Diversity and ecology of black flies in tea plantation area of Puncak Bogor, Indonesia

Accepted Manuscript Title: Diversity and ecology of black flies in tea plantation area of Puncak Bogor, Indonesia Authors: Upik Kesumawati Hadi, Susi Soviana, Isna Lailatur Rohmah PII: DOI: Reference:

S0001-706X(19)30061-0 https://doi.org/10.1016/j.actatropica.2019.04.010 ACTROP 4986

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Acta Tropica

Received date: Revised date: Accepted date:

16 January 2019 9 April 2019 9 April 2019

Please cite this article as: Kesumawati Hadi U, Soviana S, Lailatur Rohmah I, Diversity and ecology of black flies in tea plantation area of Puncak Bogor, Indonesia, Acta Tropica (2019), https://doi.org/10.1016/j.actatropica.2019.04.010 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Diversity and ecology of black flies in tea plantation area of Puncak Bogor, Indonesia

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Upik Kesumawati Hadi 1*, Susi Soviana 1, Isna Lailatur Rohmah1

Entomology Laboratory, Division of Parasitology, Departement of Animal Infectious diseases

and Veterinary Public Health, Faculty of Veterinary Medicine, IPB University, Jl Agatis Darmaga Bogor 16880.

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*Corresponding author e-mail: [email protected]

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ABSTRACT

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Black flies fauna in Indonesia has been studied extensively, however their ecology is still remaining unexplored. The study was carried out by collecting the larvae and pupae black flies

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in tea plantation area, Puncak Bogor. The collection sites were the streams located in 3 differents type of altitude, i.e. (1) the natural forest area (1200 m above the sea level) (P1); (2) the tea

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plantation area (900-1200 m asl) (P2); and (3) the housing area of the official tea plantation ( 900

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m asl) (P3). The collection of black flies were done beweekly from July 2012 to April 2013. The result showed that 12 species of black flies were recorded which belong to one genus, Simulium

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s.l. and three subgenera (Nevermannia, Gomphostilbia and Simulium s.str). In P1, the area with high elevation (natural forest), it was found the most number of black flies species ( 11 species).

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In the streams around and in the tea plantation area (P2), it was found 7 species, and in P3, the official housing area, it was recorded 8 species. The analysis satistically showed that P1 was dominated by larvae and pupae of S. (S.) argyrocinctum, P2 by larvae and pupae of S. (N.)

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feuerborni, and P3 by S. (S.) argyrocinctum and S. (N.) feuerborni. The distribution of these species was different according to the elevation of the areas.

Keywords: Diversity, ecology, Simuliidae, Puncak, Bogor, Indonesia.

1.

Introduction

Black flies (Simuliidae, Diptera) are well known worldwide because of their female bite on human and animals (Crosskey, 1990; Adler and McCready, 2002). This family comprises 2151 species (Adler and Crosskey, 2014), and in Indonesia, there were 124 species of black flies (Hadi and Takaoka, 2018). Some species, when they bite not only cause severe skin diseases to human and animals but also serve as vector of filarial parasites (Ishii et al., 2008). The preimaginal

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black flies inhabit unpolluted running water (Currie and Adler, 2008). The distribution of black fly larvae depends on the flow velocity and the substrates such as stones, rocks, vegetations or

other submerged objects. Moreover some studies demonstrated that the composition of black fly species assemblages in rivers is strongly dependent on some environmental variables which are directly affected by human pressures on river ecosystem such as loss of riparian vegetations

(Feld et al., 2002), hydromorphological modification of the riverbed (Lautenschlager and Kiel,

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2005), and most of all, chemical and physico chemical impairment of water (Kachvoryan et al.,

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2007).

Black fly larval studies have been done in many parts of the world such as in the temperate

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region (Ciadamidaro et al., 2016), in the tropical region of South America (McCready et al.,

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2004), in the Atlantic Forest, Brazil (Docile et al., 2015), and the Oriental Region, notably Thailand (Pramual and Wongpakam, 2010) and Peninsular Malaysia (Ya’cob et al., 2016).

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Recently, Rohmah et al. (2018) reported the ecology of black fly larval around streams of

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waterfall areas of Bogor, however, the significance of Indonesian black flies remains unexplored. Hence, the currents study aims to explore the diversity and the seasonal occurrence of black

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flies in Tea Plantation Area of Puncak Bogor.

2.

