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12 Passion Fruit

Elen L. Aguiar-Menezes,1 Euripedes B. Menezes,2 Paulo Cesar R. Cassino2 and Marco A. Soares2 1Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa de Agrobiologia, BR 465, Km 7, Caixa Postal 74505, Seropedica, RJ 23890-000 Brazil; 2Universidade Federal Rural do Rio de Janeiro, Centro Integrado de Manejo de Pragas ‘Cincinnato Rory Gonçalves’, BR 465, Km 7, Seropedica, RJ 23890-000 Brazil

Introduction important Passifloraceae, such as Passiflora ligularis Juss. (granadilla) and P. quadrangularis Passion fruits belong to Passiflora L. (family L. (badea, parcha granadina, tumbo) are culti- Passifloraceae) which has a wide genetic base. vated in Central America and in the Andean While some species are undomesticated, oth- regions of South America (Kluge, 1998). ers are cultivated as ornamental plants, for Commercial production of passion fruits nourishment and for medical purposes. The is currently increasing due to industrialization majority of Passiflora species are indigenous of the processed passion fruit products to the tropical and subtropical regions of (Akamine et al., 1954; Pires and São José, 1994). South America; Brazil is the centre of diver- Although the passion fruit crop has great eco- sity of the Passifloraceae (Cunha, 1996; Manica, nomic potential, its establishment and expan- 1997). Of the 400 known species of Passiflora, sion have been hindered by various problems. about 50 or 60 bear edible fruits. The majority For example, a wide host range of diseases, of these species are unknown outside their insects and mites attack passion fruit. Some centre of origin (Martin and Nakasone, 1994). pest species cause significant crop losses, A few species are economically important reaching the status of key pests or secondary e.g. Passiflora edulis botanical form flavicarpa, pests. Another limiting factor is the low sexual the yellow passion fruit, whose juice and self-compatibility. Increased fruit set depends pulp are used extensively as ingredients of on effective cross-pollination. Therefore, hand beverages, salads, fruit cocktails and desserts cross-pollination is the second most expensive (Donadio, 1983). Passiflora edulis f. flavicarpa production cost of passion fruit culture. Deneger, P. edulis Sims. (purple passion fruit) Knowledge of effective pollinating agents and P. alata Dryand (sweet passion fruit) are might be useful to secure maximum fruit the main species cultivated in the world. The production at lower cost. major producers of passion fruit are found in South America, mainly Brazil, Colombia, Peru and Ecuador (Ruggiero et al., 1996). Flowering and Fruit Setting Commercial plantations of passion fruit are also found in Australia, Hawaii, USA, The period of flowering of passion fruit India, New Guinea, Kenya, South Africa, Sri varies among species and among regions. For Lanka and Costa Rica (Kluge, 1998). Other example, in Hawaii, USA, the passion fruit

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flowers for 8–9 months a year with two but is unlikely to deposit it on the stigma. distinct periods of flowering and fruit setting. When the flower begins to close, the styles The first period of flowering occurs in late return to an upright position. The process of winter or early spring (April and May), and recurvature requires about 1 h. However, the the fruit matures in midsummer. The second styles of some flowers do not curve down- period of flowering occurs in late summer ward as much as others, and because there is (July and August), and the fruit matures in a greater distance between anther and stigma midwinter (Free, 1993). for a pollinator to bridge, they are less likely According to Akamine et al. (1954), there to be pollinated. This applies particularly is little or no overlapping of the functional to those flowers whose styles always remain periods of the flowers so that not much cross- upright, many of which are infertile as female ing takes place between the purple and yellow flowers (Akamine et al., 1954; Free, 1993). In types. In Hawaii, USA, and Brazil, the flowers Brazil, no fruit set is obtained on flowers of the purple passion fruit open early in of yellow passion fruit pollinated when their the morning, usually around dawn, and close styles are upright. On flowers with styles par- before noon. The flowers of the yellow passion tially curved and totally curved, 13% and 45% fruit open about noon and close about 2100 fruit set is obtained, respectively (Ruggiero or 2200 h (Akamine et al., 1954; Free, 1993; et al., 1976). Studies of Vasconcellos (1991) Teixeira, 1994). showed that the percentage of fruit set for In New South Wales, Australia, passion sweet passion fruit was 0, 44.19 and 73.47% fruit flowers start to open in the night or early on flowers with styles upright, partially morning and start to close at about midday curved and totally curved, respectively. the following day, but the stigmas are fully Under natural conditions, the stigma remains receptive on the morning of the first day only. receptive only on the day of flower opening, Anthers of the most flowers do not dehisce and the pollen loses its viability after 24 h until the afternoon (Cox, 1957). (Akamine and Girolami, 1959; Ruggiero et al., In Jaboticabal and Botucatu, SP (Brazil), 1976; Vasconcellos, 1991). the sweet passion fruit flowers for 12 months a The flowers of passion fruit are fragrant year with two flowering peaks, one in January when open. Nectar is secreted in a groove and February and the other in September at the base of the gynophore, and the pollen and October. Its flowers open at about is heavy and sticky. These features, in conjunc- 0400 to 0500 h and close at 1800 to 2000 h tion with the position of the anthers when the (Vasconcellos, 1991; Ruggiero et al., 1996). pollen is exposed and the functional position of the stigmas, indicate that flowers of passion fruit are adapted to pollination by insects rather than by wind. Wind is not important Characteristics of Passion Fruit Flowers in cross-pollination (Akamine et al., 1954; and Their Pollination Akamine and Girolami, 1959; Nishida, 1963; Semir and Brown, 1975; Free, 1993), and this Recent interest in commercial production of was confirmed in studies of caged plants passion fruit has prompted several studies that prevented access to insects; no fruit set on the pollination ecology. When the flowers occurred although plants flowered profusely first open, the stamens hang down, and the (Akamine and Girolami, 1957). anthers dehisce on the undersides, exposing Corbet and Willmer (1980) reported the pollen, the style remains erect, and there nectar sugar concentration of P. edulis f. flavi- is no stickiness on the stigmatic surfaces. carpa to be about 45–50%, which varies little Eventually, the erect styles curve downwards throughout the day. They calculated that the and outwards, and when the process is com- mean volume of the nectar chambers of yellow pleted, they are more likely to be touched passion fruit is 180 µl and that nectar secretion by insects collecting nectar and pollen. How- continues throughout the afternoon. The ever, for the first hour of flowering, a visiting hypothesis in this study is that in order to insect is likely to receive pollen on its body support large bee pollinators, nectar sugar

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concentrations will be low, and nectar pro- In the West Indies, the successful duction rates will be high. pollinators of passion flowers included three In Hawaii, the principal insects visiting species of hummingbird, and in higher passion fruit flowers include honeybee, numbers, Xylocopa mordax Smith (Corbet Apis mellifera L. (Apidae) and carpenter bee, and Willmer, 1980). While collecting nectar, X. Xylocopa varipuncta Patton (Anthophoridae) mordax moves around the flower while facing (Akamine et al., 1954). It is doubtful whether inward, often making at least one complete the honeybee is effective for pollinating the circuit. Only the tip of the galeae can be flowers because of its small size. However, inserted past the operculum at the mouth according to Hammer (1987), the foraging of the nectary and into the nectar groove. habits of honeybees, not their size, may cause Because of the depth of the nectar groove, at less than expected fruit set. The carpenter bee, least 13 µl of nectar remained inaccessible to on the other hand, is large enough so that, in the bees. The collected nectar load has about moving around the flower to obtain nectar, its 50–70 µl volume, and 45–49% sugar concen- body brushes along the anthers and stigmas, tration. Xylocopa mordax spends about 8.5 s transferring pollen from one organ to the per flower visit. On sunny days each flower other (Plate 88). received a mean of four visits in the morning Approximately, 700 species of bees and two in the afternoon; overcast conditions belong to Xylocopa Latreille (Anthophoridae). reduced the visits. Besides nectar, X. mordax They are found throughout the tropical regions collected pollen on the dorsum when in con- of the world (Hurd and Moure, 1963; Hurd, tact with the fully recurved stigmas in differ- 1978) with two generations and activity peaks ent passion fruit species (Free, 1993). Accord- during the periods of December to March and ing to Corbet and Willmer (1980), most yellow July to September (Camillo, 1978a; Camillo passion flower pollination by X. mordax occurs and Garófalo, 1982), coinciding with the flow- between 1330 and 1500 h (Fig. 12.1) when the ering peaks of the passion fruit. Pope (1935) stigmas have curved downward. The daily stated that carpenter bee, X. varipuncta, certain percentage of flowers pollinated ranged from moths and hummingbirds were large enough 25% on overcast days to 94% on bright sunny to transfer pollen from the stamens to the days. Flowers on lower branches were less stigmas of the passion flowers. Nishida (1958, likely to receive a visit by X. mordax and are 1963) reported insect species within Diptera, less likely to set fruit than flowers on higher Hymenoptera, Coleoptera, Thysanoptera and branches. Orthoptera visiting flowers of passion fruit In Brazil, Ruggiero et al. (1975, 1976) in Hawaii, with X. varipuncta and hover fly, observed that three species of Xylocopa and Eristalis arvorum (Syrphidae), being the most Africanized honeybees were the most abun- abundant species. Nishida (1958, 1963) stated dant pollinators of passion fruit, but the pol- that thrips and midges were too small to trans- linating efficiency of the honeybee was low fer the relatively large pollen grains of flowers compared with Xylocopa spp. (3% and 75% of passion fruit. set, respectively). Xylocopa bees were more The insects most commonly visiting efficient pollinating flowers whose styles were passion flowers in El Salvador are Bombus totally and partially curved and less efficient spp., Trigona spp., and Xylocopa spp. (Free, on rainy days. Camillo (1978b, 1980) also found 1993). In São Paulo (Brazil), the most common that Xylocopa suspecta Moure & Camargo is a species visiting passion fruit flowers are more effective pollinator of yellow passion Xylocopa spp., Epicharis spp. and Apis mellifera flowers than X. frontalis (Olivier) in Brazil. scutellata (Nishida, 1963; Ruggiero et al., 1976). The author cited other insects, i.e. Epicharis Akamine and Girolami (1959) noticed that rustica (Friese) (Anthophoridae), Bombus hover fly E. arvorum and long-horned grass- morio, B. atratus, Apis mellifera, Scaptotrigona hopper Conocephalus saltator (Tettigoniidae) postica, Geotrigona sp. (Apidae), and Oxaea feed on pollen of passion flowers, but consid- flavescens Klug (Oxaeidae) visiting flowers ered that their value as potential pollinators of yellow passion fruit. However, S. postica outweighed their potential pest status. and A. mellifera usually collect pollen while

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Fig. 12.1. Pollination of Passiflora edulis flavicarpa, yellow passion fruit. Changes throughout a day in the number of bee visits, number of flowers with at least one stigma curved downward to another level, and the number of pollinated flowers (those with pollen on at least one stigma) (after Corbet and Willmer, 1980).

E. rustica, B. morio, and O. flavescens collect Three carpenter bees, Xylocopa mordax nectar. Smith, X. scutellata Moure, and X. (Megaxy- Sazima and Sazima (1989) also reported locopa) fimbriata Fabricius, were the most that X. suspecta and X. frontalis were effective important pollinators of passion fruit in east pollinators of passion fruit in Ribeirão Preto, and southeast of Lake Maracaibo (Venezuela). SP (Brazil), but Trigona spinipes (Fabricius) Xylocopa nests were observed in wooden (Apidae) collected nectar and pollen without trellis supporting passion fruit plants. Most pollinating the flowers. When T. spinipes was flower visits occurred between 1500 and numerous, their visits depleted the flowers 1800 h (Dominguez-Gil and McPheron, 1992). of nectar, thereby diminishing foraging by Ways of facilitating pollination by Xylocopa. Moreover, Trigona attacked and Xylocopa have been advocated. Nishida (1958) repelled Xylocopa when the latter attempted to advised that either the area of passion fruit visit passion fruit flowers, resulting in 6–25% should not exceed the pollinating capacity fruit set reduction. The deleterious effect of of the insects present, or the number of Trigona colonies is likely to be more serious in pollinators on the crop should be increased. small plantations. Different ways to increase the population Hoffmann and Pereira (1996) found the of pollinators have been suggested (Nishida, following species of bees visiting flowers 1954; Akamine and Girolami, 1959; Cobert of yellow passion fruit in Campos dos and Willmer, 1980). The carpenter bee builds Goytacazes, RJ (Brazil): A. mellifera, Xylocopa its nest in wood or plant stems, and thus ordinaria, X. frontalis, Eulaema nigrita, and its presence as a pollinating agent can be E. cingulata (Apidae). Most flower pollination encouraged by placing wooden posts by Xylocopa bees occurred between 1400 and throughout the passion fruit plantation. The 1700 h. Species of Eulaema were observed only post may be redwood, kukui, or some other during the morning. suitable soft wood. Abundance of nesting In Malaysia, Mardan et al. (1991) observed sites might reduce time spent searching for that carpenter bee, Platynopoda latipes, was nests and diminish competition between the most important pollinator of passion fruit. adult females (Akamine et al., 1954; Free, They suggested that honeybees (Apis cerana 1993). Studies of Camillo and Garófalo (1982) and A. dorsata) were detrimental to fruit set by showed that eucalyptus was the wood removing pollen before effective pollination preferred by Xylocopa bees given a choice by P. latipes could occur. between nine types of wood. Hoffmann (1997)

