Pests

Major and minor insect pests attacking annonas are described by numerous authors (Melo et al., 1983; George et al., 1987; Bustillo and Peña, 1992;

Oliveira et al., 1992; Torres and Sánchez, 1992; Agustín and Alviter, 1996;

Junqueira et al., 1996; Pinto and Silva, 1994; Nakasone and Paull, 1998;

Nava-Díaz et al., 2000) in many countries and ecological regions (Table 10-13) with different levels of economic damage and cost of management control.

Table 10-13. Major and selected minor insect pests of Annona species

Common Name Specific Name Affected Plant Parts

Country/Region Major Insect Pests

Annona moth Cerconota anonella Seeds and fruits Universal Cherimoya seed

borer

Talponia batesi Seeds and fruits Mexico, Peru, Spain Atis moth borer Anonaepestis bengalella Fruits Philippines Wasps (wasp) Bephratelloides

maculicollis and B. cubensis

Seeds and fruits Several countries/regions Borers (trunk

borer) Cratosomus bombina, Heilipus catagraphus

Trunk and branches, base of the trunk

Mexico, Brazil

Flies (fruit flies) Anastrepha obliqua, A. ludens, Ceratitis capitata, Bactrocera dorsalis and B. tryoni

Fruits Peru, Mexico.

Colombia, Ecuador, Spain, Peru, Australia, New Zealand Mealy bugs Planacoccus citri,

Dysmicoccus spp., Ferrisia virgata,

P. pacificus (India)

Fruits and leaves

Several countries/regions

Scale insects Several genera and species Leavesand

stems Several countries/regions Spider mites Several genera and species Leaves and

flowers Several countries/regions Minor insect pests

Leaf hopper Empoasca fabae, Membracis foliata, Aethalion spp.

Leaves and stems

Brazil, Colombia, Venezuela, American tropics

Thecla moths Oenomaus ortygnus Flowers and fruits

American tropics, Brazil

Aphids Aphis gossypii and Toxoptera aurantii

Leaves and shoots

USA, Colombia, Peru, Brazil and Venezuela Hemipterous

insects

Leptoglossus zonatus and Antiteuchus tripterus Fruit spotting

bug

Amblypelta nitida Young fruits Australia Leaf larvae Several genera and species Leaves and

stems

American tropics, Brazil

Leaf miners Leucoptera spp. and Leaves Cuba and Ecuador

Chapter 10. Agronomy

Common Name Specific Name Affected Plant Parts

Country/Region Phyllocnistis spp.

Root grubs Anomala Roots Philippines Ants ("saúvas") Atta spp. and Acromyrmex

spp. Leaves and

petioles Universal

There are three important groups of borer insects attacking annona species:

the trunk borer, the fruit borer and the seed borer. Trunk borers are coleopterons, generally weevils, and three species are the most common:

Cratosomus bombina bombina (Plate 6), Euripages pennatus and Heillipus catagraphus (Oliveira et al., 1992). These insects are 2-4 cm long and they perforate the trunk, causing plant decline and finally death. The external symptom of the attack is a black oxidized sap exudation from the small holes where the insects entered the trunk. Injection of liquid pesticides, such as D-aletrina and D-tetrametrina into the trunk holes is an effective method of control (Oliveira et al., 2001). In the Brazilian Cerrados brushing of the tree trunk with a 1% solution of a pesticide, commercially named Creolina, together with lime at 10%, has prevented fruit borer attack on soursop.

The annona moth (Cerconota annonella), commonly known as the 'fruit borer', is the most important of the insect pests attacking Annona species (Plate 5). Although it is known as the soursop moth in many areas, it has been recorded attacking and damaging fruits of several other annonas as well, including sugar apple and custard apple (Coronel, 1994; Oliveira et al., 1992;

