Proc. Fla. State Hort. Soc. 121:10–13. 2008.

Microlepidoptera Complex Affecting Sapodilla ( zapota van Royen) in

LISA MYERS1, JORGE E. PEÑA2*, RITA DUNCAN2, AND JOHN B. HEPPNER3 1Ministry of Agriculture and Lands, Kingston, 2University of Florida, Tropical Research and Education Center, Homestead, FL 33031 3 Florida Department of Agriculture and Consumer Services, Department of Industry, Gainesville, FL 32611

ADDITIONAL INDEX WORDS. , sapodilla, banisis, chemical control The sapodilla ( van Royen), also known as naseberry, nispero, zapote, zapotillo, chicozapote, native to and is currently grown in southern Florida. Pests and diseases are not usually considered a major problem on sapodilla; however, the larva of the small myrsusalis has been reported as an occasional pest that causes extensive damage to sapodilla blooms in Florida. Damage to buds, flower drop, and damage to 70% of have been observed (Peña, unpublished data). A preliminary survey of sapodilla groves was conducted from May to July 2002, since very little was known about this moth. The survey indicated the presence of lepidopterous pests feeding on the young , flowers, or young fruits. Three were frequently encountered: Banisia myrsusalis (Lepidoptera: ), Dichrorampha sapodilla (Lepdioptera: ), and a Zamagiria sp. (Lepidoptera: ). A test was conducted in 2006 to determine the efficacy of Fury, Novaluron, Venom, Danitol, Thiamethoxan, and Alverde for control of the sapodilla .

The sapodilla (Fig. 1; Manilkara zapota) is extensively planted Materials and Methods and consumed in Mexico, Central America, the , Colom- bia, and in some Asiatic countries (Balerdi and Crane, 2002). The SURVEY AND DESCRIPTION OF DAMAGE. A survey was carried sapodilla is a medium to large with small bisexual clusters of out from May to June 2002. Five sapodilla located at the flowers that will bear a round to oval-shaped 2–4 inches in Tropical Research and Education Center were selected. Five diameter (Balerdi and Crane, 2002). The most important clusters of flowers and fruits were collected per tree. Samples problems are several causing extensive damage were brought to the laboratory and inspected for eggs, larvae to flowers and fruit. While a new species of Tortricidae appears to and pupae of lepidopterans. Each sample was observed for the be the most common species (Heppner, 1981), less-known species presence of eggs, larvae, and pupae. Samples were placed in also cause damage to either fruit and flowers. Here we present 800-mL jars until moth emergence. Emerging were sent results 1) from a survey conducted during 2002, with a descrip- to the junior author (J.B.H.) for identification. tion of the insects and the damage caused to sapodilla, and 2) of PESTICIDE EFFICACY. The trial was conducted in an experimental a pesticide efficacy test against these lepidopteran pests. sapodilla row of trees located at the University of Florida Tropi- cal Research Center, 3 miles north of Homestead. The treatments were arranged in a RCB design consisting of four-tree plots. These trees were about 25 ft tall with 10-ft spacing between trees. One single tree was used as a barrier to separate treatments. Treatments were applied on 11 July 2006 with a hand-gun sprayer operating at 350 psi and delivering 100 gpa of finished spray (~1 gal/tree). The insecticides (Table 1) were compared for efficacy against the sapodilla moths by collecting two flower clusters (with about 3–9 flowers) from the periphery of each tree. Samples were collected before treatment and on 18, 25, 31 July and 7 Aug. 2006. Floral clusters were placed in plastic bags and brought to the laboratory where the number of damaged flowers per cluster was recorded. Data were analyzed using the GLM procedure. Means were separated (LSD) using the Student–Newman–Keuls test.

Results and Discussion Fig. 1. The sapodilla (Manilkara zapota van Royen), also known as naseberry, nispero, zapote, zapotillo, chicozapote, native to Mexico and Central America, SURVEY. A range of 10–75 flowers and 2–10 fruits were col- is currently grown in south Florida. lected per sampling date. were abundant during collec- tion, while a very small number of fruits (n = 31) were collected. *Corresponding author; phone: (305) 246-7001, ext. 223; email: [email protected]fl.edu Flowers sustained an infestation range of 10% to 53%, while 0