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recommended the use of posts about 20 cm honeybees are plentiful, it has been observed diameter have been 60–70 cm length in which that they visit the flowers as soon as flowers two holes of 1.5 cm diameter have been made. have opened. The bees remove the pollen The first hole is longitudinal, 20 cm deep, and from the anthers and carry it back to the hive. the second one is perpendicular to the first at By the time the styles have moved into 15 cm high, allowing them to meet. The first position where their stigmas can be pollinated hole is closed by a woody piece or a cork, and by carpenter bees, the pollen may be entirely the second is used as the nest entrance. gone. Unless the carpenter bees have some Camillo (1996) increased the pollination pollen remaining on their bodies from early of passion fruit by introducing into planta- visits to the flowers, pollination is entirely tions Xylocopa spp. in Holambra, São Paulo precluded and fruit setting fails to occur. (Brazil). Before the placement of Xylocopa In Hawaii, Nishida (1958) found that in nests, the natural pollination resulted in 3.2% two localities, flowers bagged and pollinated fruit set. With the introduction of 49 nests by hand had about the same percentage set of X. frontalis and X. grisescens into 1.5 ha as unbagged flowers. However, in two other of passion fruit, the percentage of fruit set localities, bagged and hand pollinated flowers increased to 25%. had a greater fruit set, indicating that the local Carpenter bee populations can be insect pollinators were too few in these sites increased by providing seasonal spreads of (Fig. 12.2). His results also showed that the nectar and pollen sources, thereby reducing fruit set from cross-pollinating, bagged flow- competition with other nectar sources while ers varied from 50 to 100%, depending on the passion fruit is flowering (Akamine et al., locality. So the maximum fruit set in some 1954). In Brazil, Hibiscus spp., Cassia spp., localities was limited by factors other than Ipomoea purpurea, and Crotalaria juncea have pollinators. The percentage of fruit set from flowers that are very attractive to carpenter hand pollination and the difference in set bees (Ruggiero et al., 1996). between hand and natural pollination also Evaluation of the need to either increase varied within a season. Akamine and numbers of carpenter bees or perform hand Girolami (1959) reported that natural fruit set pollination is by counting the number of was less than that achieved by hand pollina- flowers dropped, because this may be caused tion. Corbet and Willmer (1980) confirmed by lack of fertilization, indicating low popula- that bagged flowers only set fruit following tion density of insect pollinators. To evaluate cross-pollination (mean of 77% fruit set). Fur- whether the pollinators occur in the crop at a thermore, manually cross-pollinating flowers suitable level, Ruggiero et al. (1996) recom- exposed to insect pollinators increased fruit mended that three opening flowers per plant set from 27 to 73%, indicating that natural should be labelled on a sunny day. For 2–3 ha, pollination was inadequate. this operation must be repeated with > 34 Nishida (1963) found that the abundance plants, labelling 100 flowers in total. If the area of honeybees on the crop and the proportion is greater, the quantity of labelled flowers of pollen gathered varied greatly from one should be increased proportionally. Four days month to the next and was probably associ- later, the fruit set on the labelled flowers is ated with the presence of competing sources counted. Of the 100 labelled flowers, Ruggiero of forage. He observed that sometimes honey- et al. (1996) observed that 40–50% developed bees were so abundant that nearly all pollen into fruit, meaning that the population density was removed soon after the flowers opened. of carpenter bees was adequate. However, A few honeybees were present on the crop values < 30% indicated there was a lack of when it was not flowering and in the morn- pollinators and, in this case, flowers must be ings before the flowers opened; these bees hand pollinated. were collecting from the extrafloral nectaries According to Akamine et al. (1954), on the leaf petioles. He found that when the Akamine and Girolami (1957, 1959), and density of honeybees present increased to a Nishida (1958), honeybees may actually cause certain level there was a tendency for the fruit unfruitfulness of passion fruit. In areas where set to decrease. However, there was a positive

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correlation between the increase in fruit set (1963) suggested that X. varipuncta is a and the increase in the population of X. more efficient pollinator than the honeybee, varipuncta that was present (Fig. 12.3). Nishida because it is larger, works faster and carries

Fig. 12.2. An experiment to determine the efficiency of natural pollination of Passiflora edulis, passion fruit, in three sites in each of four localities: A, flowers bagged; B, flowers bagged and hand pollinated; C, flowers not bagged nor hand pollinated (after Nishida, 1958).

Fig. 12.3. Relationship between the number of Xylocopa varipuncta, carpenter bees, in Passiflora edulis, passion fruit, fields and percentage of flowers pollinated (after Nishida, 1963).

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larger loads. Ruggiero et al. (1976) confirmed Table 12.1. Reciprocal crosses between this by experiments in which caged plants varieties of passion fruit, and the percentage of resulted in better fruit set when confined with fruit set following cross-pollination. (From Akamine Xylocopa spp. than with honeybees (75% and and Girolami, 1959.) 45% fruit set, respectively). Reciprocal No. flowers Percentage of On the other hand, Free (1993) suggested crosses pollinated fruit set that honeybees as pollinators are important because they forage in the lowlands and in the C 39 and C 37 258 92 humid uplands, and may be easily manipu- C 39 and C 77 250 97 C 39 and C 80 167 97 lated. Cox (1957) reported that honeybees are C 37 and C 77 83 2 abundant and effective pollinators of passion C 37 and C 80 106 2 fruit in Australia. In Florida, USA, where hon- C 77 and C 80 80 4 eybees are the sole pollinators of P. edulis,up to 25% of its flowers produce fruit (Hardin, 1986). pollinators. However, other hymenopterans As pointed out by Gilmartin (1958), it has (e.g. Apis, Bombus, Epicharis, Oxaea) and orth- not been determined that cross-pollination opterans, dipterans, etc., visit the flowers of between flowers of different clones or variet- passion fruit, and may pollinate, even though ies is necessary for maximum fruit setting. It is they may be less effective than Xylocopa. advisable to plant several selected varieties in Thus, as stated by Price (1997) studies of an orchard to enhance the possibility of cross- pollination ecology, co-evolution between pollination and to minimize crop losses which plant and pollinator, energetic relationships, might occur from planting with a variety demographics of plant and pollinator, repro- strain that proved to be highly self-incompati- ductive strategies, population dynamics and ble. Akamine and Girolami (1959) found that community ecology, are still warranted and any cross that involved variety ‘C 39’ (Table needed for Passifloraceae. 12.1) was compatible, but crosses between other varieties were nearly completely incom- patible. They suggested that plants of compat- Pests ible clones, which flower at the same time, should be distributed in the field to ensure the Although passion fruit is attacked by several maximum possibility of cross-pollination. pest species of insects and mites that feed upon all parts of the plant, a limited number of species are clearly of major economic Conclusions importance. Few have key pest status, while some species are secondary pests because Plants of the Passifloraceae depend on cross- they are sporadic or occur at low population pollination to set fruit because their flowers levels, and therefore do not require control present characteristics that make it difficult strategies. Insect and mite pests that are for self-pollination, such as presence of stig- frequently associated with passion fruit are mas above the level of the anthers and stigma described below, including their description, receptivity and low self-fertility. Thus, the life history, behaviour, hosts, damage and passion fruit depends largely on mutualistic control (Santo, 1931; Lordello, 1952b; Correa relationships, with insects as pollinators. In et al., 1977; ICA, 1987; Dominguez-Gil et al., fact, the flowers of passion fruit are large, 1989; Figueiro, 1995; Lima and Veiga, 1995). attractive, colourful, fragrant, and produce plentiful nectar and pollen that facilitate insect cross-pollination. Most of the studies Lepidopterous defoliators dealing with pollination of the Passifloraceae support the theory that carpenter bees, Three heliconiine species, Dione juno juno mainly Xylocopa spp., are the most effective Cramer, Agraulis vanillae vanillae Linnaeus,

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and Eueides isabella huebneri Ménétries full-grown larva is about 35–40 mm in length, (Nymphalidae), are the most common the dorsum has orange, blue and white stripes lepidopterans feeding upon foliage of and six longitudinal lines of branched black passion fruit (Dominguez-Gil and McPheron, spines (Plate 90). The larvae has five instars, 1992). Dione juno juno is the key pest of and lasts about 17 days (Lordello, 1952a). passion fruit in Brazil and causes severe The chrysalis is suspended by the cremaster, damage to the plants (De Bortoli and Busoli, which is usually attached to a branch of the 1987; Gravena, 1987). D. juno is distributed host plant. The chrysalis is about 25 mm in in the southern USA, the Antilles, Guyana, length, sharply angled, and creamy white and Surinam, French Guiana, Trinidad, and from lasts about 7 days. Colombia to Argentina (Toledo, 1991), while Two-thirds of the forewing of Eueides A. vanillae occurs in South America and isabella huebneri is dark brown, almost black, over a large part of the southeastern USA with irregular yellow spots, and one-third is (Carter, 1992). Eueides isabella is found in orange with black stripes. The hindwings are Venezuela and south of Brazil (Silva et al., orange with black borders and a central stripe. 1968; Brown Júnior and Mielke, 1972; The wingspan is 70–80 mm. Females oviposit Dominguez-Gil and McPheron, 1992; Boiça single eggs on leaves or stems. The eggs Júnior et al., 1993). are whitish yellow when recently laid, and are darker close to hatching, which occurs DESCRIPTION AND LIFE HISTORY Adults of D. 4–7 days after oviposition. The newly hatched juno have orange wings with black borders larva is 1–3 mm long, white with black head and venation. The wingspan is about 60 mm. and body hairs. The full-grown larva is 30 mm Eggs are laid in groups of 40–70 on the leaf long. The dorsal surface of its body is black underside, near the border. The 0.9 × 0.6 mm with transversal narrow white stripes, and egg is light yellow when first laid, and darkens the dorsal surface of the eighth and ninth just before hatching. Eggs hatch in 6–7 days. abdominal segments is orange. The larvae The larvae pass through four or five instars, require five instars. The chrysalis has spines requiring 19–27 days to reach full growth. on the thorax and abdomen, differing from the When fully grown, the larva is about other heliconiines. 29–35 mm in length, 3–5 mm in width, dark brown, with small yellow spots, and covered HOST PLANTS Caterpillars of D. juno feed with black setae arranged in rows. The larvae on all Passiflora species, except P. foetida are gregarious and, when disturbed, raise (Echeverri et al., 1991; Carter, 1992). According their head and thorax, and stand on their to Boiça Júnior et al. (1993), P. alata, P. setacea pseudolegs. The chrysalis is suspended by and the hybrid P. alata × P. macrocarpa are the cremaster, is obtect, cream in colour, more resistant to attack by D. juno than and about 16–25 mm in length. The pupal P. edulis, P. cincinnata, P. caerulea and the stage requires 7–9 days (D´Almeida, 1944; hybrid P. edulis × P. alata. Lordello, 1954; Silva, 1979; Chacón and Rojas, 1984; De Bortoli and Busoli, 1987; Toledo, INJURY The three species of heliconiine 1991; Dominguez-Gil and McPheron, 1992; defoliators reduce leaf area, thereby indirectly Dominguez-Gil, 1998). reducing yield. Dione juno usually causes The A. vanillae butterfly has red-orange damage that is more serious because of its wings, with black markings and venation, gregarious behaviour (Fancelli and Mesquita, and silver spots on the underside (Plate 89). 1998). During the first instar, the caterpillars Wingspan varies from 60 to 75 mm (Carter, scrape the leaf epidermis of young leaves, 1992). The female lays eggs singly on leaves or leaving small holes in the leaves, while older stems. The eggs are light yellow when recently larvae devour both young and older leaves oviposited, spindle shaped, and about 1 mm (Lordello, 1954; Chacón and Rojas, 1984). in length. The eggs hatch in 3 days (Lordello, Besides defoliation, the caterpillars may 1952a). The newly hatched larva, approxi- feed on the apical buds, flowers or stems mately 3 mm long, is creamy white. The (De Bortoli and Busoli, 1987).

