Pest-potential organisms on Begoniaceae collection of Eka Karya Bali Botanic Garden

Begonia thrives in shady plantations but can tolerate more sun if the soil moisture is maintained. Therefore, the collection of begonia in Eka Karya Bali Botanic Gardens (BBG) is planted in a greenhouse. This increases the potential damage due to pest attacks. The purpose of this study was to identify the pest-potential organisms on begonia. The research was carried out in April–June 2019 at Begonia Park of BBG using survey methods to identify potential organisms and their damage symptoms. We found three species of insects that attack begonia collection, i.e. Spodoptera litura (Lepidoptera: Noctuidae), Aleurodicus destructor and Bemisia tabaci (Hemiptera: Aleyrodidae), and two species of Gastropods namely Parmarion martensi (Gastropoda: Ariophantidae) and Bradybaena similaris (Gastropoda: Bradybaenidae). This result could be utilized as a reference to determine the pest-controlling technique on Begoniaceae.


Introduction
Charles Plumier, a clergyman who was also a botanist, introduced begonia in 1690.Begonia was named after his colleague, botanist and Governor of France, Michel Begon [1,2].Various begonia plants (Begoniaceae) have been widely used as attractive plants in numerous Indonesian locations, particularly West Java and Bali.Begonias are a popular ornamental plant because their blooms and leaves come in various shapes, patterns, and colors, and they are easy to grow and bloom.Begonias can be grown both vegetatively and generatively.Some begonias can even develop tubers that can tolerate harsh temperatures [2].
In contrast to other ornamental plants, what makes begonia unique is its asymmetrical leaves.The leaves of begonias are glossy green to reddish brown with various shapes and sizes, scattered leaves, oval to elongated in shape, and have protective leaves that fall off easily [1,3,4].Begonia are erect herbaceous plants, shrubs, or creepers found throughout the world's tropics and subtropical regions [2].Begonia thrives in moist, well-drained soil rich in organic matter.Begonia prefers partially shaded planting areas but can tolerate more sun if soil moisture is maintained.Therefore, the collection of Begoniaceae at the Eka Karya Bali Botanical Garden (BBG) is planted in a greenhouse.
Because it is planted with the same family in the same area, pest attack is a serious problem that needs attention.According to [5], potential pests on begonia include aphids, mealybugs, naked snails, and leaf miners.This statement is supported by the results of [6] which reported pests that attack begonia collections at Cibodas Botanical Garden are naked snails, mealybugs, aphids, ground snails, caterpillars, and shield lice.The attacks of these pests cause damage to the leaves, thereby reducing the aesthetic value of begonia [7,8].Previous research reported that Begoniaceae had become a new host for Gastrophysa viridula (Coleoptera) [9].In addition, the presence of Bradysia spp., commonly known as fungus gnats on begonias, must be watched because these species can spread Fusarium and other pathogens [10].
As a plant conservation site, the identification of pests that attack plant collection at BBG cannot be separated from plant conservation efforts.Thus, this research aims to identify the pest-potential insects on Begoniaceae of BBG.Pest inventory and identification can be used as a first step to determine the appropriate pest control methods that must be carried out to maintain the integrity and beauty of the collection without ignoring the effects on the environment and visitors.

Methods
The study was conducted from April to June 2019 at the Begonia Park of BBG from 08.00 a.m. to 03.00 p.m. BBG is located in Candikuning Village, Bedugul District, Tabanan Regency, Bali, at 1250-1450 m above sea level.This study was conducted at an average daily temperature of 21-22°C and 80-90% relative humidity (RH).
The observations were made on all begonia plants collection of BBG.The parameters observed were the form of damage/symptoms attack and the types of organisms that have the potential as pests.The symptom attack from several plant organs was recorded and documented for further comparison with the literature.
Insects that cause damage to begonia plants collection were taken using tweezers, put in a plastic, and then identified in the Laboratory of Applied Botany, BBG.Insects found were identified through a literature study.

Results and Discussion
The results showed five organisms had the potential to become pests.Three of those species were insects included in Lepidoptera and Hemiptera, while the other two were non-insect species found in the Gastropods (Table 1).Parmarion martensi Gastropods Slug/semi-slug snail