10 Proc. Fla. State Hort. Soc. 121: 2008. Table 1. Insecticides tested against microlepidoptera infestation of at the base of most primary setae. The frontal area of the head is sapodilla. sclerotized. The larva possesses two prespiracular setae on the Pesticide Product Dose/acre prothorax and the Pi group setae are bisetose on the mesothorax Fenpropathrin Danitol 2.4EC 15 oz and metathorax. Crochets are present on the ventral prolegs on Alverde BAS 320 16 oz abdominal segments A3–A6 and A10. The crochets are biordinal Dinotefuran Venom 70 SG 4 oz and are arranged in a circle on the ventral prolegs A3–A6 but Novaluron 0.83EC 10.3 oz are arranged as a uniordinal transverse band on A10. The mature E2Y45 DPX – E2Y45 0.088 lb a.i./acre larva becomes pinkish before pupation. The 12-mm-long pupa is + 0.5% MSO obtect and reddish brown. The adult moth is small and pinkish Thiamethoxam Actara 25WG 4.5 oz gray. Multiple black transverse bands can also be seen on both Zeta-Cypermethrin Fury 1.5 EC 4 oz fore- and hindwings. The wings are held away from the body when at rest. The wingspan varies between 18 and 23 mm with the forewings being slightly narrower than the hindwings. Two to 60% of the fruits were infested with larvae or pupae of the transparent discal spots are present towards the center of each microlepidoptera (Table 2). The microlepidoptera collected were forewing which are usually subdivided into seven cells (Arnett, B. myrsusalis (Walker) (Lepidoptera: Thyrididae), D. sapodilla 1985). The abdomen is stout, silvery gray with a pink tinge. Heppner (Lepdioptera: Tortricidae), and Zamagiria sp. (Lepi- BIOLOGY. In the US (South Florida) adults have been observed in doptera: Pyralidae). late spring and summer (May–July) but may be present throughout the year as long as flowers and fruit are present. Eggs are ovipos- Banisia myrsusalis (Walker) (Lepidoptera: Thyrididae) ited singly on the base of petals of floral buds. Upon hatching, Banisia myrsusalis, commonly known as the sapodilla borer, the larva wanders and starts boring into the bud. Buds are often bores and feeds on the ovary of flower buds and in the pulp and glued together by latex as the larva bores from one flower bud of young sapodilla fruits. In and , it is consid- to the next, consuming the ovaries. If both flower buds and fruits ered economically important (Carneiro et al., 2002; Jhala et al., are present, the larva will attack the flower buds first and then 1986; Patel et al., 1993). bores into the fruit. Large quantities of frass are produced as the DISTRIBUTION. Banisia myrsusalis is one of three Banisia larva feeds. The larva will pupate outside of the fruit, spinning species recorded in Florida (Heppner, 2002). It has also been silk threads to anchor the cocoon between leaves or on the fruit recorded in (Instituto Nacional de Biodiversidad, epidermis. Adults emerge within 14 d of pupation. 1997), Brazil (Carneiro et al., 2002), (Bendicho-Lopez, 1998), (Foon Fong, 2002; Ibrahim, 1992), Australia Dichrorampha sapodilla Heppner (Lepdioptera: Tortricidae) (CSIRO, 2004), Hong Kong (Hong Kong Lepidopterists Society, The adult moth of the sapodilla pod borer, D. sapodilla, was 2002), and India (Jhala et al., 1986). first described by Heppner (1981) from sapodilla flowers. The HOST RANGE. Banisia myrsusalis feeds primarily on flower buds larva was observed during this study feeding on the anthers and and young sapodilla fruits in the US and Brazil (Balerdi and Crane, ovary of the floral buds. 2000; Carneiro et. al., 2002). In Cuba it feeds on DISTRIBUTION. The species D. sapodilla has only been described oliviforme, also a member of the family (Bendicho- in the US (Heppner, 1981). The Dichrorampha consists Lopez, 1998). In India and Malaysia, B. myrsusalis is described of about 115 species (Ulenburg, 2002) of which 14 have been primarily as a feeder of young sapodilla leaves (Foon Fong, recorded in the US and Canada (Arnett, 1985). The distribution 2002; Ibrahim, 1992; Jhala et al., 1986; Patel et al., 1993). of the genus is Holartic (Ulenburg, 2002). DESCRIPTION. Eggs are conical and pink, changing to cream HOST RANGE. In the US, D. sapodilla has only been reported with conspicuous white ridges after eclosion. The ridges (n = feeding on the flowers of Manilkara zapota (Sapotaceae). Another 11) radiate from the base to the top. The ridges possess trans- related species, D. manilkara, feeds on wild dilly (Manilkara bu- verse white lines between them. The micropilar area shows a hamensis) in the US (Heppner, 1981). In the Netherlands, larvae of deep round depression. The mature larva is about 15 mm long, the genera Dichrorampa feed on a restricted number of host plant robust, and cylindrical. The integument is smooth with only species, all of which belong to the family Asteraceae (Ulenberg, primary setae, and white with conspicuous pigmented pinacula 2002). Dichrorampa simpliciana, a nondescript member of this