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NATURAL ENEMIES Several predators and regular intervals until the crop is harvested. In parasitoids have been reported from these passion fruit it is very important to protect heliconiids. However, these natural enemies pollinating insects by timing insecticidal treat- are not considered to be effective. For instance, ments when pollinators are not present in the Silva et al. (1968) reported Alcaeorrynchus field. Choosing an insecticide that is selective grandis (Dallas) and Apateticus mellipes for the pest and less toxic to pollinators, preda- Bergroth (Pentatomidae) as predators of tors and parasitoids is important in these D. juno. In Argentina, A. vanillae was recorded agroecosystems. Bacillus thuringiensis (Bt) to be parasitized by Pteromalus caridei Berliner, which effectively controls a variety Brèthes (Pteromalidae). Silva (1979) reported of caterpillars and has little or no effect on Spilochalcis spp. (Chalcididae) parasitizing natural enemies, is commonly recommended. D. juno. In the state of Pernambuco (Brazil), Menezes et al. (1989) performed a laboratory Lima and Veiga (1995) found Spilochalcis experiment with different strains of Bt to con- spp., Polistes sp. (Vespidae), Paratrechina trol D. juno. Figueiro (1995) demonstrated that longicornis, Crematogaster sp., Pseudomyrmex suspensions of Baculovirus dione at concentra- gracilis (Formicidae), and Forcipomuia sp. tions of 10, 20, 40 and 80 g of larvae per 500 l of (Ceratopogonidae) as natural enemies of water, were highly pathogenic and efficient D. juno. Ruggiero et al. (1996) recorded the at controlling larvae of D. juno under labora- hymenopteran wasps, Polistes spp. and Polybia tory conditions. Studies of Moura et al. (2000) spp. (Vespidae), as predators of passion on selectivity of insecticides to vespid preda- fruit heliconiids in Brazil. In Lake Maracaibo tors of D. juno, showed that the deltamethrin (Venezuela), Dominguez-Gil and McPheron was highly selective to Polybia scutellaris (1992) reared two specimens of Spilochalcis sp. and Polybia fastidiosuscula, and showed inter- from field-collected larvae and chrysalis of mediate selectivity to Protonectarina sylveirae. A. vanillae and E. isabella. Cartap was moderately selective to all Lima and Veiga (1993) verified the occur- three species of predatory wasps. Malathion rence of nuclear polyhedrosis virus (NPV) was selective to P. sylveirae and showed inter- infesting D. juno caterpillars in Pernambuco. mediate selectivity to P. fastidiosuscula. In Lake Maracaibo, larvae of D. juno were also infected by NPV. Once infected, larvae became sluggish, and their cuticles become discoloured and fragile. Chacón and Rojas Coreid bugs (1984) estimated that NPV kills 100% of the D. juno population in Colombia. A NPV Many species of bugs attack passion fruit and epizootic occasionally reduced populations of the majority belongs to the Coreidae (leaf- A. vanillae in plantations located east of Lake footed bugs). In passion fruit producing Maracaibo where NPV was very abundant areas, three main species of coreids are repor- during January and February for 3 consecu- ted: Diactor bilineatus Fabricius, Leptoglossus tive years (Dominguez-Gil et al., 1989). spp. and Holhymenia spp. D. bilineatus is the most common species, and is known as the CONTROL In small areas, cultural control passion fruit bug because it feeds only on during periodic crop inspection includes hand fruit of Passiflora spp. Among the Holhymenia, picking and destruction of eggs and cater- H. clavigera (Herbst.) and H. histrio (Fabricius) pillars (Rossetto et al., 1974). However, these are the most common species attacking methods require considerable time and labour passion fruit. The bugs Leptoglossus, L. and are often impractical for a large-scale cul- gonagra Fabricius and L. australis Fabricius, tivation. In this case, injurious populations of usually cause damage to passion fruit. defoliating caterpillars infesting passion fruit D. bilineatus is considered the most must be controlled with insecticidal sprays. important pest of passion fruit in Brazil Action thresholds have not been defined. by Mariconi (1952) and Fancelli and Growers spray the foliage, often starting Mesquita (1998). However, Dominguez-Gil with appearance of the pest, and continue at and McPheron (1992) consider that Diactor

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bilineatus Fabricius, Leptoglossus spp. and with black legs and antennae. The bugs pass Holhymenia spp. are the second most signifi- through five nymphal instars in about 55 cant phytophagous group of pests in passion days (Chiavegato, 1963, De Bortoli and Busoli, fruit plantations in the Lake Maracaibo region 1987). The adult passion vine bug, L. australis, (Venezuela). is elongate, approx. 20 mm in length, and dull black in colour with orange spots on the DESCRIPTION AND LIFE HISTORY Adults of D. underside of the body. In Hawaii, passion bilineatus are orange on the ventral face of the vine bugs migrate from surrounding scrub head, and the dorsal face is dark metallic green to infest passion fruit plantations. Neglect of with two orange longitudinal lines that vines may allow populations of the bug to continue on the prothoracic tergum and the build up. Feeding usually occurs on flowers or scutellum, both of which are dark metallic green-mature fruit. Nymphs often cluster on green. The hind legs have the tibia expanded fruit when feeding. Damage to mature fruit and leaf-like, dark green in colour with some is not pronounced; however, young fruit orange markings. Males are about 20 mm develops dimple-like surface blemishes at in length, and females, 21.5 mm. When the feeding sites (Murray, 1976). disturbed, they walk or make short flights, mainly in cold periods. A female lays a batch HOST PLANTS Silva et al. (1968) listed several of six to nine eggs on the underside of the species of Passiflora as being hosts of D. leaves. They are about 3 mm long, light yel- bilineatus. Mariconi (1952) verified that P. low, bright, elipsoid and flattened in the base. quadrangularis is seriously damaged by this The incubation period for eggs is 13–16 days. pest. Besides passion fruit, H. clavigera feed The nymphs, which pass through five instars, on guava (Fancelli and Mesquita, 1998). Silva require about 43–46 days to reach the adult et al. (1968) mentioned P. edulis as host of this stage (Mariconi, 1952). The first instar nymph species. L. gonagra feeds on a large number of has an orange head that turns dark blue in host plants, including passion fruit, chayote, the following instars. The thorax is orange, citrus, tobacco, guava, sunflower, cucumber, and a white stripe surrounds the femurs and grape, pomegranate, São Caetano melon tibiae. The hind legs are characterized by the (Cayaponia espelina), bixa (Bixa orellana), expanded leaf-shaped tibia. The abdomen araçazeiro (Psidium araca), and Anisosperma is orange with six pairs of lateral, dark passiflora (Chiavegato, 1963). blue expansions from the third to the eighth abdominal segments (Dominguez-Gil, 1998). NATURAL ENEMIES Silva et al. (1968) reported The adult body of Holhymenia spp. is that D. bilineatus eggs were parasitized by black with orange spots. The legs are reddish Hadronotus barbiellinii Lima (Scelionidae). orange. The head, the prothoracic tergum and Eggs of H. clavigera were reported to be the scutellum are black with white spots parasitized by Hexacladia smithii Ashmead (De Bortoli and Busoli, 1987; Brandão et al., (Encyrtidae) (Silva et al., 1968). 1991; Dominguez-Gil, 1998). The adult L. gonagra (Plate 91) is about INJURY Both immature and adult bugs 15–19 mm in length and dark brown in colour. injure the crop, piercing stems, leaves, fruits The head colour ranges from dark brown to and flowering buds, and sucking plant juices. almost black, with two yellow longitudinal However, the nymphs prefer to feed on flow- lines. The prothoracic tergum is brown with ering buds and young fruits, usually resulting a yellow transverse line. The antennae are in excessive dropping. The adults may also brown with the second, third and distal attack leaves, stems and fruits at any stage of two-thirds of the forth segments light yellow ripening. If larger fruits are fed upon, they wilt in colour. The hind tibiae are expanded and and show a wrinkled surface. Fruits may also leaf-like. The longevity of adults is about 37 develop dimple-like blemishes at the feeding days. Eggs are 1.4 mm in length, dark brown sites on the fruit surface (Murray, 1976). Lepto- with triangular cross-section. The eggs hatch glossus gonagra often causes misshaping or in 8 days. Newly hatched nymphs are reddish dropping of young fruits (Chiavegato, 1963).

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CONTROL In small passion fruit producing HOST PLANTS In Brazil, yellow passion fruit areas, hand picking and destruction of is susceptible to attack by Philonis spp. while eggs, nymphs and adults is recommended Passiflora alata, P. maliformis, P. serrato digitada (Mariconi, 1952). Chiavegato (1963) suggests and P. caerulea are not infested by this pest the removal of the alternative cucurbit host, (Oliveira and Busoli, 1983). Cruz et al. (1993) ‘São Caetano melon’, a preferred host of L. observed that yellow passion fruit is very sus- gonagra, or to avoid the cultivation of chayote ceptible to Philonis obesus attack, but P. alata and Anisosperma passiflora in adjacent areas as and P. giberti show some plant resistance. tactics to reduce pest densities. In southeast Queensland, Australia, regular inspections INJURY Larvae of Philonis spp. feed within are recommended during the summer months the stems, opening longitudinal galleries to detect any build-up of L. australis (Murray, inside stems that prevent plant development. 1976). The attacked stems are easily identified by the presence of excrement and sawdust (Santos and Costa, 1983). As the larva develops, infested stems become weak and frail, and Stem weevil die (Fancelli, 1992a). According to De Bortoli and Busoli (1987), the simultaneous attack of In Brazil, the stem weevil Philonis spp. (Cur- several larvae is characteristic of weevil infes- culionidae) was first reported in Alagoas in tations, which causes hypertrophy in stems 1972. Currently, the infestation has expanded where the pupal cell will be constructed to several states in Brazil (Warumbi and (Rossetto et al., 1978; Oliveira and Busoli, Veiga, 1978; Leão, 1980; Torres Filho and 1983; Racca Filho et al., 1993). Attack by Araújo, 1981; Oliveira and Busoli, 1983; Cruz the stem weevil also causes fruit drop before et al., 1993; Racca Filho et al., 1993; Boaretto maturation (Costa et al., 1979). et al., 1994). It is commonly found on borders of young plantations (Fancelli, 1992a). Severe CONTROL Periodic inspections of the crop outbreaks of this pest have caused the are essential for an early detection of weevil- eradication of 250 ha in Brazil (Rossetto et al., infested stems (Fancelli, 1992a). When infesta- 1978). Racca Filho et al. (1993) reported the tion symptoms are detected on the crop, occurrence of P. passiflorae O´Brien and P. affected stems should be pruned and burned obesus Champion in Rio de Janeiro. The spe- (De Bortoli and Busoli, 1987). According to cies that occurs in São Paulo was identified Leão (1980) and Costa et al. (1979), a contact as P. crucifer (Piza Júnior and Kavati, 1995). insecticide (e.g. decamethrin at 25% (5–10 g a.i. ha−1)) should be applied during early DESCRIPTION AND LIFE HISTORY Adults of P. afternoon hours for stem weevil control, at passiflorae are about 7 mm in length, brown the time of adult emergence. After 4–5 days, with whitish elytra with two brown stripes. systemic insecticides for control of future stem Adults of P. crucifer are 4 mm in length, brown infestations should be used. with black markings. They are nocturnal (Piza Júnior and Kavati, 1995). According to Santos and Costa (1983) and Boaretto et al. (1994), females lay eggs on young or old stems. The Flies eggs hatch in 8–9 days. The larvae are white and legless. The full-grown larva is about Some fly species feed upon the fruits of 8 mm long. The larval stage is 53–64 days, and Passiflora spp., and others attack flowering the pupal period is 14–35 days (Costa et al., buds. In Brazil, Lordello (1954), Santos and 1979). All stages of development of this Costa (1983) and Teixeira (1994) reported the species occur inside the stem. Pupae and following genera of flies damaging passion recently emerged adults are frequently found fruits: Anastrepha Schiner (Tephritidae) and in cocoons spun by the full-grown larva Lonchaea Fallén (Lonchaeidae). A. consobrina (De Bortoli and Busoli, 1987). (Loew), A. curitis Stone, A. dissimilis Stone,

