Jurnal Biosains, 17(1), 89–101, 2006

FOLIVOROUS INSECT FAUNA ON TWO BANANA CULTIVARS AND THEIR ASSOCIATION WITH NON-BANANA PLANTS Justin N Okolle*, Mashhor M and Abu Hassan A School of Biological Sciences, Universiti Sains Malaysia, 11800 USM, Pulau Pinang, Malaysia Abstrak: Persampelan serangga pemakan daun dan kerosakan akibatnya telah dijalankan di dua tapak tanaman baru, melibatkan kultur pisang tempatan biasa (Pisang Mas) dan kultur komersial (Cavendish). Pada kedua-dua tapak kajian, persampelan telah dijalankan setiap dua minggu bermula dari bulan pertama selepas penanaman sehingga tumbuhan mengeluarkan hasil pertama. Kehadiran serangga ini turut direkodkan pada tumbuhan lain dan rumpai yang terdapat di kawasan kajian. Lima spesies serangga pemakan daun daripada lima famili dan tiga order telah direkodkan pada kedua-dua kultur tanaman kajian. Belalang tempatan, Valanga nigricornis dan ulat beluncas, Spodoptera litura dikenal pasti sebagai spesies perintis. S. litura merupakan perosak utama Pisang Mas yang mengakibatkan 65.4% kematian tumbuhan berusia 1–2 bulan, sementara E. thrax pula merupakan ancaman utama Cavendish. Kupu-kupu pisang, E. thrax, didapati melengkapkan keseluruhan kitar hidupnya pada tumbuhan pisang yang bertindak sebagai perumah dengan serangga dewasa mendapatkan makanan daripada cecair dalam bunga tumbuhan tersebut. Hanya V. nigricornis dan Hypomeces squamosus dijumpai pada tumbuhan lain dan rumpai di sekeliling kawasan kajian. E. thrax tidak pernah dijumpai pada rumpai dan tumbuhan lain di kawasan kajian. Walau bagaimanapun, pada spesies Erionota lain, pemangsa serangga dan parasitoids kerap kali dijumpai pada Asystasia intrusa dan Ipomoea cairica. S. litura dan E. thrax merupakan serangga perosak utama tumbuhan pisang yang berusia 1–5 bulan. A. intrusa pula bertindak sebagai rumpai perumah yang penting untuk beberapa spesies semut, lebah dan Lepidoptera selain E. thrax. Abstract: Sampling of leaf-feeding insects and their damage were carried out on two newly planted fields of a common local banana cultivar (Pisang Mas) and a commercial cultivar (Cavendish). In both fields, sampling was done biweekly from the first month after planting till the first fruits emerged. The presence or absence of these insects was also recorded on non-banana crops and weeds. Five folivorous insect species belonging to five families from three orders were recorded on both banana cultivars. The Malaysian locust, Valanga nigricornis and the cluster caterpillar, Spodoptera litura were the first colonizers. Spodoptera litura was most damaging on Pisang Mas, causing 65.4% death of 1–2 month old plants, while Erionota thrax was most damaging on Cavendish. The banana skipper, E. thrax, was found to complete its entire life cycle on the banana host, with adults feeding on fluids in the flowers. Only V. nigricornis and the gold dust weevil, Hypomeces sqamosus, were found on non-banana crops and weeds around the field. Erionota thrax was never found on any of the weeds and non-banana crops while other Erionota species, insect predators and parasitoids were commonly found on Asystasia intrusa and Ipomoea cairica. Spodoptera litura and E. thrax are very important pests on young banana plants of 1–5 months old. Asystasia intrusa serves as an important weed host for several ants, wasps and lepidopterans other than E. thrax. Keywords: Colonization Dynamics, Banana Phenology, Folivorous Insects, Weeds

*Corresponding author: okollejustin@yahoo.com

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INTRODUCTION Growth stage of a plant can influence the number of insect species on it as well as the severity of damage. Most leaf-chewing insect pests particularly lepidopterans have been reported to prefer younger plants or younger plant parts (Wilson et al. 1982; Pencoe & Lynch 1982; Fowler & Lawton 1984; Overholt et al. 1994; Steinbauer et al. 1998; Smyth et al. 2003). Knowledge on the biology and ecology of different insect species feeding on a plant species is necessary, as it would help to record most serious and potential pests at the early and most vulnerable stages of a plant or crop. Such information is also very important in the timing of control measures.