Table 2. Infestation of microlepidoptera on sapodilla flowers and fruits between May and June 2002. Collection Flowers (no.) Fruits (no.) Larvae (no.) Pupae (no.) Infestation (%) date per sample per sample Flowers Fruit Flowers Fruit Flowers Fruit 21 May 75 6 34 0 1 0 46 0 25 May 15 8 8 0 0 0 53 0 28 May 20 0 5 --- 0 --- 25 --- 31 May 25 2 6 0 0 0 24 0 3 June 10 10 3 6 0 0 30 60 6 June 20 0 2 --- 1 --- 10 --- 10 June 20 5 4 2 0 0 20 40 18 June 15 0 4 --- 0 --- 26 --- 20 June 30 0 9 --- 1 --- 33 --- 21 June 35 0 12 --- 1 --- 37 ---

Proc. Fla. State Hort. Soc. 121: 2008. 11 genus, is fairly common in the British Isles, where it inhabits where Eriobotyra japonica (Rosaceae) was recorded as another meadows, pastures, and hedgerows (Kimber, 2002). host for Z. liadion (Espina, 1968; Iruegas, 2002; Umbelina de DESCRIPTION. The eggs are oval, cream in color. The mature Sousa, 2003). larva is about 5 mm long. The body is also somewhat flattened DESCRIPTION. No eggs have yet been observed. Early instars with a flattened, sclerotized head. The color of the integument of the larvae are green with intersegmental yellow bands. As the is white possessing only primary setae. Crochets are present on larvae mature, they become pinkish brown, with yellow bands the ventral prolegs on abdominal segments A3–A6 and A10. becoming pink-red. The last instar larva is 15 mm. The head of the The crochets are uniordinal and are arranged in a circle on the larva has characteristic dark spots located on the dorsal and lateral ventral prolegs (Myers, unpublished data). The pupa is obtect, surfaces of the frontal area. The integument is smooth possessing light brown, and about 5 mm long. The adult moth is small and only primary setae (Myers, unpublished data). The larva shares gray with a bronze luster. Dark bars are present on the forewing some common characteristics to the Zamagiria spp. described extending from the anal margin to midwing, angled toward the by Iruegas et al. (2002). The larva spins a silken cocoon where apex (Heppner, 1981). The costal margin of the forewing has 6–7 it pupates. The cocoon is regularly surrounded by frass along the major dark fuscous strigulae continued diagonally toward the tip edges. It can be found between two leaves or close to the eaten of the wing. The wingspan is 10–13 mm (Heppner, 1981). When buds. Adults emerge within 14–21 d. The adult moth is small at rest, wings are held adjacent to the body. and gray. Its appearance is similar to Z. dixolephella, described BIOLOGY. Usually only one larva is observed per flower. Lar- by Iruegas et al. (2000). The forewings are dark and smoky-gray vae complete their life cycle in the flower where pupation and with raised scales, colored brown and dark gray. The hindwings emergence occur. Adults emerge within 14 d of pupation. In the are gray and transparent, with a wingspan of about 18 mm. The British Isles, adults of Dichrorampha species are active from June wings are held against the body when at rest. to August in late afternoon and early evening (Kimber, 2002). BIOLOGY. In Mexico, oviposition of Z. dixolephella is reported The braconid Bracon sp. (Hymenoptera: Braconidae), an external throughout the year on the buds of M. zapota (Iruegas et al., 2002), parasitoid, was reared from late larval instars of B. myrsusalis. with highest population peaks during the peak of flowering. In In 2002 the level of parasitism was as high as 30% during late Z. liadion pupates in the soil or between two leaves spring (Myers, unpublished data). (Espina, 1968). The same species causes great damage to young sapodilla trees, reducing tree growth (Espina, 1968). In the US, Zamagiria sp. (Lepidoptera: Pyralidae) the appearance of Zamagiria sp. coincides with the leaf flushing Larvae of the genus Zamagiria are considered economic pests period in June (Myers, unpublished data) and pupation has been of sapodilla. In Brazil Z. liadion causes 60% to 70% damage to observed between two leaves. sapodilla flower buds. Damage can be so severe that productivity of sapodilla trees can be adversely affected. In Florida, Zamagiria Economic importance of the microlepidoptera complex sp. was found feeding on young leaves as well as on buds. Extensive damage to buds, fruits, or young leaves can be DISTRIBUTION. Two Zamagiria species have been reported from caused by either of the species of the microlepidoptera complex. Florida, Zamagiria austrelella Hulst and Z. laidion Zeller (Hep- Because of the similarity of the feeding behavior of these spe- pner, 2002). The best-known species of this genus is Z. laidion cies, the effect of the injury caused by each species is difficult to (Ireugas et al., 2002). This species has also been recorded in determine. Our preliminary observations have shown that flower , , Venezuela, , and Brazil (Carneiro et buds infested with B. myrsusalis and D. sapodilla can be as high as al., 2002; Espina 1968; Iruegas, 2002; Umbelina de Sousa, 2003). 45%. Damage to buds, flower drop, and damage to 70% of fruits Another species, Z. dixolephella, that also feeds on sapodilla has have been observed for B. myrsusalis (Peña, unpublished data). been reported in Mexico (Iruegas et al., 2002). Cuba has the spe- cies Z. fraterna that feeds on Bumelia microcarpa (Sapotaceae) Pesticide efficacy (Iruegas et al., 2002). Only Thiomethoxam provided a significant reduction on the HOST RANGE. Zamagiria species have been reported feeding on number of flowers damaged per cluster 2 weeks after spray ap- primarily in the family Sapotaceae, such as M. zapota, M plication (Table 3). There were no significant differences among emarginata, and B. microcarpa. There are exceptions, however, treatments and the untreated control for the mean number of