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A. fraterculus (Wiedmann), A. kuhlmanni from puparia buried up to 2–5 cm deep in the Lima, A. lutzi Lima, A. pseudoparallela (Loew), soil, and crawl to the surface. They feed A. striata Schiner, and A. xanthochaeta Hendel on juice of ripening fruits (Plate 92) and are reported as being the most common on honeydew excreted by aphids, mealybugs, species associated with passion fruit in Brazil and soft scale insects. Females deposit their (Santos and Costa, 1983; Teixeira, 1994; eggs mainly in ripening fruit, depositing two Zucchi, 1988, 2000). Anastrepha pallidipennis to six eggs in the cavity beneath the skin. After Guerne was reported on yellow passion fruit 2 or 3 days, the whitish eggs hatch. The cream in Colombia (Chacón and Rojas, 1984). The coloured larvae bore into the fruit pulp and oriental fruit fly, Bactrocera dorsalis (Hendel), contaminate it with bacteria and fungi, melon fly, Bactrocera cucurbitae Coquillett, which cause the fruit to decay. Large fruits and the Mediterranean fruit fly, Ceratitis may contain as many as 100 larvae. Under capitata Wiedmann, are known to attack the favourable conditions, larvae complete devel- passion fruit vines in Hawaii, USA (Back and opment in about 9–13 days. They exit the Pemberton, 1918); however, the relative fruit while it is hanging on the tree or after importance of each species appears to vary it has fallen to the ground. In the tropical with respect to location of the vineyard areas, the pupae complete development in (Akamine et al., 1954). The Queensland fruit 10–14 days. In temperate areas, the pupae fly, Bactrocera tryoni (Froggatt), is the most complete development in 7–11 days during important insect pest of passion fruit in the summer, but in winter may remain Australia (Murray, 1976). dormant for several months. Flies of the Neosilba pendula (Bezzi) and Dasiops sp. genus Anastrepha produce a variable (Lonchaeidae) are the most common species number of generations depending on the attacking flowering buds of passion fruit inhabited region (Orlando and Sampaio, 1973; (Rossetto et al., 1974; Silva, 1982; Fancelli and Morgante, 1991). Mesquita, 1998). Dasiops sp. attacking flower- The adult of Bactrocera tryoni is wasp-like ing buds was reported in Rio de Janeiro, Brazil in appearance, about the size of a house fly, (Silva et al., 1968; Vasconcellos et al., 1995). The with transparent wings bearing a dark band species of Dasiops known to attack flowering on the front margin. Bright yellow patches buds or fruits of Passiflora spp. in the Americas interrupt the general reddish brown body are D. curubae Steykal, D. inedulis Steykal, and colour. The female lays several pale cream, D. passifloris McAlpine (Steyskal, 1980). elongate eggs beneath the skin surface of the Other flies may also feed upon flowering fruit. Creamy coloured maggots may emerge buds, such as Lonchaea cristula McAlpine from the eggs in 2 or 3 days and tunnel within (Lonchaeidae) and Zapriothrica salebrosa the fruit while feeding. During the warmer Wheeler (Drosophilidae) (Chacón and Rojas, weather the larval stage is completed in about 1984). Hernández et al. (1985) observed that L. 2 weeks. The mature larvae then leave the cristula is more common in curuba (Passiflora fruit to burrow into soil to pupariate for an molissima) when this crop is cultivated near additional 2 weeks, after which adults emerge areas where other host fruits grow. The larvae from puparia. Very few eggs laid in immature of these fly species destroy pollen by boring passion fruit produce adult flies. The develop- into anthers, and may cause intensive drop- ment of woody tissue around eggs in the rind ping of infested buds (Chacón and Rojas, of the fruit prevents some eggs from hatching, 1984). or when hatching occurs, causes high mortal- ity of young larvae. Egg hatching in ripe fruit DESCRIPTION AND LIFE HISTORY Anastrepha is mostly unaffected since the fruit has ceased adults are 6.5–8.0 mm in length, predomina- growing and does not form the woody tissue tely yellow in colour, with brown and yellow around the eggs (Murray, 1976). In Queens- markings on the wings. The adult Medfly is a land (Australia), B. tryoni invades passion smaller colourful insect with yellow and black fruit vines from alternative host plants and is markings on the body and black and orange most active from September to April (Swaine markings on the wings. Adult flies emerge et al., 1985).

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The adult Dasiops curubae is blackish blue. secondary pest of several fruits, especially tan- The wings are hyaline and slightly smoky gerine (Rossetto et al., 1974). Dasiops curubae yellowish, while the calypters and wing damages flowers of curuba (P. mollissima) fringes are pale yellowish (Steyskal, 1980). (Steyskal, 1980; Causton, 1993). Dasiops The adult Dasiops inedulis is bright inedulis is reported in Panama to be a serious metallic dark blue with hyaline wings; the pest of purple granadilla, P. edulis (Steyskal, calypters and wing fringes are yellowish to 1980). This species has been implicated in nearly white (Steyskal, 1980). Peñaranda et al. 21–65% loss of flowering buds of passion fruit (1986) reported that the length of the life cycle in the Cauca Valley (Colombia) (Peñaranda of this species takes 22.8 days under labora- et al., 1986). Dasiops passifloris attacks fruits of tory conditions. The period of incubation P. suberosa (syn., P. pallida) (Steykal, 1980). requires 2–3 days; the larval stage, 4–9 days; and the pupal stage, 10–17 days (Peñaranda INJURY Fruit fly adult damage is caused by et al., 1986). oviposition in green fruits, causing disfigurat- Dasiops passifloris was described by ions of the fruit surface. The larvae damage McAlpine (1964), who recorded its distribu- the fruit by feeding on its pulp, contaminating tion in Florida. Adults are metallic blue- it with bacteria and fungi (Plate 93), and black, and females have a long ovipositor causing premature fruit drop (Medina et al., resembling those species in the Otitidae and 1980; Santos and Costa, 1983; Morgante, 1991). Tephritidae. They oviposit one to four eggs According to Akamine et al. (1954), the in the pulp of immature fruit. After hatching, oriental, melon, and Mediterranean fruit flies larvae bore through the immature fruit and puncture the fruit while the rind is still tender. feed on developing seeds. The maturing As the fruit enlarges, a woody area (callus) larvae then begin feeding on the fruit pulp develops around the puncture. If the fruit is immediately beneath the skin. In about small and undeveloped, the damage may be 12 days the larvae mature and drop to the sufficient to cause it to shrivel and fall from the ground, where they pupariate within the soil plant. If the fruit is well developed, it may or possibly beneath some refuse. The pupal continue to maturity. At the time of ripening, stage lasts 14 days (Stegmaier, 1973). the area around the puncture has the appear- The adult Neosilba pendula is about 4 mm ance of a small, woody crater, which disfig- long, bright metallic dark blue, with hyaline ures the outer appearance of the fruit but does wings (Rossetto et al., 1974). not impair pulp quality. Although oviposition scars are present on ripening fruits, they HOST PLANTS The highly polyphagous Ana- generally do not contain living larvae. Larvae strepha spp. infest approximately 270 plant appear to be able to develop better in imma- species in 41 families, and are considered to be ture than in mature fruit. the major fruit pests of tropical and subtropi- Oviposition by B. tryoni in immature cal America. Passiflora has been reported as a green fruit also results in the formation of host of the larvae of two groups of Anastrepha calluses in the skin of the fruit at the puncture (chiclayae and pseudoparallela) (Norrbom and site. Punctured fruits may persist on the plant Kim, 1988; Stefani and Morgante, 1996). to maturity but are not acceptable for fresh Anastrepha chiclayae Greene has been found market sale because of the damage (May, 1953; associated with Passiflora spp. in Mexico Hargreaves, 1979). (Hernández-Ortiz, 1992). Larvae of A. limae According to Murray (1976), passion fruit Stone feed upon fruits of P. quadrangularis increase rapidly in size during the first 10–15 (Stone, 1942; Caraballo, 1981). Lordello (1954) days after fruit set. During this period the skin observed infestations by Anastrepha and of the fruit is turgid and easily punctured by Lonchaea species on Passiflora quadrangularis the ovipositor. Infested immature fruit shows and P. macrocarpa. The Medfly attacks 253 characteristic skin blemishes. The woody kinds of fruits, nuts, and vegetables; many of tissue, which forms around the eggs, develops which are tropical plants. Neosilba pendula is a hard raised area around the puncture mark. known as the key pest of cassava, and is a Egg laying or puncture often cause young

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fruit to shrivel and drop. Puncture marks are papaya, tomato, and other fruits in which difficult to detect on ripe fruit. A few days the flies breed and on which the adults feed. after larval infestation, mature fruit will show Santos and Costa (1983) recommended that wrinkling and breakdown. passion fruit must be planted far away from Anastrepha pseudoparallela lays eggs in coffee plantations and wild host plants that unripe fruits of P. alata, and the larvae develop grow adjacent to the passion fruit crop should by feeding on the seeds. Cyanogenic com- be removed. Fruit flies may be controlled pounds are present in all parts of Passiflora using bait sprays composed of molasses (7%) plants, including seeds of unripe fruits. These or protein hydrolysate (1%), and an insecti- glycosides protect the plant by preventing cide. The bait is sprayed over 1 m2 of the plant feeding by herbivore species. Thus, the use of canopy, using 100–200 ml of bait per plant these resources by A. pseudoparallela for larval (Santos and Costa, 1983). The bait should be breeding is probably associated with its ability applied during the night (Rossetto et al., 1974). to tolerate these chemical defences and sug- Boaretto et al. (1994) reported that bud flies gests a high degree of specialization (Stefani may be controlled by insecticide baits com- and Morgante, 1996). posed of fenthion, molasses and water. The The larvae of flies that attack the flower- bait is applied at the beginning of the flower- ing buds and immature fruits cause prema- ing peak, and usually three applications ture fruit drop (Brandão et al., 1991). Immature spaced at 8–10 days are necessary. The authors fruits infested by D. passifloris become dirty, also suggested burying the attacked buds and whitish green in colour, while infested ripe planting trap crops, such as sweet pepper. fruits become bluish white (Stegmaier, 1973). Dasiops inedulis larvae bore into the anthers, and the ovary, causing flowering bud drop (Peñaranda et al., 1986). Mites

NATURAL ENEMIES Most species of tephritid Several species of mites have been reported fruit flies are attacked by a complex of larval from passion fruit (Sanches, 1996). Brevipalpus parasitoids while egg and pupal parasitoids phoenicis (Geijskes) (Tenuipalpidae), the red are much less common (Bateman, 1972). spider mites Tetranychus mexicanus (McGregor) Doryctobracon Enderlein, Diachasmimorpha and T. desertorum Banks (Tetranychidae) are Viereck, Opius Wesmael, Psyttalia Walker and known to infest passion fruit plants. Warm Utetes Foerster (Braconidae) are the most com- temperature and low precipitation favour mon larval parasitoids of tephritid fruit flies development of these species (Haddad and (Wharton, 1996). Pachycrepoideus vindemiae Millán, 1975; Oliveira, 1987; Brandão et al., (Rondani) and Spalangia endius Walker (Ptero- 1991). On the other hand, Polyphagotarsonemus malidae) are pupal parasitoids of Medfly latus (Banks) (Tarsonemidae) prefers high (Back and Pemberton, 1918). In Colombia, temperatures and > 80% relative humidity Opius sp., Zelus rubidus (Reduviidae), and (Oliveira, 1987; Brandão et al., 1991). spiders of Thomisidae were reported as natural enemies of D. inedulis (Peñaranda DESCRIPTION AND LIFE HISTORY Brevipalpus et al., 1986). phoenicis mites are quite small, e.g. 0.3 mm in According to Silva et al. (1968), larvae of length, and pass through five stages in their N. pendula are parasitized by Alysia lonchaeae life cycle: egg, larva, protonymph, deutony- Lima, Ganaspis carvalhoi Dettmer, Tropideucoila mph, and adult. Adults are bright red, depos- weldi Lima (Cynipidae), and Opius sp. iting bright red, oval eggs of about 0.1 mm and preyed upon by Belonuchus rufipennis long, on the underside of leaves or in crevices (Fabricius) (Staphylinidae). on the stems (Swaine et al., 1985). The length of the cycle from egg to adult varies from as little CONTROL Akamine et al. (1954) argued that as 18 days (30°C) to as long as 49 days (20°C) one of the most important steps in controlling (Oliveira, 1987). In Queensland (Australia), fruit flies is the elimination of over-ripe the life cycle takes about 6 weeks. According