Torres and Sánchez, 1992), but has not been reported on cherimoya fruits (Bustillo and Peña, 1992). The soursop fruit borer moth has a life cycle from egg to adult emergence averaging 36 days. The adult moth is attracted to black-light traps, which is an important method for monitoring this insect pest (Bustillo and Peña, 1992). The removal of rotted and damaged fruits from the ground is also an important cultural control method. Bagging the fruits with chemically treated bags (a common type is the chlorpyriphos bag) can keep 92% of the fruits totally undamaged before harvesting (Bustillo and Peña, 1992). Biological control using two braconids, which parasitize larvae of C. annonella, has been successful in Colombia and Ecuador (Bustillo and Peña, 1992). In the Cerrado ecosystem of central Brazil, the soursop ecotype Morada is less susceptible to the attack of the soursop moth than any other ecotypes (Junqueira et al., 1996; Pinto and Silva, 1996), suggesting that appropriate cultivar selection can help to minimize the problem. Chemical control with triclorphon or fenthion at 0.1%, every 15 days can help to control this pest. Spraying should be directed at the fruits and started when they are still small (Torres and Sánchez, 1992)

The moth Anonaepestis bengalella is cited as the most destructive pest of sugar apple fruit in the Philippines (George and Nissen, 1992; Coronel, 1994). Another moth Oemanus ortygnus, which is widespread throughout the Caribbean region and the American tropics is considered a minor pest (Nakasone and Paull, 1998) and attacks the flowers instead of the fruits. In addition to the natural control methods described above for the annona moth, the removal of damaged and attacked fruits from the ground or even from the plant, followed by burial in holes at least 50 cm deep, would be a very effective cultural practice. The same chemical control can also be used for both species.

The soursop wasp (Bephratelloides maculicollis or B. cubensis, Hymenoptera), also called the annona seed borer (plate 5), is the second most important insect pest. Similarly Talponia batesi (Lepidoptera) also attacks cherimoya seed in Mexico (Nava-Díaz et al., 2000). All other cultural practices for control of Cerconota anonella can be used for Bephratelloides spp. and Talponia batesi, except for the use of black-light traps, which are ineffective with these species. Chemical control with decamethrin 0.05%

every 15 days when the fruits are still small (Torres and Sánchez, 1992;

Junqueira et al., 1996) can reduce infestation.

Several genera of fruit fly, Anastrepha, Ceratitis and Bactrocera are frequently mentioned (George et al., 1987; Peña and Bennet, 1995; Rebollar-Alviter et al., 1997; Alvarez et al., 1999; Farré et al., 1999) as important insect pests attacking annona fruits in many countries and regions (Table 10-13), especially on cherimoya fruits. The infestation occurs with the deposition of the eggs by the adult on the fruit skin or through the stem cavity (George et al., 1987). By making galleries in the pulp, the larvae completely destroy the fruit. The larva starts its pupation phase outside the dropped fruit, underground (about 10 cm deep in the soil), from where the adults emerge and start a new cycle. The cycle of the fruit fly from egg to adult is completed in about 30 days (Nascimento et al., 2000).

According to Farré et al. (1999), an incidence of fruit fly attack is generally due to favourable climatic conditions, high reproductive potential, alimentary adaptability and in some circumstances absence of natural enemies, which makes them a difficult pest to control. The size of the area under cultivation and economic importance of the crop can also add to the impact of an attack and the importance of the pest. In Spain, which is one of the most important cherimoya producers, the Mediterranean fruit fly (Ceratitis capitata) has a major economic impact, attacking up to 50% of cherimoya fruits (Farré et al., 1999), while in Ecuador the incidence of cherimoya fruit fly (Anastrepha spp.) is greater than 94% (Alvarez et al., 1999). However, in Brazil, a typically tropical country with very small areas producing cherimoya, the

Chapter 10. Agronomy incidence of fruit flies on this species, or even on its hybrid atemoya, is not mentioned in the literature (Kavati et al., 1997; Bonaventure, 1999). Also, the incidence of fruit flies on soursop, sugar apple and custard apple fruits is negligible or without economic importance, since there is no citation in the literature reviewed (Torres and Sánchez, 1992; Junqueira et al., 1996; Pinto and Silva, 1994; Kavati and Piza Jr., 1997). The only exception occurs in Mexico, where the attack of Anastrepha ludens on soursop is cited by Rebollar-Alviter (1987), describing the work of Ponce and Vidal (1981). It is not clear why fruit flies are only minor annona pests in this area, because the flies attack other fruit species in the same areas where annonas are grown.