Table 3. Mean number of damaged sapodilla flowers per cluster before and after spray. Before After treatment Treatment treatment 1 Week 2 Weeks 3 Weeks 4 Weeks Fenpropathrin (Danitol 2.4EC) 2.62 1.00 1.12 abz 0.88 0.88 Alverde (BAS 320) 2.25 2.12 1.12 ab 0.38 1.12 Dinotefuran (Venom 70SG) 3.12 2.25 0.75 ab 1.25 0.50 Novaluron 0.83EC 2.12 1.62 1.00 ab 0.12 0.75 E2Y45 (DPX- E2Y45-215) 1.25 1.00 0.75 ab 0.12 0.75 Thiamethoxam (Actara 25WG) 2.12 1.25 0.12 b 0.38 0.25 Zeta-Cypermethrin (Fury 1.5EC) 2.00 0.50 0.88 ab 1.25 1.00 Control 1 3.12 1.38 1.37 ab 0.88 1.25 Control 2 2.75 2.88 2.25 a 1.00 2.12 P < 0.0594 0.1658 0.0204 0.3918 0.6050 zColumns with different letters indicate a statistical significance (α = 0.05). Means were separated (LSD) using Student–New- man–Keuls test.

12 Proc. Fla. State Hort. Soc. 121: 2008. larvae per cluster and/or for the proportion of flowers damaged Heppner, J.B. 1981. Two new Dichrorampha (Lepidoptera: Tortricidae) per cluster. from Florida. Florida Entomologist 64:271–276. Hong Kong Lepidopterist Society. 2002. Thyrididae recorded from Hong Literature Cited Kong. Banisia myrsusalis (Walker 1859). July 2002. . Ibrahim, A.G. 1992. The bionomics of lepidoptera pests of Achras sapota Arnett, R.H. 1985. American insects: A handbook of the insects of (Manilkara zapota) Acta Hort. 296:177–179. America north of Mexico. Iruegas, R., B. Gomez, L. Cruz-Lopez, E.A. Malo, and J.C. Rojas. 2002. Balerdi, C., J. Crane, and I. Maguire. 2005. Sapodilla growing in the A new record of a moth attacking sapodilla with descriptions of female Florida home. EDIS Publ. University of Florida Coop. Ext. Serv. Sept. genitalia and the last instar larva. Florida Entomologist 85:394–397. 2007. . Jhala, R.C., A.H. Shah, C.B. Patel, and S.H. Patel. 1986. Population Balerdi, C. and J. Crane. 2000. The sapodilla (Mailkara zapota van dynamics of some insect pests of chiku in South Gujarat. Gujarat Agr. Royen). EDIS Publ. University of Florida Coop. Ext. Serv. May 2002. Univ. Res. J. 11:69–71. . Kimber, I. 2002. UK moths: Dichrorampha simpliciana. 26 June 2002. Carneiro, J.S., D.N. Ferreira, E.L. Araujo, and P.H. Soares da Silva. . 2002. Identificacao e avaliacao de danos cuasados por insectos e Patel, B.S., R.C. Jhala, H.V. Pandya, and C.B. Patel. 1993. Biology of acaros fitofagos as fruteiras exoticas no Meio-Norte do Brasil. Sept. leaf roller (Banisia myrsusalis elearalis) Lepidoptera: Thyrididae, a 2007.

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