, R. F. Doren, R. L. Hof- veys are not complete and are continuing through- stetter, R. L. Myers, and L. D. Whiteaker [eds.], out the plant’s range in South America. New her- Proc. Symp. Exotic Pest Plants, 2-4. November 1988, Miami, FL. U. S. Dept. Interior, National Park Ser- bivore species found during field surveys in Brazil vice, Washington, DC. 387 pp. and Paraguay during 2006-2008 support this as- CAMPELLO, J. D., AND MARSAIOLI, A. J. 1975. Ter- sertion (Razowski & Brown 2008). Additional ex- ebenthifolic acid and bauerenone: new terpenoids plorations might be continued especially focused ketones from Schinus terebinthifolius. Phytochemis- on seed feeders, flower feeders, and the stem and try, 14: 2300-2302. root borer guilds. We consider that classical biolog- CASSANI, J. R. 1986. Arthropods on Brazilian pepper- ical control of Brazilian peppertree in the US tree, Schinus terebinthifolius (Anacardiaceae), in based on the introduction of specific natural ene- south Florida. Florida Entomol. 69: 184-196. mies from South America has great potential. CASSANI, J. R., MALONEY, D. R., HABECK, D. H., AND BENNETT, F. D. 1989. New insect records on Brazil- ian peppertree Schinus terebinthifolius (Anacardi- ACKNOWLEDGMENTS aceae), in south Florida. Florida Entomol. 72: 714- 716. We appreciate the generous contributions of numer- CUDA, J. P., FERRITIER, A. P., MANRIQUE, V., AND MED- ous workers to this effort. We thank Muñoz, J. D. Uni- AL, J. C. [EDS.]. 2006. Florida’s Brazilian Peppertree versidad Nacional de Entre Ríos, Paraná, Argentina for Management Plan, 2nd edition: Recommendations assistance with identification of the Anacardiaceae of from the Brazilian Peppertree Task Force, Florida Argentina. For the identification of different insect Exotic Pest Plant Council, April 2006. Available at groups we thank O’Brien, C. (Curculionidae) Greenval- http://ipm.ifas.ufl.edu/reports/BPmanagPlan.pdf. ley, AZ, USA; Burckhardt, D. (Psyllidae) Naturhis- CUDA, J. P., MEDAL, J. C., VITORINO, M. D., AND HA- torisches Museum, Switzerland; Cabrera, N. BECK, D. H. 2005. Supplementary host specificity (Chrysomelidae) and Aquino, D. (Chalcidoidea) Museo testing of the sawfly Heteroperreyia hubrichi, a can- de La Plata, Argentina; Avalos, S. (Tachinidae) Univer- didate for classical biological control of Brazilian sidad de Córdoba, Argentina; Di Dorio, O. (Ceramby- peppertree, Schinus terebinthifolius, in the USA. cidae) Universidad de Buenos Aires, Argentina; BioControl 50: 195-201. Navarro, F. (Mimallonidae) Universidad Nacional de CULLEN, J. M. 1990. Current problems in host-specific- Tucumán, Argentina; Whitfield, J. (Braconidae) Univer- ity screening, In E. S. Delfosse, [ed.], Proc. VII Intl. sity of Illinois; Wahl, D. (Ichneumonidae) American En- Symp. Biol. Control of Weeds, 6-11. March 1988, tomological Institute; Prinsloo G. (Torymidae) ARC- Rome, Italy. Instituto Sperimentale per la Patologia Plant Protection Research Institute; Becker V. O. Vegetale Ministerio dell’ Agicoltura e delle Foreste, (Gelechiidae) Instituto Iraçu, Reserva Serra Bonita, Rome/CSRIO, Melbourne, Australia. 701 pp. Brazil; Brown, J. W. (Episimus); Pogue, M. G. (Nystalea DAVIS, C. J., AND KRAUSS, N. L. 1962. Recent introduc- ebalea, Protambulyx strigilis; Tecmessa elegans); Davis, tions for biological control in Hawaii - VII. Proceed- D. R. (Gracillariidae), Nakahara, S. (Paraleucothrips n. ings, Hawaiian Entomol. Soc. 18: 125-129. sp.) Smith, D. R. (Symphyta) all from the USDA/ARS/ DAVIS, R. D. 1987. Gracillariidae (Tinoidea), pp. 372- SEL. For the identification of the fungal pathogen we 378 In F. W. Stehr [ed.], Immature insects. V. 1, thank Rayamajhi, M. USDA/ARS/IPRL Ft. Lauderdale, Kendall/Hunt Publishing Company, Dubuqueque, FL USA. We thank C. Cagnotti for technical assistance IA. 754 pp. during this study. We thank S. Schooler (CSIRO), S. D’ ARAÚJO E SILVA, A. G., GONÇALVES, C. R., GALVÃO, Hight (USDA-ARS-CMAVE), A. Peard Bugliani, and J. D. M., GONÇALVES, A. J. L., GOMES, J., SILVA, M. N., Briano (SABCL) for valuable comments and sugges- AND DE SIMONI, L. 1968. Quarto catálogo dos insetos tions on the manuscript. This project was partially que vivem nas plantas do Brasil. Seus parasitos e funded by Florida Department of Environmental Pro- predadores. Parte II, 1. 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