Pisang Mas and Cavendish are very important banana cultivars locally and internationally, respectively. In commercial farms, tissue-cultured plantlets are the main planting material and these plants are kept in the nursery under greenhouse conditions for about seven weeks. They are then left out of the greenhouse to acclimate and become hardened for about one week before planting in the field. Once in the field, various agronomic and agricultural practices are carried out (e.g. fertilization, pruning, pesticide treatments, manuring and irrigation). From planting to fruiting takes about six to seven months while from fruiting to harvesting requires about three months. Although there are reports on several banana insect pests (Waterhouse & Norris 1989; Nakasone & Paull 1998; Gold et al. 2002), only caterpillars (lepidopterans) have been recorded as banana leaf-chewing insects. Haysom and Coulson (1998) emphasized that there is a need for more studies of variations in insect abundance and species richness on single host-plant species. In spite of the several reports of insect pests on bananas or Musa species, there are no reports on the association or interaction of these insects with non-banana crops or weeds within banana agroecosystems, and such interactions are important for the effective management of potential pests. Most insects do not reach pest status on crops because they are highly polyphagous and use most weeds as their host or food plant. However, the frequent and heavy use of herbicides in and around agroecosystems has a serious effect on weeds and this might in turn with time cause insects to switch, using the crop as a host or food plant. On the other hand, such a study might help in the identification of suitable non-banana crops or weeds that can be used as trap plants for pests or to enhance natural enemy activities.

The objective of this research was to study the folivorous insect fauna on two banana cultivars (Pisang Mas and Cavendish). The specific questions addressed by the research were: (i) what are the earliest colonizing insects on the leaves of newly planted bananas and do the populations of these insects change over time, i.e. in relation to banana phenology? (ii) Do the insects interact with non-banana crops or weeds within and around the banana farms? And if so, what type of interactions?

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Folivorous insert fauna on banana cultivars MATERIALS AND METHODS Sampling of Insects and Damage on Plants and Leaves Sampling of all insects feeding on banana leaves was carried out on two newly planted fields of a common local cultivar (Pisang Mas) and the most common commercial cultivar (Cavendish). The newly planted field for Pisang Mas was about 0.3 km away from a two-year old Cavendish plantation while the newly planted block for Cavendish was within the established Cavendish plantation. Tissue-cultured plants of Pisang Mas from the nursery were planted on June 2004 while those of Cavendish were planted on April 2005. In both fields, sampling was carried out at two weeks interval from the first month after planting till when the first fruits emerged. Plants that were one or two months old were less than 60 cm in height. In each field, and for each month, 100 plants were randomly selected and their leaves inspected thoroughly with the aid of a hand lens such that all leaf-eating insects (larvae or nymphs and adults) were counted in situ. For the banana skipper (Erionota thrax) and Spodoptera litura, only young larval stages (first and second instars) were counted to avoid counting the same insect twice. First and second instars of E. thrax and S. litura are shorter and smaller in size compared to the other instars. The bodies of first and second instars of E. thrax are not also covered by a white powder found on the older instars. Unfamiliar immatures and adults were taken to the laboratory, where immatures were reared till adults emerged and the adults kept in 70% alcohol for identification. Presence of adults of the three major parasitoids of E. thrax was also observed on the leaves. When plants were greater than 1.5 m in height, an adjustable ladder was used to inspect the leaves; and in the course of inspection, larger insects like grasshoppers that were seen on the leaves but flew away from the sampling plant were also recorded. Data from each sampling date per month were pooled and considered as the total for that particular month. Furthermore, a general observation was carried out to find out the feeding pattern of the insect species; and the nature of damage on the plants and leaves. Association of Insects with Non-banana Plants In both fields, most abundant non-banana crops including weeds within and around the fields were inspected throughout the study duration. Presence and/or absence of banana leaf-eating insects, as well as insect predators and parasitoids on these non-banana plants were recorded. To get a major weeds in the fields, 300 randomly selected points within the Cavendish plantation were marked. A 1 m2 quadrat was then used to record the percentage covers by the weeds in all the marked points and this measurement was done once a month for three consecutive months. Identification of the Insects and Weeds Identification of the insects was done by using a pictorial guide, morphological and biological descriptions of insect pests in Malaysia by Khoo et al. (1991). Banana skipper adults emerging from pupae were carefully observed using a hand lens and a light microscope. With the aids of reports of Christie et al.