Spodoptera litura
Spodoptera litura (Lepidoptera: Noctuidae) lays its eggs on the underside of the leaves [11].About 960 eggs were laid at 30°C and 90% RH, while only 145 eggs were laid at 35°C and 30% RH.Eggs hatch in 3-4 days in warm conditions and 12 days in cooler conditions [12,13].
The larvae of this species go through 6 instars for 12-15 days and hide in the soil to rest.The population explosion with the most serious damage occurred when the larvae matured and survived for 6-7 days.Newly hatched larvae eat leaves in groups, then spread using threads that come out of their mouths and move to other plants [12].Adult larvae are blackish-green or brownish-grey with a yellow stripe on the back and grey on the sides of the abdomen [11,12].These characteristics correspond to the individual larvae found in the begonia collection at BBG.The larvae found were 6 cm in size, brown with blackish-brown vertical stripes on the back, and grey on the sides of the abdomen.Along the larvae's back is also a semicircular yellow pattern (Figure 1).
Their pupae are formed in the soil and last for 7-11 days [12,13].The imago is a moth that survives for 8-10 days, is active at night and can fly 1.5 km in 4 hours.Wind can help moth activity and spread further [12].
The life phase of S. litura which has the potential to become a pest is the larva which is better known as the armyworm.The armyworm has a chewing-biting mouth type, it generally attacks leaves but can also cut the stems.Symptoms of leaf damage start from the edges.The edges of the leaves are damaged and torn.At high attacks, armyworms can devour leaves until the plants are bare [11,13].Similar symptoms were also found on begonia leaves attacked by armyworms (Figure 1).This species has been widely reported for its attacks on various agricultural commodities such as chili, cabbage, rice, corn, tomatoes, tobacco, eggplant, beans, soybeans, and peanuts which can cause yield losses of up to 80% [14,15,16].Several studies have reported life tables of S. litura which contain basic data on the population dynamics of various host plants [17,18,19].The life table is useful for determining the weakest moment of a pest's life cycle so that it can increase the potential for successful pest control.

Aleurodicus destructor and Bemisia tabaci
Other insects found in the begonia collection of BBG were Aleurodicus destructor and Bemisia tabaci.These two insects come from the same ordo (Hemiptera) and family (Aleyrodidae).They have several local names including whitefly and mealybug.The naming of whiteflies is based on the unique morphological characteristics that exist in A. destructor, which has a thick white waxy layer in the middle of the back and a thinner waxy layer on the edges of its body that looks like lumps.This insect is also known as coconut whitefly because it often attacks coconut plants [20].The whitefly is a small insect pest with a piercing-sucking mouth type, usually found on the underside of leaves.Eggs are laid in a circular or semicircular pattern [21].Nymphs are yellowish-white, emerge in 5-7 days, are flattened ovals, move short distances before flattening themselves with leaves to feed, and secrete a shiny white sweet liquid [13,21].The whitefly nymph phase found in the begonia collection at BBG showed an  attack symptom in the form of the appearance of fluid that coalesces resembling dangling hairs on the lower surface of the leaves, has a smooth and sticky texture, and is shiny white (Figure 2a).The imago looks like a little moth with white wax powder covering its body and wings, and it instantly takes flight when the leaves are agitated.
Under favorable conditions, one generation of whiteflies takes 3-4 weeks.Females can lay 400 eggs at a time [21].The presence of whiteflies is triggered by high humidity before and at the end of the rainy season with humidity above 80% with daily temperature fluctuations of 21-27°C [13].
In general, A. destructor and B. tabaci have the same morphology and bioecology.The difference between the two is the color of the imago.The imago of A. destructor found in the begonia collection at BBG was white with greyish-black spots on the wings (Figure 2b).Meanwhile, the imago of B. tabaci found was yellowish white with a yellow head.B. tabaci is classified as a polyphagous pest and a vector for viruses that cause disease in various agricultural horticultural commodities.These insects obtain their nutrition by sucking the phloem sap of their host.B. tabaci secretes honeydew onto the surface of leaves or fruit and transmits the disease virus to its host.Honeydew excretion by B. tabaci stimulates the growth of fungi that cause powdery mildew disease in plants [22].This is worth paying attention to as [23] previously reported the powdery mildew disease incidence on begonia collection at BBG.
Whiteflies in small numbers do not cause significant damage unless they act as virus vectors.Their attack is characterized by the presence of a sticky liquid with a white circular pattern and white fly crowds on the lower surface of the leaves [13].Symptoms of this attack were also found in begonias in BBG as shown in Fig. 2c.Heavy attacks cause a decrease in plant vigor, wilt, stunt, leaves turn yellow, and fall.Whiteflies secrete sticky white wax, thereby reducing the aesthetics of plants and allowing pathogenic fungi to attach more easily to leaves [13].