Material and Methods

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2.1 Study Area

The study was carried out by doing collections both of reared adult and immature (larvae

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and pupae) black fly in tea plantation area, Puncak Bogor. The collection sites were the streams located in 3 differents type of altitude (Table 1), i.e. (1) the natural forest area with elevation more than 1200 m above the sea level and water temperature was about 15-17 ˚C (P1); (2) the tea plantation area with elevation about 900-1200 m above the sea level and water temperature was about 18-20 ˚C (P2); and (3) the housing area of the official tea plantation with elevation about

900 above the sea level and water temperature was about 15-17 ˚C (P3). The collection of black flies were done beweekly from July 2012 to April 2013.

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2.2 Collection of immature stage and identification

The method used in the field to collect the immature stages and to obtain reared adults

follows the method of Takaoka (1983). The grass leaves and/or sticks in running water were

searched for larvae or pupae of black flies. The larvae, if present together with pupae were first removed and put in a small vial with 70% alcohol. The substrates were cut into pieces so that

each part harbored a single pupa. They were each put in plastic test tubes (10 cm long x 1.7 cm

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diametral) with very little water at bottom. Pupa attached to the surface of stones or rocks were

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carefully removed by forcepts. The tubes containing an individual pupa were aligned in 30 x 30 x 3 cm plastic tray and then wrapped with a wet towel to avoid exposure to high temperatures.

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They were kept in the course of collection and trasportation until adult emerged. Reared adults

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were transferred to small glass vials containing clean soft tissue paper and allowed to live for at least 24 hours. After that, these black flies were preserved in 70% alcohol together with their

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pupal excuviae. During each field investigation notes were made on the present and relative

relevant data.

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abundance of Simulium, the characters of stream bed, the current flow, the water temperature and

The collected specimens were identified base on the morphological features and

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classification of Crosskey (1993) and Takaoka and Davies (1996).

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2.3 Data analysis

The analysis data on the diversity and dominance index of black flies larval and pupal

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collected followed of Shannon-weiner (Southwood 1978).

3.

Results

3.1 Diversity of black fly species

The result showed that during the ten-month investigations on seasonal occurrence of black flies, 12 species of black flies were found. All species belong to one genus, Simulium s.l. and three subgenera Nevermannia, Gomphostilbia and Simulium s.str. Table 2 shows the black fly species diversity in three different type of altitude in tea plantation, Puncak Area. In P1, the area with highest elevation, it was found the most numbers of

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black flies spesies ( 11 species), i.e. S. (N.) feuerborni, S. (G.) sundaicum, S. (G.) gyorkosae, S. (G.) atratoides, S. (S.) argyrocinctum, S. (S.) eximium, S. (S.) upikae, S. (S.) sigiti, S. (S.)

iridescens, S. (S.) nebulicola, and S. (S.) celsum. In the streams around and in the tea plantation area with moderate elevation (P2), it was found 7 species, i.e. S. (N.) feuerborni, S. (G.)

sundaicum, S. (G.) gyorkosae, S. (G.) atratoides, S. (S.) argyrocinctum, S. (S.) iridescens, and S. (S.) nebulicola. In P3, the official housing area of the tea plantation, 8 species were recorded, i.e.

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S. (N.) aureohirtum, S. (N.) feuerborni, S. (G.) sundaicum, S. (G.) gyorkosae, S. (G.) atratoides,

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S. (S.) argyrocinctum, S. (S.) iridescens, and S. (S.) nebulicola.

Several species such as S. (S.) eximium, S. (S.) upikae, S. (S.) sigiti and S. (S.) celsum were

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only found in the area with high elevation (P1), and S. (N.) auroeohirtum was only collected in

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the official housing area of the tea platation (P3). The rank abundance of black fly larvae and pupae in three different collection sites in Puncak area were shown in Fig 1-2. The analysis

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statistically showed that P1 was dominated by larvae and pupae of S. (S.) argyrocinctum, P2 by

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larvae and pupae of S. (N.) feuerborni, and P3 by larvae of S. (N.) feuerborni and S. (S.) argyrocinctum (Table 3).

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3.2 The seasonal occurrence of each black fly species The seasonal occurrence of each black fly larval species were shown in Fig. 3-14. During

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10 month observations, S. (N.) aureohirtum was found every month from July 2012 to April 2013 in the housing area (P3), and the numbers of larvae were peak during September to

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November. However, this species was not found in P1 and P2 (Fig. 3). In this area pupal and larval were found at trailing grasses in a small stream 20-29 cm wide at outlet of small pond, and also in another streams1-2 m with moderate flow, exposed to the sun. Water temperature was 20 ˚C and 21 ˚C, repectively. Fig. 4 showed that S. (N.) feuerborni was found every month in P2 and P3 (except September) and the larval and pupal population were high during March to April in P2, and

November to December in P3. This species was found in P1 only in September and April. Pupae and larvae of this species were collected in small to medium size man-made streams (10-50 cm wide) shaded or exposed to the sun, especially along the small road in the tea plantation. This species was also found in the open fields near the natural forest (P1), with water temperature was 19-20 ˚C.