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to Flechtmann (1989), this mite develops on necrosis, culminating in leaf drop. Attacked both upper and lower leaf surface, but prefers young stems dry from the extremity to the lower leaf surface. Large numbers congre- the base and eventually die (Flechtmann, gate in leaf axils, along grooves in the terminal 1989). In Queensland, Australia, B. phoenicis shoots and leaf stalks, and along the main infestations are usually most damaging dur- veins of leaves (Swaine et al., 1985). Severely ing the summer and autumn. Heavy infesta- infested leaves are completely webbed by tion may result in defoliation (Swaine et al., spider mites (Oliveira, 1987). 1985). In Hawaii, B. papayensis, known as red Female spider mites are < 0.5 mm long, mite, is one of the most troublesome pests of and red. Males are slightly smaller than passion fruit, but it is usually most damaging females, and greenish yellow. The life cycle in areas of low rainfall and during prolonged of spider mites comprises five stages: egg, dry weather. Its effects are yellowing, shrivel- larva, protonymph, deutonymph, and adult. ling, and falling of the leaves. With heavy and The length of female and male life cycles is prolonged infestation, leaf fall increases and about 18 and 20 days, respectively (Oliveira, the vine has the appearance of dying back. At 1987). The period of incubation is 5–6 days. the same time, developing fruit may begin to The larva of T. mexicanus is light yellow with shrivel and fall prematurely from the plant. three pair of legs, and the larval stage requires Close examination reveals the presence of 4–7 days. Its protonymph is reddish yellow mites as scattered reddish patches on the with four legs and develops in 4–5 days. The surface of the fruit, particularly around the deutonymph completes its development in stem end, along the midrib and veins of the 2–4 days (Dominguez-Gil, 1998). leaf, especially on the under-surface. If red Polyphagotarsonemus latus females are spider mites are left uncontrolled, the plant about 0.2 mm in length. The body varies may eventually die (Akamine et al., 1954). in colour from white to yellowish. Males are Red spider mites cause a general weaken- smaller than females, and hyaline (Brandão ing of the plants. Initial damage to foliage et al., 1991). The entire cycle from egg to adult appears as fine silver speckling on the lower takes about 3–5 days. The species develops surface of the leaves, which turn brownish rapidly through four stages: egg, larva, pupa, on the upper side as mites continue to feed. If and adult. This mite attacks young leaves, and a large number of mites are present, entire its colonies are localized on the lower leaf leaves or plants turn yellow and necrotic surface (Oliveira, 1987). (Oliveira, 1987). Photosynthesis and trans- piration of the plants are suppressed. Dense HOST PLANTS A wide variety of host plants populations of spider mites produce silken are attacked by the mites. Brevipalpus phoenicis webs that cover the leaves. Heavy infestations feeds on citrus, coffee, cashew, papaya, cause leaves to drop and plants to lose vigour banana, guava, pomegranate, apple, loquat, (Oliveira, 1987). peach, pear, grape, grevillea, and various P. latus induces malformations in devel- weeds (Oliveira, 1987). Tetranychus desertorum oping leaves, which later dry and drop. It occurs on cotton, sweet potato, bean, papaya, may attack flowering buds, causing a reduc- passion fruit, strawberry, peach, tomato, tion in the number of flowers, and in turn, grape, and certain ornamentals. Tetranychus of fruits produced per plant (Oliveira, 1987; mexicanus feeds upon cotton, citrus, apple, Flechtmann, 1989). papaya, passion fruit, pear, peach, cacao, walnut, and ornamentals (Flechtmann, 1989). NATURAL ENEMIES Important natural ene- Hosts of P. latus are bean, potato, cotton, mies of spider mites are predacious mites coffee, citrus, apple, pumpkin, walnut, grape, belonging to Phytoseiidae. The life history of peach, pepper, rubber plantation, and various these predators is closely related to that of weeds (Oliveira, 1987). their host. Larvae and adults of Stethorus sp. (Coccinellidae) were also observed as preda- INJURY Brevipalpus phoenicis is responsible tors of T. mexicanus in passion fruit plantations for general discoloration of the leaves, and in Lake Maracaibo (Venezuela) when spider

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mites reached high population densities DESCRIPTION AND LIFE HISTORY The charac- (Dominguez-Gil and McPheron, 1992). teristic of Myzus is the presence on the head of tubercles at the base of the inner side of anten- CONTROL Periodic inspections of the nae. Because of this, the frons shows an outline orchard and other adjacent hosts, including that is scooped out in the middle. The apterous weeds, are essential to verify the occurrence form of M. persicae is 1.2–2.3 mm long, and fre- and first symptoms of mite attacks (Oliveira, quently pale green in colour, but populations 1987; Brandão et al., 1991). Mites have also also occur that are yellowish or tending to red- become resistant to many of the organophos- dish. The cornicles are long and cylindrical, phate miticides. Selective miticides, dosages, sometimes with a slight swelling of the distal timing, and refining application techniques part, which is often blackish. The cauda is may be useful in an integrated mite manage- subtriangular, shorter than the cornicles. The ment system. The four principal requirements length of the antennae is a little less than for a practical operation are: (i) presence of that of the body. The alate form is about predacious mites in the orchard; (ii) know- 1.2–2.2 mm in length and green in colour; ledge of the appearance and habits of plant- head, antennae and thorax are brown or feeding and predacious mites; (iii) careful blackish (Barbagallo et al., 1997). examination of relative numbers of predators The apterous form of the cotton aphid, and plant-feeding mites, particularly during a A. gossypii, has an ovoid body shape, and period when rapid population changes are is medium to small in size (1.0–1.8 mm in occurring; and (iv) knowledge of pesticides to length). Colour is variable, from ochreous use, how to use them, and what pesticides to brown to mottled, more or less dark green or avoid, in order to conserve predators. even bluish tinged. Antennae are brown with Flechtmann (1989) recommended the use the middle part cream coloured; cornicles and of sulphur that is not toxic to pollinating cauda are blackish brown. The alate form has insects. According to Piza Júnior (1992), head and thorax blackish, as are the antennae, fenthion, propargite, chlorfentezine, and cornicles and cauda; the abdomen has the avermectin are effective miticides. same variation in colour as does the apterous form. Length of body is 1.2–2.0 mm. The cotton aphid has a nearly cosmopolitan world Secondary Pests distribution. This species is of greater serious- ness in warm-temperate regions and in the intertropical zone. It is typically anholocyclic, Secondary pests include various species remaining active during the whole year with of insects that may become abundant, and uninterrupted generations of parthenogenetic occasionally damage the passion fruit crop. females. However, there are recorded cases The insects in this group are either associated of the appearance of sexual forms, with the frequently with a particular environmental subsequent deposition of resistant eggs on condition, or else occur within limited various plants (Barbagallo et al., 1997). geographical areas. M. solanifolii is about 2.6–4.0 mm in length, green, with wax secretions on the body of immature forms (Barbagallo et al., 1997). Aphids HOST PLANTS Peach is the preferred primary Aphids (Aphidae) are known to attack host of M. persicae. It may infest other Prunus passion fruit vines, although they seldom species, in particular almond and plum. Its cause serious damage. Nevertheless, at least secondary host plants include numerous wild three species of aphids, Myzus persicae and cultivated plants, such as passion fruit (Sulzer), Aphis gossypii (Glover), and Macro- (Barbagallo et al., 1997). Aphis gossypii infests siphum solanifolii Ashmead (= M. euphorbiae numerous species of dicotyledonous plants, (Thomas)), must be regarded as potentially including passion fruit. Favoured hosts are important pests of passion fruit. in the Malvaceae (cotton, hibiscus, etc.) and

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Cucurbitaceae (pumpkin, cucumber, water- Fancelli, 1993). Peridroma saucia (Hübner) melon, melon) (Barbagallo et al., 1997). M. (Noctuidae) attacks the floral structure, and solanifolii is a very polyphagous species, show- may reduce fruit production (Chacón and ing preference for the Solanaceae, i.e. potato, Rojas, 1981). Pyrausta perelegans (Hampson) tomato, etc. (Barbagallo et al., 1997). (Pyralidae) is also associated with passion fruit flowers. In Colombia, this species is INJURY Although these aphids cause mal- one of the most important pests of curuba, formation in foliage, they are more important and may infest 70% of the crop. Caterpillars as disease vectors. Myzus persicae and A. of Aepytus (Pseudodalaca) serta (Schaus) gossypii transmit a virus disease that causes a (Hepialidae) and Odonna passiflorae Clarke disease associated with hardening of fruits (Oecophoridae) are passion fruit stem borers (Brandão et al., 1991; Piza Júnior and Resende, (Chacón and Rojas, 1984). 1993). Myzus persicae and M. solanifolii are vec- tors of the passion fruit woodiness virus in DESCRIPTION AND LIFE HISTORY Caterpillars Australia. In Hawaii, however, where these of A. penicillana lodge in flowering buds or in a two species are present, this virus does not nest made from leaves, which are joined by occur (Akamine et al., 1954). silk webs produced by the insect. The cater- pillar is whitish, and when fully grown, NATURAL ENEMIES Naturally occurring pre- 25 mm long. The adult is a small pale greyish dators and parasites are effective against moth (Santos and Costa, 1983; Fancelli, 1992b; aphids. The Coccinellidae are effective against Fancelli, 1993). P. saucia is a moth with a cotton aphids, and in particular the larval 39 mm wingspan. Forewings are crimson red, stage of Scymnus. Other predators include the hindwings are whitish. Females lay their eggs Chrysopidae (Chrysoperla), Cecidomyiidae on the underside of leaves, usually in clusters (Aphidoletes) and Syrphidae (Syrphus). Para- of 60–244. Eggs are about 0.7 mm in diameter. sitism by Lysiphlebus sp. (Aphidiidae) has Eggs are creamy white when first laid, but been reported (Barbagallo et al., 1997). Accord- turn reddish blue when close to hatching, after ing to Grasswitz and Paine (1993), Lysiphlebus 8–10 days, depending on temperature. The testaceipes (Cresson) parasitizes Myzus, Aphis, newly hatched larva, approximately 0.97 mm and Macrosiphum. Silva et al. (1968) reported long, is reddish brown; full-grown larvae are parasitism of M. solanifolii by Aphidius platensis about 40 mm, and brownish grey. The larva Brèthes, A. brasiliensis Brèthes, Diaeretiella has six instars and becomes fully grown in rapae (McIntosh) (Aphidiidae), and predation 31–38 days. The pupa is about 18.1 mm in by Bacha clavata (F.) (Syrphidae), Coccinella length and dark brown. The pupal stage lasts ancoralis Germar, Cycloneda sanguinea (L.), and from 18 to 22 days (Chacón and Rojas, 1981). Eriopis connexa (Germar) (Coccinellidae). They Moths of A. serta are pale brown and have also reported parasitism of M. persicae by a wingspan of about 45 mm. Eggs, each about Aphelinus mali (Hald.) (Aphelinidae), A. 0.65 mm in diameter, are light yellow and laid platensis, and D. rapae in Argentina and on the bark of stems near the ground. The Uruguay. Cabbage aphid is the primary host larva is cream in colour with a dark brown of D. rapae which is commercially available head. The full-grown larva is about 38 mm. for release against a wide range of aphids, Pupae are light brown and about 39 mm long, especially Myzus and Brachycaudus spp. and 34 mm in length for females and males, (Hsieh and Allen, 1986). respectively (Chacón and Rojas, 1984). The adult moth of O. passiflorae has a wingspan of 24–30 mm. The head and thorax are greyish, and the dorsal of the abdomen is Caterpillars olive-green anteriorly, and greyish posteri- orly. The full-grown larva is 18–21 mm long Caterpillars of Azamora penicillana (Walker) with a light brown head and cream coloured (Pyralidae) are defoliators of passion fruit body, with several setae. The pupa is dark yel- (Santos and Costa, 1983; Fancelli, 1992b; low and about 9.5–13.0 mm long. The pupal

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stage occurs inside galleries constructed by outside the principal and lateral stems. Sev- the larvae (Chacón and Rojas, 1984). eral larvae in different stages of development The adult P. perelegans is a pale coloured attack simultaneously at the same point of the microlepidopteran with a wingspan of about stem, and cause cellular hypertrophy. They 35 mm. The wings are yellow semi-hyaline. form galleries in different directions, resulting The borders of the forewings are dark rose. in total destruction of the stem. The young larva is about 1.95 mm long and The caterpillars of P. perelegans infest green. The full-grown larva is about 23.8 mm 6-month-old plants, and remain during the long, and the pupa is dark brown and about whole vegetative period. They attack the buds 13.24 mm long (Chacón and Rojas, 1984). and developing flowers, feeding on nectaries, gynophores, and young fruits (Chacón and HOST PLANTS A. penicillana was reported Rojas, 1984). damaging a wild species of passion fruit (Passiflora cincinnata) in Brazil (Fancelli, 1993). NATURAL ENEMIES Naturally occurring pre- P. saucia damages and causes reduction in dators and parasites are particularly effective fruit production of curuba (Passiflora mollis- against P. saucia in Colombia. A tachinid fly, sima). It is a polyphagous insect, feeding on Incamyia sp., is an important factor for reduc- potato (Solanum tuberosum), oak (Quercus ing the population of P. saucia caterpillars. suber), Calendula officinallis, cotton, tobacco, Another dipterous parasitoid is Megaselia bean, tomato, lucerne, soybean, and beet scalaris (Phoridae). Adults of the predator (Chacón and Rojas, 1981). Anisotarus sp. (Carabidae) feed on caterpillars and prepupae. Some caterpillars may also INJURY Although the caterpillars of A. be infected by bacteria (Bacillus cereus, Pseudo- penicillana cause defoliation, the most serious monas aeruginosa and Streptococcus spp.) damage is caused by the phytotoxic effects of and nematodes (Pseudodiplogasteridae). The the fluid secreted by the caterpillar on the larval stage of O. passiflorae is infected with the leaves and young stems. Heavy infestations fungus Beauveria bassiana and is parasitized cause leaves to dry and drop, and passion fruit by the hymenopteran Neotheronia sp. (Ichneu- plants lose vigour and bear fewer flowers. monidae). Sathon sp. (Braconidae) and Enytus In Bahia, Brazil, the population peak of this sp. (Ichneumonidae) parasitize larvae of P. pest occurs during the rainy season (April to perelegans. The former has gregarious behav- June) (Santos and Costa, 1983; Fancelli, 1992b, iour, and on average 11 adult wasps may 1996). emerge from one larva (Chacón and Rojas, P. saucia larvae feed upon floral struc- 1984). tures of P. mollissima. Young larvae migrate from leaves to the flowers where they feed CONTROL According to Chacón and Rojas on the floral tube, nectary and gynophore, (1984), the infestation of A. serta depends causing flower dropping. The sixth instar on the wood used to made the trellises. The larvae may occasionally continue feeding authors suggest the use of resistant wood on the young fruit, or drop onto the soil to such as mangrove (Rhizophora mangle). Wood pupate. In Colombia, P. saucia infested 64% of Barbados cherry (Malpighia glabra) and of the flowers during the summer (July to Cassia tomentosa are susceptible to attack by September) (Chacón and Rojas, 1981). A. serta, and are not recommend for trellises. Larvae of A. serta bore into roots located near the surface, and occasionally bore into stems. Stem injury is characterized by the presence of sawdust. A single larva is Mealybugs regularly found in 1-year-old plants, while in 6–8-year-old plants, up to five larvae may Citrus mealybug, Planococcus citri Risso, and develop (Chacón and Rojas, 1984). the passion vine mealybug, Planococcus The damage of O. passiflorae caterpillars is pacificus Cox (Pseudococcidae), are pests of characterized by the presence of sawdust lesser importance on passion fruit.