The mining character of fruit fly larvae, together with their underground pupation, has led practically all control methods to be directed at the adults, by using insecticides (Farré et al., 1999). The spraying of insecticide on entire plants is still the most common practice. Distribution of a toxic bait, consisting of 4% hydrolyzed protein and 0.15% dimethoate, on the entire tree or over the top third only, has also been used (Fuentes et al., 1999) to control Mediterranean fly (Ceratitis capitata) on cherimoya fruits. However, besides having questionable effectiveness, this method is also questioned by an increasingly environmentally sensitive society.

An integrated control system involving chemical, biological and cultural methods should be implemented for management and control of the fruit fly.

For instance, in Spain, Farré et al. (1999), describing work of Hermoso et al.

(1994) in the Experimental Station of La Mayora, affirmed that phosphate baits or pheromone traps, combined with field hygiene (removal of fruits on the ground), can reduce fruit fly attacks to 4 - 7% without any insecticide treatment. This percentage of fruit fly attack can be further reduced (to 0.5 - 2.0%) with immersion of cherimoya fruits in hot water (between 45 and 47°C) for 60 minutes. Similarly, Rebollar-Alviter et al. (1997) suggest that control involving only the removal of dropped over-ripened fruit on the ground can reduce fruit fly populations by up to 80%. Fruit bagging also provides an adequate protection against attack (Nakasone and Paull, 1998).

After the removal of the fruit, a cultural practice commonly used in mango orchards in north-eastern Brazil, harrowing beneath the canopy, i.e. turning over the first soil layer, impedes pupation of fruit flies and interrupts their life cycle. Given the importance of these pests in many areas, it is curious that more complete integrated pest management systems have not been reported.

In Mexico, the insects Biosteres longicaudatus and Aceratoneuromyia indica have been used for biological control of Annona fruit flies (Rebollar-Alviter et al., 1997). The use of chemical compounds from seeds or leaves of Annona trees, such as wild soursop and sugar apple, have also been tested with some success against fruit flies. Extracts from an infusion of 5% (dry

weight) in water of sugar apple leaves can kill up to 70% of adult fruit flies when ingested in the laboratory (Catarino and Ezequiel, 1999) - see Chapter 6 on the chemical properties of Annona species.

Mealy bugs, various species of scales or cochineals and spider mites attack the stems, leaves, flowers and fruits of Annona species in numerous countries and regions (Table 10-13). They are all considered to be sucking insect pests and may be considered as economically important, due to their impact when they suck the sap of the young vegetative parts and fruits of annona trees. An orchard monitoring system is necessary to detect the phenological phase in which the attack is occurring at an economic level, so as to make control more effective. Mealy bugs are reported to be a major pest on marketable fruits in some areas of Australia and red spider mites can become a serious problem when attacking growing annona trees in dry areas (Nakasone and Paull, 1998). In Colombian and Brazilian soursop orchards, these insect pests have been controlled with mineral oil and systemic insecticides (dimethoate) (Torres and Sánchez, 1992; Junqueira et al., 1996). It is recommended that mites be controlled by spraying specific insecticides (propargite) which can kill the eggs and the adult insects. The insecticide and water mixture needs to be used with an adherent. The mealy bug Planococcus citri is biologically controlled by its predator Cryptolaemus montrouzieri, however, the predator's action is hindered when there is a large population of the Argentinean ant, Iridomyrmex humilis (Farré et al., 1999). Control of mealy bug should focus on biological control where possible, or the use of mineral oil.

Some minor insect pests also have significant economic importance in some regions. Aphids can transmit serious viral diseases to annona trees, while attacks of aphids and hemipterous bugs on fruits can promote irreversible damage to their quality for market. These insect pests are controlled by spraying with the pesticides malathion or parathion (Torres and Sánchez, 1992; Junqueira et al., 1996). Aphids and bugs attacking soursop trees have been controlled efficiently in the Brazilian Cerrados by spraying a 20%

solution of macerated leaves of the Neem (Azadirachta indica) tree. The fruit-spotting bug (Amblyphelta nitida) is considered a serious annona pest in Australia and its damage resembles the symptoms of black canker or diplodia rot (Nakasone and Paull, 1998). Where possible, if damage is limited, chemical use should be avoided.