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(1989), and identification key and pictorial guide by Fleming (1983) and Corbet and Pendlebury (1992), the adult skippers were identified to species. The weeds were identified using pictorial guides and notes by Shiew and Hong (1985), Terry and Michieka (1987), Zimdahl et al. (1989), and Barnes and Chan (1990). Relevant websites were also consulted to confirm identification of these insects and weeds. RESULTS Species and Damage of the Insects The different insect species feeding on the leaves of the banana plants and their status as pest based on the degree or level of damage is shown in Table 1. With the exception of the whitefly (Aleurodicus dispersus Russel), all insect species recorded on Cavendish plants were the same species found on Pisang Mas (total of four species for Pisang Mas and five for Cavendish) and the insects belonged to four orders and five families. Table 1: Leaf-eating insect species on two banana cultivars (Pisang Mas and Cavendish) in Synergy Farm, Pulau Pinang, Malaysia.

Order Family Species Common name Damage

Lepidoptera Noctuidae Spodoptera litura Cluster caterpillar Very serious Lepidoptera Hesperiidae Erionota thrax Banana skipper Not very

serious Orthoptera Acrididae Valanga

nigricornis Malaysian locust Not

significant Coleoptera Curculionidae Hypomeces

squamosus Gold dust weevil Not

significant Homoptera Aleyrodidae Aleurodicus

dispersus* White fly Not

significant

* The only species found on Cavendish but not found on Pisang Mas.

Eggs of S. litura were laid on the undersurface of leaves and young larvae hatching from these eggs fed in groups. Feeding resulted in skeletonization of the leaves, which eventually became brownish. As the larvae mature, various mortality agents kill many while the few survivors move to the growing or vegetative regions of the plants. In these regions, they feed and create tunnels that consequently kill the plants or retard their growth, and the larger larvae then move to the soil to pupate.

Adult of E. thrax laid their eggs either singly or in batches on the under or upper leaf surfaces. Young instars hatching from the eggs move to the margin of the leaves, feed and construct smaller shelters (leaf-rolls). As they become mature, they move to other non-infested leaves, where they continue feeding and construct larger leaf-rolls. Two or three mature larvae could defoliate an entire banana leaf while a single mature larva was capable of rolling a banana leaf up to one meter. Mature larvae fed very little at all times but spent most of the time

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Folivorous insert fauna on banana cultivars constructing and sealing their leaf-rolls that subsequently become yellowish and then brownish. Larvae transformed to pupae within tightly sealed leaf-rolls and adults that emerged from these pupae start visiting the flowers of the banana plants.

In the case of Valanga nigricornis, nymphs and adults damaged leaves by chewing young and older leaves; and like E. thrax, did not feed much and adults laid their eggs in loam soil around the edges of the field. On the other hand, adults of Hypomeces squamosus fed mostly on younger leaves and; like V. nigricornis and E. thrax, they too did not feed much and A. dispersus was found only on the underside of Cavendish leaves. Damage on the leaves was insignificant and their feeding (small brown spots) was slightly visible only when they were densely populated and aggregated on the same spot.

Of all the leaf-eating insects found on both banana cultivars, the most serious in terms of degree of damage were S. litura on Pisang Mas and E. thrax on Cavendish. Of a total of 720 Pisang Mas and Cavendish plants monitored from planting to four months after planting, more than 50% of Pisang Mas plants died as a result of S. litura infestation and no Cavendish plant died as a result of any of these insects (Table 2). Infestation of S. litura (> 180larvae/100 plants) on Pisang Mas was higher than that on Cavendish (Fig. 1).

Table 2: Infestation and effects of S. litura on young banana plants.

Pisang Mas Cavendish

Number of plants sampled 720 720 Percentage of plants infested 471/720 = 65.4% 20/720 = 2.8% Percentage of dead plants from infestation 288/471 = 61.2% 0/20 = 0%

Colonization Dynamics of the Folivorous Insects On Pisang Mas, V. nigricornis and S. litura were the first colonizers appearing one month after planting, while E. thrax and H. squamosus only appeared four months after planting (Fig. 1). Peaks of S. litura density were recorded in the first two months after planting, dropping thereafter and disappearing in the 7th and 8th months after planting. Density of V. nigricornis remained constant from planting till fruiting, and was never more than 50/100 plants. E. thrax density on the other hand peaked in the 5th and 6th months after planting and dropped slightly thereafter. H. squamosus also peaked in the 6th month after planting but disappeared from the 5th month onward. With the exception of S. litura whose density peaked at 189/100 plants, densities of the other insects were at no time greater than 50/100 plants. The total number of insect species increased as the banana plants matured, with highest number of species recorded in the 4th, 5th and 6th months after planting (Fig. 2).