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DESCRIPTION AND LIFE HISTORY Citrus mealy- death of the plant (Murray, 1976; Swaine et al., bug, P. citri, is a small, oval-shaped sucking 1985). insect commonly found on passion fruit in Hawaii, USA. A white, mealy powder covers NATURAL ENEMIES Lady beetles (Coccinel- the upper surface of the insect body. Wax lidae), especially mealybug lady beetle, strands radiate from the body with slightly Cryptolaemus montrouzieri Mulsant, and longer strands posteriorly. Females are wing- maculate lady beetle, Harmonia octomaculata less and vary in length from 3 to 4 mm. The (Fabricius), substantially reduce mealybug males are fragile, with two wings, and 2 mm numbers. Of secondary importance are in length with two long white filaments small wasp parasitoids such as Leptomastidea extending from the end of the abdomen. The abnormis (Girault) (Encyrtidae) and Ophelosia female is active and feeds throughout its sp., and lacewing larvae (Oligochrysa lutea life. The male feeds only during the first (Walker)) (Murray, 1978; Swaine et al., 1985). stage (Murray, 1976). After mating, the female Silva et al. (1968) reported several species deposits up to 500 yellowish eggs in a of parasitoids and predators of P. citri in loose cottony mass or ovisac and then dies. Argentina. It is parasitized by Apanteles para- Crawlers emerge from the eggs in 3–9 days guayensis Brèthes (Braconidae), Coccophagus and moult several times until the adult stage is caridei (Brèthes) (Aphelinidae), Anagyrus reached. There are three moults in the female coccidivorus Dozier, A. pseudococci (Girault), and four in the male. Approximately 4 weeks Leptomastidea abnormis (Girault), Leptomatrix are required for completion of the cycle dactylopii Howard (Encyrtidae), and Pachyneu- during warm weather (Murray, 1976). ron sp. (Pteromalidae). Leptomastix dactylopii is The females of passion vine mealybug, P. commercially available. It is a yellowish brown pacificus, are white, oval and about 3–4 mm wasp that lays its eggs in late instar nymphs long. Eggs are laid in a loose, cottony mass and and adult mealybugs. Leptomastix prefers hatch to produce crawlers 3–9 days later. hosts in warm, sunny, humid environments. It Development from egg to adult takes about may complete one generation in 2 weeks at 4 weeks during summer. In Queensland (Aus- 30°C or in 1 month at 21°C (Fisher, 1963). tralia), these species are most common in late summer and autumn (Swaine et al., 1985). CONTROL Clusters of mealybugs under dead leaves are well protected from the insec- HOST PLANTS Citrus mealybug infests citrus ticide sprays, and little control can be achieved and many greenhouse and indoor plants. unless vines are cleaned thoroughly to allow Other plants recorded as its hosts include spray penetration. Pruning may enhance the avocado, pineapple, pumpkin, cotton, rice, effectiveness of the spray; however, this is sweet potato, potato, cacao, coffee, sugarcane, often impractical, as laterals to be pruned are chayote, tobacco, guava, mango, rose, pome- generally bearing fruits (Murray, 1976). granate, etc. (Silva et al., 1968). According to Murray (1976), occasional outbreaks of this pest are best controlled by INJURY Mealybugs characteristically aggre- two sprays of 1 : 60 oil or methidathion 0.05% gate on the plant, especially at leaf nodes combined with 1 : 100 oil, 2 weeks to 1 month and under dead leaves and trash. Aggregation apart. The 1 : 60 oil is preferred, as methidath- may also occur under dried flower bracts. ion is highly toxic to the mealybug’s natural Secretion of a sugary solution from the mealy- enemies. For good control, thorough coverage bugs promotes growth of a black fungal is essential. mould on the fruits and leaves. Ants are often found tending mealybugs for this secretion and interfere with the natural control of the mealybugs by parasites and predators. Scales If a severe infestation occurs, loss of vigour, leaf drop, and fruit malformation may Soft brown scale (Coccus hesperidum Lin- occur. Unchecked, an infestation may cause naeus) (Coccidae) may occasionally infest

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leaves and stems of passion fruit. California Azya luteipes Mulsant, Coccidophilus red scale, Aonidiella aurantii (Maskell) (Dia- citricola Brèthes, and Pentilia egena Mulsant spididae), is most common on older passion have been recorded as predators of California fruit vines (Swaine et al., 1985). red scale. Two species recorded as pathogenic fungi of this scale are Nectria coccophila and DESCRIPTION AND LIFE HISTORY Adults of soft Myriangium duriaei (Silva et al., 1968). brown scale are approximately 3 mm long, According to Forster et al. (1995), Aphytis and covered by a brown, oval, dome shaped melinus is the most important parasitoid scale. A sweet, sticky secretion produced by attacking California red scale. The adult is a this insect promotes growth of sooty mould on tiny yellow wasp. The female A. melinus feeds the fruit and leaves. Ants also tend the scale on and oviposits in immature scales, prefer- for this secretion (Murray, 1976). ring the virgin adult female scale. The solitary, California red scale is a small, flattened, ectoparasitic larva leaves a flat and dehydrated reddish orange scale. The dull-red female pro- scale body beneath the scale cover, where duces living young or crawlers that shelter the parasitoid’s cast skin and faecal pellets under the parent scale for some time. After (meconia) may be observed. The parasitoid’s leaving the protection of the parent scale, the short life cycle (10–20 days) results in two crawlers quickly settle on the vine or fruit and or three parasitoid generations for each scale then moult – twice if a female, three times if a generation. Comperiella bifasciata is an impor- male – before reaching the adult stage. The life tant encyrtid that parasitizes California red cycle from egg to adult takes about 6 weeks in scale. Adult parasitoids are black, with two summer (Swaine et al., 1985). white stripes on the female’s head. One parasitoid generation requires about 3–6 HOST PLANTS California red scale infests weeks to develop, with faster development citrus and many ornamental plants (Forster occurring on larger (later instar) hosts and at et al., 1995). Silva et al. (1968) cited several warmer temperatures. other host plants of this species such as pump- Parasitoids of C. hesperidum in Argentina kin, coconut, papaya, rose, mulberry, etc. are Aneristus coccidis Blanchard, Coccophagus Soft brown scale uses various plants caridei (Brèthes), Ablerus ciliatus De Santis (sec- as host, such as avocado, sapodilla, plum, ondary parasitoid) (Aphenilidae), Aphycus mulberry, coconut, gladiolus, papaya, laurel, flavus Howard, A. luteolus (Timberlake), and salvia, maté, pear, rose, grape, etc. (Silva et al., Cheiloneurus longisetaceus De Santis (Encyr- 1968). tidae). Among the predators is Azya luteipes Mulsant (Coccinellidae) (Silva et al., 1968). INJURY Soft scales and diaspidids injure plants by sucking sap, and when numerous CONTROL Chemical control is often not can kill the plant. They sometimes heavily required since parasitization by small wasps encrust the leaves, fruits, twigs or branches. substantially reduces populations. Should Mealybugs may be found on almost any part chemical control be necessary, a 1 : 60 oil of the host plant from which they suck the sap spray is satisfactory (Murray, 1976). (Murray, 1976; Swaine et al., 1985).

NATURAL ENEMIES Parasitic wasps are Termites important to control A. aurantii, mainly Comperiella bifasciata (Howard), and Aphytis Termites are increasingly common in passion chrysomphali (Mercet) (Aphelinidae) (Murray, fruit plantations, but losses attributable to 1976; Swaine et al., 1985). In Argentina, this them have not been quantified. Three termite species was reported to be parasitized by species, Heterotermes convexinotatus (Snyder), the aphelinids, A. chrysomphali, A. maculicornis Amitermes foreli Wasmann, and Microceroter- Masi, and Aspidiotiphagus citrinus (Crawford) mes arboreus Emerson, were observed to feed (Silva et al., 1968). on roots and stems of 2–4-year-old passion

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fruit plants in Venezuela (Dominguez-Gil Bees and McPheron, 1992). In some passion fruit growing areas, the DESCRIPTION AND LIFE HISTORY Heterotermes honeybee Apis mellifera L. (Apidae) is consid- (Rhinotermitidae) is a widespread genus. It is ered a pest since it robs the pollen from the characterized by the soldier which has a long carpenter bees, thereby causing a reduction and rectangular head. It does not have teeth of fruit set (Akamine et al., 1954). Adults of on the interior curvature of the mandibles. The Trigona spinipes Fabricius (Apidae), known as pronotum is wide and flat (Hadlington, 1987). irapuá or arapuá in Brazil, attack leaves, It has subterranean habits, and does not con- stems, trunk, developing buds, developing struct an exposed nest. The colony always fruits, and fruit peduncles of several plant remains in contact with the soil through the species (Puzzi, 1966; Bastos, 1985; Teixeira galleries (Dominguez-Gil, 1998). et al., 1996). It may be found from northern to Amitermes (Termitidae) is cosmopolitan southern Brazil (Silva et al., 1968; Bleicher and in distribution and especially conspicuous in Melo, 1993). Carvalho et al. (1994) reported the tropics and in the warmer areas of the serious damage caused by T. amazonensis to temperate zones (Krishna and Weesner, 1970). yellow passion fruit in Acre (Brazil). The members of this genus are essentially sub- terranean in habit. The nest is usually situated DESCRIPTION AND LIFE HISTORY Trigona in the soil (Krishna and Weesner, 1970). Its spinipes is about 5–6.5 mm in length, black soldiers have the mandibles curvated, thin, with transparent wings and without an ovi- not too long, and with a prominent tooth and positor (Santos and Costa, 1983). It constructs not clearly rectangular (Hadlington, 1987). its nests on trees, usually between their Subterranean soldiers of Microcerotermes branches, or in abandoned termite nests. It (Termitidae) have long, rectangular mandi- uses fibrous filaments of plant material and bles, which are serrated on the interior face agglutinative elements, mainly resin. Like (Hadlington, 1987). A queen of M. arboreus, honeybees, they exist in large colonies with measuring 21 mm in length, may deposit 1680 a queen, without corbiculae, and with thou- eggs in 24 hours (Krishna and Weesner, 1970). sands of workers (Riek, 1979).