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Figs. 5-7 showed the fluctuation of 3 species of subgenus Gomphostilbia, i.e. S. (G.)

sundaicum, S. (G.) gyorkosae, and S. (G.) atratoides. Their existence of these 3 species almost similar, they were found in P3 in abundance during November to December. In P3, S. (G.)

sundaicum was collected every month from July to April on trailing grasses, twigs and fallen leaves in small streams, however the numbers was peak on December, then decreased in

fluctuatively on the following months (Fig. 5). S. (G.) gyorkosae was found almost every month

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in P2 (except on April) and P3 (except on January) and the larval and pupal population were

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high during July to August, November to December, but the numbers of larvae and pupae were abundance in P3. This species is found in P1 only between October and December (Fig. 6).

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Pupae and larvae of this species were found on fine roots, twigs, leaves of grasses trailing in the

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water of small shaded streams (20 – 50 cm wide) in natural forest and nearby open fields. This species were collected together with S. (N.) feuerborni, S. (G.) sundaicum, S. (G.) atratoides and

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S (S.) sigiti. Fig. 7 showed that S. (G.) atratoides was found in P1, P2 and P3, and the larval and

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pupal population were high during late September, November and December in P1, but in P2 it was found November to April. Pupae and larvae of this species were collected on fine roots, twigs and leaves of grasses trailing in the water of small shaded streams (20-40 cm wide) in the

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forest and open fields. This species was also found together with S. (N.) feuerborni, S. (G.) sundaicum, S. (G.) gyorkosae, and S (S.) argyrocinctum.

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The fluctuation of 7 species of subgenus Simulium, i.e S. (S.) argyrocinctum S. (S.)

eximium, S. (S.) upikae, S. (S.) sigiti, S. (S.) iridescens, S. (S.) nebulicola, and S. (S.) celsum were

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shown in Figs. 8-14. S. (S.) argyrocinctum, S. (S.) iridescens, and S. (S.) nebulicola have similar pattern during 10 month observations in P1, P2, and P3 (Figs. 8, 12, 13). They were also found together in their habitats. The larvae and pupae of S. (S.) argyrocinctum was found attachement to the trailing grass, and leaves in small to medium streams (20-40 cm) and also large stream exposed to the sun or partially shaded. S. (S.) eximium, and S. (S.) upikae (Figs. 9-10) were found together attached to the surface of stones in rapid permanent streams in the natural forest above

the tea plantation area (P1). The larval and pupal of those species were high during the month of September to February. S. (S.) sigiti was found only in P1 (Fig. 11) on late November to early February. This species was collected from slender roots of trees trailing in the water of small shaded grass. S. (S.) celsum was found on sticks and fine roots of grasses trailing in shaded

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stream in July to early August and early January to early of February (Fig. 14).

Discussion

Based on this research an account is given of the diversity of Simuliidae in tea plantation area, Puncak Bogor. S. (S.) eximium, S. (S.) upikae, S. (S.) sigiti and S. (S.) celsum inhabited

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upland streams, they were only found in the area with high elevation (P1), and S. (N.)

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aureohirtum inhabited low land area, and only collected in the official housing area of the tea plantation (P3). Pramual and Kuvangkadilok (2009) reported that S. (N.) aureohirtum founded at

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smaller and slower streams, open, and small streambed particles. Meanwhile the other species,

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i.e. with S. (N.) feuerborni, S. (G.) sundaicum, S. (G.) gyorkosae, S. (G.) atratoides, S. (S.) argyrocinctum, S. (S.) iridescens, and S. (S.) nebulicola were widely distributed in these area

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(P1, P2, P3). Rohmah et al., (2018) reported that no significant relationship was found between

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the altitudes with the number of Simulium larvae found. Meanwhile, Zahar (1951) stated that altitude plays a vital role in distribution because it influences river temperature. Besides that, each species of Simulium has different ability to breed at specific water temperatures. Crosskey

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(1990) stated that water temperature can influence duration off egg to adult from Simuliidae. Water temperature used by S. maculatum, S. erythrocephalum and S. reptans larva’s to emerge is

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9.9-17 ºC, 10.6-20.4 ºC, 10-16.4 ºC (Bernotiene and Bartkeviciene 2013) . Carlsson (1967) stated that each spesies of black fly has optimum temperature at larval stage.