Parmarion martensi and Bradybaena similaris
Apart from the three species of insects mentioned above, other organisms found in the begonia collection of BBG which have the potential to become pests are slugs from the Gastropod class.Eggs or young snails are often carried in fresh or dried plants.Once settled, snails actively move in search of food, especially at dusk.Its imago can survive drought for more than 6 months [13].Parmarion martensi has a reduced shell, which is more like a mantle, forming a ridge on the back, covering from the head to half of the body.Therefore, P. martensi is often referred to as slug or semislug.The shell of P. martensi is brownish yellow, transparent, thin shiny, and shaped like nails [24].As shown in Fig. 3a, the P. martensi found in the begonia collection of BBG was golden brown, 4 cm in size, without a shell, but had a bulge on its back.This is supported by the research results of [24,25] which stated that the body length of P. martensi reaches 3-5 cm, is yellowish brown or greyish brown, and dark brown on the back of the body.In addition, the snail's body has two black parallel lateral lines extending from the base of the antenna on the head to the rear end of the body [24,25].
Slug snail mainly attacks young leaves because they have a soft texture, but can also attack stems, flowers, and fruit [26].Apart from ornamental plants, P. martensi as a polyphagous pest is also capable of attacking various types of plants such as the Cucurbitaceae, Brassicaceae, Asteraceae, and Araceae [27].P. martensi is also reported as the obligate host of Angiostrongylus cantonensis which causes eosinophilic meningitis in humans [28].
Bradibaena similaris is known as a tramp snail because it is often found in shrubs at an altitude of 1800 meters above sea level which stores a lot of organic matter around it [29].It is a small to mediumsized snail (up to 15 mm in diameter), polyphagous, attacks a wide range of plant species, and can be very dangerous to ornamental plants.The shell is round and convex, yellow-brown, with 5 to 6 circular grooves [30,31].B. similaris found in the begonia collection of BBG was also small (±1 cm in diameter), brownish yellow, with 5 circular grooves (Figure 3b).Based on its life cycle, B. similaris is grouped into r-strategist species [32].This shows that the tramp snail population is regulated by its biotic potential.Previously, [33] stated that B. similaris had a wide distribution status on the island of Sumatra.
Slug snails and tramp snails are nocturnal animals, but can also carry out activities during the day when the weather is foggy, after rain, after irrigation, or when environmental conditions are damp.After eating, the snails will hide among the weeds or burrow into the ground [26].Therefore, P. martensi and B. similaris are often found in begonia collections of BBG during the day because they are supported by foggy weather and humid environmental conditions.Gastropod pest attack symptoms are generally preceded by slime marks appearing shiny on the leaves.Furthermore, there are holes and tear marks of irregular shape and size in the roots, leaves, and flowers [13].Similar symptoms were also found in begonias attacked by P. martensi and B. similaris (Fig. 3b, c).
Our research shows that not only insects act as potential pests on begonia, but also gastropods.Previously, [5] found aphids, mealybugs, slug snails, and leaf miners as a pest in the begonia collection of BBG.The economic threshold for pest attack on begonia collection of BBG is very low because this is the only Indonesian Botanical Garden with the largest collection of begonias.Out of 2,000 species of begonia worldwide, Indonesia has 400 species, some of which are endemic to Indonesia.The most complete collection is in BBG which collected 300 different species.However, pest attacks leave a  variety of symptoms that disrupt the aesthetics of the begonia garden and threaten our conservation efforts.Additionally, planting one plant family in one area will facilitate and accelerate pest attacks.Thus, pest control on begonia requires special attention to maintain the aesthetics of begonia plants' BBG collection and its germplasm conservation.

Conclusion
Pests that attack the Begoniaceae collection of Eka Karya Bali Botanical Garden are the armyworm Spodoptera litura (Lepidoptera: Noctuidae), two species of whiteflies Aleurodicus destructor and Bemisia tabaci (Hemiptera: Aleyrodidae), slug snail Parmarion martensi (Gastropoda: Ariophantidae), and tramp snails Bradybaena similaris (Gastropods: Bradybaenidae).The armyworm attack is characterized by its larvae biting starting from the edge of the leaf, while slime marks and holes in the leaves with irregular shapes, sizes, and positions precede attack symptoms caused by tramp snails and slug snails.Meanwhile, the symptoms of a whitefly attack are white circular patterns on the underside of the leaves.The results of this study can be used as a reference to determine appropriate pest control techniques in Begoniaceae conservation efforts.

Figure 1 .
Figure 1.Armyworm attacks on begonia leaves (a) starting from the edge of the leaf, (b)continuing to all parts of the leaf until the leaves are damaged and torn.

Figure 2 .
Figure 2. Symptoms of white fly attack on Begoniaceae in Eka Karya Bali Botanical Garden.(a) nymphs secrete a white, shiny, yet sticky liquid resembling hair, (b) the whitefly imago resembles a small moth, its body and wings are covered with white wax powder, (c) traces of egg laying are visible in the presence of circular pattern on the underside of the leaf after the colony leaves the affected leaf.

Figure 3 .
Figure 3. Snail found in the Begoniaceae collection at the Eka Karya Bali Botanical Garden.(a) Parmarion martensi (Gastropoda: Ariophantidae), (b) Bradybaena similaris (Gastropoda: Camaenidae) with damage symptoms to the leaves in the form of mucus marks, (c) advance attack marked by holes and tear marks in irregular shape and size on the leaves.

Table 1 .
Pest-potential organisms found in the Begoniaceae collection of Eka Karya Bali Botanic Garden