INJURY Termites penetrate and excavate the INJURY Trigona spinipes causes malfor- roots and continue upwards within the stems. mation of foliage and dropping of flowers, The plant often dies, and death may be associ- resulting in a reduction in the number of fruits ated with the presence of soil pathogens, which produced per plant. It also attacks developing usually cause rotting, including Fusarium spp. flowering buds (Fancelli and Mesquita, 1998). and Phytophthora spp. (Dominguez-Gil and McPheron, 1992; Piza Júnior, 1992). HOST PLANTS Trigona spinipes damages various plant species, especially flowering CONTROL The use of tillage operations to buds and leaves, of sapodilla, mulberry, reduce populations of soil-inhabiting insects banana, citrus, coconut, mango, rose, pine, may work in several ways. In the case of and fig (Silva et al., 1968). termites, it may change the physical condition of soil and expose the colony to the sun. Piza NATURAL ENEMIES Silva et al. (1968) reported Júnior (1992) recommended that after tillage, the parasitism of larvae of T. spinipes by the soil should be treated with Thiodan 350 CE Pseudohypocera nigrofascipes Borgn. & Schn. (endosulfan) at 100–500 cm3 per 100 l of water. (Phoridae). The soil must be treated when it is wet to allow the penetration of the insecticidal solution. CONTROL Recommendations to prevent When the crop is already established, the insec- honeybees from robbing passion fruit flowers ticidal solution must be applied to the soil of their pollen have been made. One of them is around the plants in large quantities to reach a to plant more attractive plant species such depth of 35 cm. as eucalyptus and basil in adjacent areas to

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382 E.L. Aguiar-Menezes et al. n ó .,

al 1993; 1995 ., et Chac al Bortoli 1977; McPheron, McPheron, McPheron, McPheron, 1984; 1984; 1984 1984 1984

et ., De Silva al Kavati, 1974; 1994 1994 1994 and and and and 1991;

et ., ., Filho Rojas, Rojas, Rojas, Rojas, Rojas, al a 1987 al and 1984; ê

et 1952b; 1994 1994 et 1994 and and and and and nior o n n n n n Teixeira, Racca Teixeira, Corr Teixeira, ú ã ó ó ó ó ó J Busoli, Rojas, Chac Teixeira, Teixeira, Rossetto Dominguez-Gil 1992; Dominguez-Gil 1992; Chac Dominguez-Gil 1992; Teixeira, 1968; Chac References Dominguez-Gil 1992; Brand Piza Chac Lordello, and Chac and adult adult adult adult adult adult and and and and and and stage adult adult nymph nymph nymph nymph nymph nymph and and Adult Larva, Larva, Larva, Larva, Larva, Larva, Damaging Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Adult Larva Larva Larva Larva Larva Larva Larva Adult Adult Adult Larva world. the chewer chewer chewer chewer chewer leaf leaf fruit around flower chewer pollen habits and and and borer borer borer borer borer borer borer on sucker sucker sucker sucker sucker sucker chewer chewer chewer chewer chewer chewer chewer and chewer chewer chewer spp.) Feed Fruit Leaf Leaf Leaf Leaf Leaf Feeding Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Flower-bud Seedling Leaf Stem Stem Stem Stem Stem Stem Stem Leaf Flower Flower Calyx

Passiflora ( M. fruit (F.) é (Banks) é (Banks) (Germar) (McGregor) Degeer

Schaarschmidt latus (Geijsks) Bechyn Brien passion (F.) ’ Wood Harold Latreille Hood (F.) (F.) (Koch) Bechyn O (F.) Germ. with undecinpunctata Champion

melanocephala sp.

stammeri mexicanus desertorum urticae sp. auripes phoenicis sp. bispinus marginata famelica melanoptera orphelia walteriana cingulata bogotana sp. fasciculatus poss. sp.

diadema sp.

name conspicua atomaria passiflorae obesus crucifer associated

Scientific Tarsonemus Polyphagotarsonemus Tetranychus Tetranychus Tetranychus Brevipalpus Frankliniella Trichaltica Euryscopa Cacoscelis Cacoscelis Cacoscelis Cacoscelis Cacoscelis Diabrotica Maecolaspis Monomarca Acalymma Litostylus Philonis Philonis Philonis Chramesus Stenygra Lepturges Stizocera Epicauta Cyclocephala Leucothyreus Araecerus arthropods Thripidae Tarsonemidae Tetranychidae Tenuipalpidae Chrysomelidae Family Curculionidae Scolytidae Cerambycidae Meloidae Scarabaeidae Anthribidae Phytophagous 12.2. e l b a INSECTA Thysanoptera ARACHNIDA Acari T Class/Order Coleoptera

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Passion Fruit 383 and De n Brown ó and 1952a, Sazima continued n McPheron, McPheron, 1984 1984 1984; 1984 1984 1984; 1984 ó 1983; 1972; 1987; Chac 1968; 1998 1998 ., 1992 1994; and and

al Chac ., Dominguez-Gil Lordello, 1989; Rojas, Rojas, Rojas, Rojas, Rojas, Rojas, Rojas, al et Costa, 1968; Busoli, Mielke,

et ., 1992b and and and and and and and al 1976; and 1992; 1931; and 1984 1984 and n n n n n n n Silva et ó ó ó ó ó ó ó McPheron, Sazima, nior ú Silva Fancelli, Chac Chac Santos Chac Chac and Bortoli Carter, Rojas, Chac and Dominguez-Gil, Dominguez-Gil 1992 J Chac Carvalho 1954; Santo, Murray, Rojas, Chac Dominguez-Gil, Dominguez-Gil 1992 adult adult adult and and and (workers) (workers) (workers) Adult Adult Adult Adult Adult Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Nymph Nymph Nymph Adult Adult Adult stem stem stem borer chewer and and and fruit sucker fruit stem stem root root root chewer chewer chewer chewer chewer chewer and borer borer borer sucker sucker on on on on on stem flower, chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer chewer Feed Flower Flower Flower Feed Stem Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Stem Flower Flower Flower Stem Bud, Leaf Calyx Stem Stem Leaf, Feed Feed Feed tries (R) é e) bner) n é bner) Druce (Snyder) ü é ü S. Emerson (Weymer) M (H (Godart) (Godart) (H (L.) (F.) (Guen Felder) . bner)

wernickei (Hampson) L.

matrica (Walker) (Walker) ü Clarke R (L.)

robigus (Schaus) (Olivier) (H & arboreus aliphera narcaea F. huebneri dianosa vanillae maculosa Wasmann phyllis (L.) (L.) apseudes sp. sp. poss.

conexinotatus (C.

serta sp.

ornihogalli sp.

sp. foreli juno dido wernickei sp. silvana sara ethilla erato saucia consueta sp. phaetusa perelegans penicillana

isabella isabella aliphera vanillae vanillae (P.) passiflorae amalthea spinipes amazonensis hesperidium

juno glycera

Trigona Trigona Trigona Crematogaster Solenopsis Heterotermes Microcerotermes Amitermes Eueides Eueides Eueides Dione Dione Agraulis Agraulis Dryadula Philaethria Philaethria Heliconius Heliconius Heliconius Heliconius Sabulodes Aepytus Peridroma Copitarsia Spodoptera Odonna Pyrausta Azamora Pococera Langsdorfia Coccus Ceroplastes Hexaleurodicus Coccidae Aleyrodidae Nymphalidae Rhinotermitidae Termitidae Geometridae Hepialidae Noctuidae Oecophoridae Pyralidae Cossidae Apidae Formicidae Homoptera Isoptera Lepidoptera Hymenoptera

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384 E.L. Aguiar-Menezes et al. o ã ., ., and

al al and n and ó

et et n Brand Lordello, ó Busoli, 1988; Santos nior 1984 1992 Rojas, ú 1968; Chac Dominguez- J and Chac ., Chiavegato, 1974; 1954; 1954; and Swaine 1976; Dominguez-Gil, Swaine al ., ., ., Zucchi, Rojas, n Piza al al et al 1983; ó 1987; 1987 1993 Bortoli 1980; et 1952; et et 1994 and 1976; 1976; 1976; McPheron, 1984; 1984 n Murray, ICA, De Chac ICA, Silva 1991; ó Costa, ., and

al Rossetto Resende, Murray, Teixeira, Chac Rojas, 1954; and 1987; Gil 1984; Murray, 1998; References 1985; Akamine 1985 Mariconi, 1963; Steyskal, Rojas, Akamine Murray, et adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult stage and and and and and and and and and and and and and and and Damaging Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Larva Nymph Nymph Nymph Nymph Nymph Nymph Nymph suckers bud bud bud bud chewer stem sucker sucker sucker sucker sucker sucker sucker sucker fruit flower flower flower flower fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit fruit habits on on on on on on on on on on on on on on on on fruit fruit fruit fruit fruit fruit fruit fruit fruit, sucker sucker sucker sucker sucker Feeding Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Leaf, Feed Feed Feed Feed Flower-bud Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Feed Leaf, Leaf Leaf Leaf Leaf Leaf (Loew) (Stal) Guerne (Morgan) marginella Ashmead (F.) (Loew) Lima Wheeler (F.) Cox (Herbest.) (F.) (Walker) (Macquart) (Hendel) McAlpine (F.) McAlpine Coquillett (Maskell) (F.) Steykal Risso Steykal (Dallas) Lima (Sulzer) (Wiedemann) (Glover)

articulatus solanifolii Bezzi gonagra conspersus citri pacificus (Froggatt) histro clavigera salebrosa pallidipennis consobrina ethalea grandis kuhlmanni lutzi pseudoparallela foliacea flavolineata dorsalis

auranti cristula name

capita curubae inedulis passifloris zonatus bilineatus persicae curcubitae tryoni gossypii pendula

Scientific Selenaspidus Aonidiella Myzus Aphis Macrosiphum Planococcus Planococcus Holhymenia Holhymenia Veneza Leptoglossus Leptoglossus Anisoscelis Anisoscelis Diactor Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Anastrepha Ceratitis Dacus Bactrocera Dacus Zapriothrica Lonchaea Silba Dasiops Dasiops Dasiops . Tephritidae Drosophilidae Lonchaeidae Coreidae Diaspididae Aphididae Pseudococcidae Family

Continued 12.2. e l b a Diptera Hemiptera T Class/Order

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Passion Fruit 385

passion fruit. Collection of wild swarms is also Back, E.A. and Pemberton, C.E. (1918) The Medi- recommended (Boaretto et al., 1994). The con- terranean fruit fly in Hawaii. United States trol strategies recommended for T. spinipes Department of Agricultural Bulletin 536, 1–118. include the destruction of nests near the crop, Barbagallo, S., Cravedi, P., Pasqualini, E. and Patti, I. (1997) Aphids of the Principal Fruit-Bearing and weekly inspections to verify the occur- Crops. Bayer, Milan, 123 pp. rence of this pest on flowers. In exceptional Bastos, J.A.M. (1985) Principais Pragas das Culturas cases, chemical control is recommended. e Seus Controles, 3rd edn. Nobel, São Paulo, 329 pp. Bateman, M.A. (1972) The ecology of fruit flies. Conclusions Annual Review of Entomology 17, 493–518. Bleicher, E. and Melo, Q.M.S. (1993) Artrópodes Associados ao Cajueiro no Brasil. EMBRAPA/ Several different species of arthropods have CNPAT, Fortaleza, Documentos 9, 33 pp. been reported in passion fruit. Other pests Boaretto, M.A.C., Brandão, A.L.S. and São José, A.R. doubtless occur, and new ones will appear in (1994) Pragas do maracujazeiro. In: São José, the future. Fortunately the majority of these A.R. (ed.) Maracujá, Produção e Mercado. DFZ/ species are not injurious. The species listed UESB; Vitória da Conquista, pp. 99–107. in Table 12.2 are generally accepted as being Boiça Júnior, A.L., Lara, F.M. and Oliveira, J.C. responsible for most of the insect and mite (1993) Resistência de genótipos de maracu- damage wherever passion fruit grows. jazeiro ao ataque de Dione juno juno Cramer, For control of insect and mite pests which 1779 (Lepidoptera: Nymphalidae). In: Resumos attack passion fruit, we must consider two do 14 Congresso Brasileiro de Entomologia. SEB, Piracicaba, p. 143. basic problems: (i) creation and preservation Brandão, A.L.S., São José, A.R. and Boaretto, M.A.C. of conditions favourable to carpenter bees, (1991) Pragas do maracujazeiro. In: São José, whose function in pollination is of vital A.R., Ferreira, F.R. and Vaz, R.L. (eds) A importance for fruit set; (ii) suitable control Cultura do Maracujá no Brasil. FUNEP, of insects and mites that damage the plant. Jaboticabal, pp. 136–168. Additionally, a latent problem is the conserva- Brown Júnior, K.S. and Mielke, O.H.H. (1972) The tion of natural enemies, which is complicated heliconians of Brazil (Lepidoptera: Nympha- because beneficial and noxious insects and lidae). Part II. Introduction and general mites are closely associated with the plant. comments, with a supplementary revision The timing of spraying is critical, so that of the tribe. Zoologia 57, 1–40. Camillo, E. (1978a) Aspectos reprodutivos de applications are not made when passion algunas espécies de Xylocopa (Hymenoptera: fruit flowers are open and the carpenter bees Anthophoridae). Ciência e Cultura 30, 594–595. are active. The choice of a selective pesticide, Camillo, E. (1978b) Polinização do maracujazeiro. with low toxicity to predators and parasites, is In: Anais do 2 Simpósio Sobre a Cultura do important to maintain not only natural control Maracujazeiro, Jaboticabal, pp. 32–39. but also pollinators. Camillo, E. (1980) Polinização do maracujazeiro. In: Ruggiero, C. (ed.) Cultura do Maracujazeiro. FCAN, Jaboticabal, pp. 47–53. Camillo, E. (1996) Utilização de espécies de References Xylocopa (Hymenoptera: Anthophoridae) na polinização do maracujá amarelo. In: Anais Akamine, E.K. and Girolami, D.G. (1957) Problems do 2 Encontro Sobre Abelhas. Ribeirão Preto, in fruit set in yellow passion fruit. Hawaii Farm pp. 141–146. Science 5, 3–5. Camillo, E. and Garófalo, C.A. (1982) On the Akamine, E.K. and Girolami, D.G. (1959) Pollination bionomics of Xylocopa frontalis (Olivier) and and Fruit Set in Yellow Passion Fruit. Hawaii Xylocopa grisescens (Lepeletier) in southern Agricultural Experiment Station, Honolulu, Brazil. I. Nest construction and biological cycle. Technical Bulletin 39, 32 pp. Revista Brasileira de Entomologia 42, 571–582. Akamine, E.K., Hamilton, R.A., Nishida, T., Caraballo, J. (1981) Las moscas de las frutas del Sherman, G.D. and Storey, W.B. (1954) Passion género Anastrepha Schiner, 1868 (Diptera: Fruit Culture. University of Hawaii, Extension Tephritidae) de Venezuela. MSc thesis, Circular 345, 23 pp. University Central de Venezuela, 210 pp.