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Like the situation on Pisang Mas, V. nigricornis and S. litura were also he first colonizers on Cavendish plants; appearing on the 2nd month after lanting while E. thrax, H. squamosus and A. dispersus only appeared by the 3th onth after planting (Fig. 3). All the other insects except V. nigricornis and H.

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Folivorous insert fauna on banana cultivars squamosus showed variable fluctuations in densities, and only densities of V. nigricornis and H. squamosus were never greater than 30/100 plants. S. litura with maximum density less than 80/100 plants appeared in the 2nd month after planting, disappeared and reappeared only in the 7th month and again disappeared in the 8th month after planting. Highest peak of E. thrax density was recorded in the 5th month (129/100 plant) with a smaller peak in the 7th month after planting. A. dispersus density on the other hand peaked in the 4th month, dropped sharply and only increased again in the 7th and 8th months. Total number of insect species peaked in the 3th, 4th and 7th months (Fig. 4), with the younger plants (1–2 months old) containing relatively lower number of insect species. 160 Spodoptera litura

Erionota thrax Valanga nigricornis Hypomeces squamosus Aleurodicus dispersus

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Figure 4: Changes in the total number of folivorous insect species on different growth stages of Cavendish bananas from one month after planting to eight months after planting. Interactions of the Insects with Non-banana Plants Of the five species of banana folivorous insects recorded, only V. nigricornis and H. squamosus were found on non-banana crops and weeds (Table 3). Although these two insects where found on Elaeis guineensis (oil palm) and Psidium guajava (guava) respectively, they were never found on weeds. Both insects fed on the leaves and also spend some time mating on the plants. Although E. thrax was never found on any of the non-banana crops or weeds, other Erionota species and butterflies were commonly found on Asystasia intrusa, Ipomoea cairica, Mimosa pudica and Cloeme rutidesperma. Adults of these insects fed on the nectar of the flowers of these weeds while their larvae fed on the leaves and construct leaf rolls or shelters; and of these four weeds, A. intrusa was the most frequently visited by the insects.

Apart from these leaf-eating insects, some predators and parasitoids were often found on the non-banana plants or weeds. An unidentified species of red ants was found on all the weeds while ladybird beetles and the pupal parasitoid Brachymeria albotibialis of E. thrax were present only on P. guajava and Digitaria ciliaris. The red ants visited these non-banana plants or weeds to get nectar from the flowers, collect honeydew from aphids if present and or feed on larvae of the butterflies. On the other hand, ladybird beetles were always found feeding on aphids, as well as mating and laying their eggs; while B. albotibialis frequently visited and rests on leaves of P. guajava. For all the non-banana plants or weeds, highest numbers of insect species were recorded on P. guajava (total of five species) and D. ciliaris (total of three species) (Table 3).

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Table 3: Association of banana leaf-eating insects with non-banana crops or weeds in Synergy Farm Sdn. Bhd., Penang, Malaysia.

Insects Non-banana plants and weeds Red

ants* Other

Erionota species

Ladybirds* Aphids Brachymeria albotibialis**

Valanga nigricornis

Hypomyces squamosus

Spodoptera litura

Erionota thrax

Aleurodicus dispersus

Psidium guajava# + - + + + - + - - -

Digitaria ciliaris +

- + + - - - - - -

Asystacia intrusa + + - - - - - - - -

Ipomoea cairica + + - - - - - - - -

Mimosa pudica + + - - - - - - - -

Cloeme rutidesperma

+ + - - - - - - - -

Borreria laevicaulis + - - - - - - - - -

Elaeis guineensis# + - - - - + - - - -

Emilia sonchifolia - - - - - - - - - -

* Insect predators. ** Parasitoid of E. thrax pupae. # Non-weedy species. + Presence of insect on non-banana plant. – Absence of insects on non-banana plants.

Folivorous insert fauna on banana cultivars

DISCUSSION Out of the four insect orders recorded on the banana leaves (Table 1), lepidopterans were the most damaging. S. litura was most damaging on young Pisang Mas plants (1–2 months after planting) while E. thrax was most damaging on Cavendish plants of 3–6 months old. S. litura is most damaging because mature instars feed on the growing regions, causing the young plants to die. Another reason why S. litura infestation and damage is higher on plants 1–2 months after planting is because these plants are shorter and nearer to the ground. Since S. litura pupates in the soil, it invariably prefers these shorter plants so that it can easily move to the soil to pupate. S. litura has been reported on vegetables such as cabbages that are also very close to the soil (Khoo et al. 1991). Although no plant death was recorded as a result of E. thrax infestation, growth and yield of bananas can be seriously impaired due to the substantial defoliation as a result of leaf rolling (Waterhouse et al. 1989). Complete defoliation of an entire banana farm has also been reported (Khoo et al. 1991).