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Carter, D. (1992) Butterflies and Moths. Dorling cuenca del Lago de Maracaibo, Venezuela: Kindersley, London, 304 pp. características morfológicas. Boletín del Centro Carvalho, E.F., Calixto, A.R.Y., Silva Filho, J.R. de Investigaciones Biológicas 32, 1–66. and Morato, E.F. (1994) Avaliação da Dominguez-Gil, O.E. and McPheron, B.A. (1992) polinização artificial na redução dos danos Arthropods associated with passion fruit in causados por Trigona amazonensis na cultura western Venezuela. Florida Entomologist 75, do maracujá amarelo. In: Anais do 13 607–612. Congresso Brasileiro de Fruticultura. SBF, Dominguez-Gil, O.E., Vera, H., Socarras, G. and Salvador, pp. 798–799. Carvajal, R. (1989) Posible epizootia de tipo Causton, C.E. (1993) Una mosca del genero Dasiops viral en larvas de Eueides isabella Ménétries y (Diptera: Lonchaeidae) atacando la curuba Dione juno juno (Cramer) defoliando planta- (Passiflora mollissima) en el Edo. Merida, Vene- ciones de parchita maracuyá en el Estado zuela. Boletín de Entomología Venezolana 8, 146. Zulia. In: Resúmenes del 11 Congreso Venezolano Chacón, P. and Rojas, M. (1981) Biologia y control de Entomologia. Sociedad Venezolana de Ento- natural de Peridroma saucia, plaga de la flor de mología, Maracaibo, p. 33. la curuba. Revista Colombiana de Entomologia 7, Donadio, L.C. (1983) Frutíferas tropicais de 47–53. valor potencial. In: Donadio, L.C. (ed.) Fruti- Chacón, P. and Rojas, M. (1984) Entomofauna cultura Tropical. FCAV/UNESP, Jaboticabal, asociada a Passiflora mollissima, P. edulis f. flavi- pp. 20–30. carpa y P. quadrangularis en el Departamento Echeverri, F., Cardona, G., Torres, F., Pelaez, C., del Valle del Cauca. Turrialba 34, 297–311. Quiñones, W. and Renteria, E. (1991) Ermanin: Chiavegato, L.G. (1963) Leptoglossus gonagra – praga an insect deterrent flavonoid from Passiflora do maracujá. O Agronômico, 15, 31–36. foetida resin. Phytochemistry 30, 153–155. Corbet, S.A. and Willmer, P.G. (1980) Pollination Fancelli, M. (1992a) A Broca da Haste do Maracujazeiro. of the yellow passionfruit: nectar, pollen and EMBRAPA/CNPMF, Bahia, Maracujá em carpenter bees. Journal of Agricultural Science Foco 53, 2 pp. 95, 655–666. Fancelli, M. (1992b) A Lagarta de Teia do Maracu- Corrêa, L.S., Ruggiero, C. and Oliveira, J.C. (1977) jazeiro. EMBRAPA/CNPMF, Bahia, Maracujá Ocorrência de Acalymma sp. (Coleoptera: em Foco 54, 2 pp. Chrysomelidae) sobre mudas de maracujá- Fancelli, M. (1993) Ocorrência de Azamora penicillana amarelo (Passiflora edulis f. flavicarpa Deg.). (Walk.) (Pyralidae: Chrysauginae) em mara- Científica 5, 229–230. cujá silvestre. Anais da Sociedade Entomológica do Costa, J.M., Correa, J.S., Santos, Z.F.A. F. and Ferraz, Brasil 22, 121–124. M.C.V.D. (1979) Estudos da Broca do Maracu- Fancelli, M. (1996) Insetos-pragas do maracujazeiro jazeiro na Bahia e Meios de Controle. EPABA, e controle. In: Lima, A.A., Borges, A.L., Santos Salvador, Comunicado Técnico 37, 10 pp. Filho, H.P., Fancelli, M. and Sanches, N.F. (eds) Cox, I.E. (1957) Flowering and pollination of passion Instruções Práticas Para o Cultivo do Maracu- fruit. Agricultural Gazette of New South Wales 68, jazeiro. EMBRAPA/CNPMF, Bahia, Circular 573–576. Técnica, 20, 44 pp. Cruz, C.A., Graça, D. and Lima, A.F. (1993) Fancelli, M. and Mesquita, A.L.M. (1998) Pragas Ocorrência de Philonis obesus em maracujazeiro do maracujazeiro. In: Braga Sobrinho, R., no Estado do Rio de Janeiro. In: Resumos do Cardoso, J.E. and Freire, F.C.O. (eds) Pragas de 14 Congresso Brasileiro de Entomologia. SEB, Fruteiras Tropicais de Importância Agroindustrial. Piracicaba, p. 16. EMBRAPA/SPI, Brasília, pp. 169–180. Cunha, M.A.P. (1996) Recursos genéticos e Figueiro, C.L.M. (1995) Aspectos biológicos e modificações em métodos de seleção para controle da lagarta Dione juno juno (Lepidop- produtividade em maracujá. Revista Brasileira tera: Heliconiinae) do maracujazeiro (Passiflora de Fruticultura 18, 413–423. edulis) por Baculovirus dione. MSc thesis, UFPa, D´Almeida, R.F. (1944) Estudos biológicos sobre Brazil, 73 pp. alguns lepidópteros do Brasil. Archivos de Fisher, T.W. (1963) Mass Culture of Cryptolaemus Zoologia do Estado de São Paulo 4, 44. and Leptomastix – Natural Enemies of Citrus De Bortoli, S.A. and Busoli, A.C. (1987) Pragas. Mealybug. University of California Agricul- In: Ruggiero, C. (ed.) Cultura do Maracujazeiro. tural Experiment Station Bulletin, No. 797. Legis Summa, Ribeirão Preto, pp. 111–123. Flechtmann, C.H.W. (1989) Ácaros de Importância Dominguez-Gil, O.E. (1998) Fauna fitófaga de Agrícola. Nobel, São Paulo, 189 pp. parchita maracuyá (Passiflora edulis f. flavicarpa) Forster, L.D., Luck, R.F. and Grafton-Cardwell, E.E. en las regiones oriental y suroriental de la (1995) Life Stages of California Red Scale and its

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Parasitoids. University of California, Division flavicarpa Deg.) na região de Campos dos of Agricultural Natural Research Publication, Goytacazes, RJ. In: Anais do 2 Encontro Sobre 21529. Abelhas. Ribeirão Preto, p. 330. Free, J.B. (1993) Insect Pollination of Crops, 2nd edn. Hsieh, C.Y. and Allen, W.W. (1986) Effects of Academic Press, London, pp. 404–409. insecticides on emergence, survival, longevity, Gilmartin, A.L. (1958) Post-fertilization seed and and fecundity of the parasitoid Diaretiella rapae ovary development in Passiflora edulis Sims. (Hymenoptera: Aphidiidae) from mummified Tropical Agriculturist 35, 41–58. Myzus persicae (Homoptera: Aphididae). Grasswitz, T.R. and Paine, T.D. (1993) Influence Journal of Economic Entomology 79, 1599–1602. of physiological state and experience on Hurd, P.D. (1978) An Annotated Catalog of the the responsiveness of Lysiphlebus testaceipes Carpenter Bees (Genus Xylocopa Latreille) of (cresson) (Hymenoptera: Aphidiidae) to aphid the Western Hemisphere (Hymenoptera: honeydew and host plants. Journal of Insect Anthophoridae). Smithsonian Institution Press, Behaviour 6, 511–528. Washington, 106 pp. Gravena, S. (1987) Perspectiva do manejo integrado Hurd, P.D. and Moure, J.S. (1963) A Classification de pragas. In: Ruggiero, C. (ed.) Cultura do of the Large Carpenter Bees (Xylocopini) Maracujazeiro. Legis Summa, Ribeirão Preto, (Hymenoptera: Apoidea). University of Cali- pp. 134–145. fornia Publications in Entomology, 366 pp. Haddad, G.O. and Millán, F. (1975) La Parchita ICA (1987) Guia para el Control de Plagas, 4th Maracuyá (Passiflora edulis f. flavicarpa edn. Ministerio de Agricultura, Instituto Degener). Fondo de Desarollo Frutícola, Colombiano Agropecuário/SOCOLEN, Caracas, Boletim Técnico 2, 82 pp. Manual de Asistencia Tecnica 1, pp. 232–237. Hadlington, P. (1987) Australian Termites. University Kluge, R.A. (1998) Maracujazeiro Passiflora sp. Press, New South Wales, Australia. In: Castro, P.R.C. and Kluge, R.A. (ed.) Hammer, L.H. (1987) The pollinators of yellow Ecofisiologia de Fruteiras Tropicais. Nobel, São passionfruit – do they limit the success of Paulo, pp. 32–47. Passiflora edulis f. flavicarpa as a tropical crop? Krishna, K. and Weesner, F.M. (1970) Biology of In: Proceedings of the Annual Meeting of the Termites. Academic Press, New York, 643 pp. Florida State Horticulture Society 100, 283–287. Leão, J.A.C. (1980) Considerações sobre as Hardin, L.C. (1986) Floral biology and breeding principais doenças e pragas do maracujá no systems for the yellow passion-fruit, Passiflora Nordeste do Brasil. In: Anais do 1 Encontro edulis f. flavicarpa. In: Proceedings of the Inter- Estadual da Cultura do Maracujá. EMATER-SE, American Society of Tropical Horticulture 30, Aracajú, pp. 67–71. 35–44. Lima, M.F.C. and Veiga, A.F.S.L. (1993) Ocorrência Hargreaves, J.R. (1979) Damage of passion-fruit do vírus da poliedrose nuclear (PNV) em by the Queensland fruit fly, Dacus tryoni lagartas de Dione juno juno (Cramer, 1779) (Froggatt). Queensland Journal of Agricultural sobre maracujazeiro, em Recife – Pernambuco. and Animal Sciences 36, 147–150. In: Resumos do 14 Congresso Brasileiro de Hernández, M.R., Rojas, M. and Trochez, A. (1985) Entomologia. SEB, Piracicaba, p. 143. Evaluacion de la proteina hidrolizada de maiz Lima, M.F.C. and Veiga, A.F.S.L. (1995) Ocorrência para la captura de Lonchaea cristula (Diptera: de inimigos naturais de Dione juno juno (Cr.), Lonchaeidae), plaga de la curuba en el Valle del Agraulis vanillae maculosa S. e Eueides isabella Cauca. Revista Colombiana de Entomologia 11, dianosa (Hüb.) (Lepidoptera: Heliconiidae) em 47–50. Pernambuco. Anais da Sociedade Entomológica do Hernández-Ortiz, V. (1992) El Genero Anastrepha Brasil 24, 631–634. Schiner (Diptera: Tephritidae) en México, Taxo- Lordello, L.G.E. (1952a) Insetos que vivem sobre o nomia, Distribucion y Sus Plantas Huespedes. maracujazeiro. I – Notas bionômicas acerca de Instituto de Ecología, Veracruz, 162 pp. Dione vanillae (L., 1758) (Lep.: Nymphalidae). Hoffmann, M. (1997) Polinização do maracujá Revista de Agricultura 29, 23–29. amarelo Passiflora edulis f. flavicarpa. In: Lordello, L.G.E. (1952b) Insetos que vivem São José, A.R.S., Bruckner, C.H., Manica, I. sobre o maracujazeiro. II – Contribuição ao and Hoffmann, M. (eds) Maracujá: Temas conhecimento de Cascoscelis famelica (F., 1787) Selecionados (1), Melhoramento, Morte (Col.: Chrysomelidae). Dusenia 3, 387–393. Prematura, Polinização e Taxonomia. Cinco Lordello, L.G.E. (1954) Insetos que vivem sobre Continentes, Porto Alegre, 5, pp. 58–70. maracujazeiro. III – Notas acerca de Dione juno Hoffmann, M. and Pereira, T.N.S. (1996) Polinização (Cramer) (Lep.: Nymphalidae) e relação de do maracujá-amarelo (Passiflora edulis f alguns outros insetos habitualmente coligidos

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