According to Van Nouhuys and Hanski (2002), colonization is more likely if the nearby source populations are large. Following this hypothesis, E. thrax was expected to be the first colonizer since the newly planted fields (especially Cavendish) were close to an established Cavendish plantation with relatively higher populations of E. thrax. Contrary to expectations, V. nigricornis and S. litura were the first colonizers on the newly planted fields. This is an indication that different insect species prefer different growth stages of a plant or have different abilities to perceive cues and therefore locate patches of their host or food plants. Of all the folivorous insects recorded, only V. nigricornis and H. squamosus did not show variable fluctuations in densities and this may be a possible reason why damage from these two insects was not significant on bananas. Schowalter (2000) referred to such populations as being stable; while populations of variable fluctuations (e.g. those of E. thrax and S. litura) as irruptive and therefore capable of causing serious damage.

In addition, V. nigricornis and H. squamosus were the only leaf-eating insects recorded on non-banana crops (oil palm and guava) although they were never found on the weeds. However, infestation of H. squamosus was very serious on young guava plants and Khoo et al. (1991) have also reported this. Khoo et al. (1991) also described V. nigricornis as highly polyphagous, a pest of oil palm that prefers leguminous weeds; however, this study did not record V. nigricornis on any of the weeds. This might be due to the absence of broad-leaf leguminous cover crops in the banana fields.

Although E. thrax was never found on the weeds, other Erionota species and predators or parasitoids were recorded on the weed species (Table 3). Aphids were also observed on most of the weeds and the non-banana crops where predators or parasitoids where found. It is therefore likely that these weeds somehow rendered the banana plants protection from potential pests such as aphids and Erionota species. Eradication of these weeds using herbicides might in the long-term force these potential pests to divert their feeding activities on bananas. Although weeds affect the growth and yield of bananas, those which are used as host or food plants by these potential pests could be maintained or

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Folivorous insert fauna on banana cultivars planted at the field edges in order to serve as trap plants and conserve natural enemies. Price (1983) mentioned that honeydews from homopteran such as aphids are important food for a variety of entomophagous species while many parasitoid species subsists on resources such as plant nectar, pollen, and secretions from scales and aphids (Menalled et al. 2003).

Presence of B. albotibialis in the newly planted fields before colonization of E. thrax shows the quick dispersal ability of this parasitoid. It also shows the ability of this parasitoid to easily detect banana farms and hence their host, E. thrax. Again, this is an indication that the banana plants have certain chemical cues that help to attract the parasitoids. Van Nouhuys and Hanski (2002) reported that the early presence of parasitoids in newly established patches is an indication that a host butterfly cannot escape parasitism by dispersal.

Among all the banana leaf-eating insects in this study, only E. thrax utilized the banana as a host plant, i.e. lives on the plant and conducts all its activities on it. It is also the only insect that has been recorded with a very narrow host range (Khoo et al. 1991; Gold et al. 2002). Based on these, any attempt such as pressure from frequent and injudicious use of insecticides to eliminate E. thrax is likely to force this pest to develop resistance to the chemicals. Insecticide resistance has been noted as one of the worst and most common ecological backlashes in insect pest management (National Academy of Science 1971; Graves et al. 1999; Pedigo 1999; Norris et al. 2003).

In conclusion, five leaf-eating insect species from four orders and five families were recorded on banana. On Pisang Mas and Cavendish, V. nigricornis and S. litura were the first colonizers. V. nigricornis and H. squamosus did not show variable fluctuations in densities, while S. litura and E. thrax showed variable fluctuations and were the most damaging on Pisang Mas and Cavendish respectively. Infestation of S. litura was higher on plants 1–2 months after planting but infestation of E. thrax was highest on plants 3–6 months after planting. V. nigricornis and H. squamosus were the only banana folivorous insects recorded on non-banana crops or weeds. Other Erionota species, aphids as well as insect predators and parasitoids were also recorded on the non-banana crops or weeds. Immatures of the Erionota species fed on the leaves of the weeds and construct leaf-rolls for shelter while the adults fed on the nectar of the flowers.

ACKNOWLEDGEMENT The management of Synergy Farm Sdn. Bhd., Pulau Pinang, Malaysia for permission to carry out the research in the banana plantations.

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