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Some species such as S. (G.) gyorkosae was found together with S. (N.) feuerborni, S. (G.)

sundaicum, and S (S.) argyrocinctum,, they were found together more than 70% of the time.. Distribution of these species may depend on the selection of the site by the gravid female. The gravid females of thoses species may share a common site for egg-laying, thus forming a primary focus of the several species. The primary sites established by the deposition of egg masses, larvae can disperse actively to the secondary sites as a response to unfavorable conditions such

as dessication, or they may be carried passively during conditions of spate. Meanwhile, Zahar (1951) stated that different river characters, for example, the type of water flow, vegetation, physical aspect, and stream width, play an essential role in the distribution of Simulium species. The environmental factors affecting the habitat of the immature stages of Simuliidae are the water temperature, the type of current, the current rate, vegetation, characters of stream bed, food

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material and oxygen (Tongjura et al., 2015; Ya’cob et al., 2016; Rohmah et al., 2018). In

addition, one of the most important environmental factors affecting the habitat of immature

simuliids in some parts of the world is stream size (Adler and McCreadie (1997). Rohmah et al., (2018) stated that in Bogor, Indonesia the black fly was found in waters with 18.19-23.17 ˚C.

Black fly larvae in Peninsular Malaysia can also be found in streams at a speed of 0.12-1.1 m/sec (Ya’cob et al., 2016). Meanwhile, Zahar (1951) stated that rivers located in the highlands have

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rocky characteristics that are rarely covered by algae or moss on their surface. Simulium likes

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these characteristics, especially for breeding, as in the semi-uplands The size of pupae depends upon the availibility of the food material during larva existence.

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Colbo and Porter (1979) stated that reduced food supply of S. vitatum and S. verecundum will

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cause extended time of development, declined of survival, decreased of size, and fecundity. When the plankton is less abundance (during drought), pupae are smaller. There is no direct

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correlation between current velocity and degree of oxygen saturation, and it is concluded that the

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relation of Simulium to current is not determined through the oxygen factor. This was inconsistent with other studies suggesting that current velocity was correlated with the amount of

2018).

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Simulium found (Hamada et al., 2002; Srisuka et al., 2015; Ya’cob et al., 2016; Rohmah et al.,

Physical conditions of the substrates have a pronounced effect in limiting larval

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distribution. Accumulation of silt and overgrowth by bryophytes compel larval migration, and these conditions occur most readily when the current rate is slow. It was difficult to determine

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the density of population accurately in different streams. As blood-suckers Simulium species are less important in Indonesia than in many other contries. However, they occasionally contributed of annoyance to humans, especially who live near the streams. Based on the interview, more than 10 people who work on tea plantation have been bitten by insect, but they didn’t have any information about the species of the insect.

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Conclusion In tea plantation of Puncak Bogor area there were 12 species of black flies recorded which

belong to one genus, Simulium s.l. and three subgenera (Nevermannia, Gomphostilbia and Simulium s.str). In P1, the area with high elevation (natural forest), it was found the most number of black flies species ( 11 species). In the streams around and in the tea plantation area (P2), it

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was found 7 species, and in P3, the official housing area, it was recorded 8 species. The analysis satistically showed that P1 was dominated by larvae and pupae of S. (S.) argyrocinctum, P2 by larvae and pupae of S. (N.) feuerborni, and P3 by S. (S.) argyrocinctum and S. (N.) feuerborni. The distribution of these species was different according to the elevation of the areas.

Acknowledgments

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We are grateful to Prof. Singgih H. Sigit and all staff of Laboratory Entomology,

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Division of Parasitology and Medical Entomology, Department of Animal infectious Diseases

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their continuous support and encouragement.

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and Veterinary Public Health, Faculty of Veterinary Medicine, IPB University, Indonesia, for

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Zahar, A.R., 1951. The Ecology and Distribution of Black-Flies (Simuliidae) in South-East Scotland. Journal of Animal Ecology 20 (1): 33-62. DOI: 10.2307/1643. https://www.jstor.org/stable/1643

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Fig 1. Seasonal occurrence of larval and pupal black fly species in three different collection sites in Puncak Bogor

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Fig 3. Seasonal occurrence of S. (N.) aureohirtum larva in three different collection sites in Puncak Bogor

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Fig 2. The rank-abundance of larval and pupal black fly species in three different collection sites in Puncak, Bogor

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Fig 4. Seasonal occurrence of S. (N.) feuerborni larva in three different collection sites in Puncak Bogor

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Fig 5. Seasonal occurrence of S. (G.) sundaicum larva in three different collection sites in Puncak Bogor

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Fig 7. Seasonal occurrence of S. (G.) atratoides larva in three different collection sites in Puncak Bogor

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Fig 8. Seasonal occurrence of S. (S.) argyrocinctum larva in three different collection sites in Puncak Bogor

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Fig 9. Seasonal occurrence of S. (S.) eximium larva in three different collection sites in Puncak Bogor

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Fig 11. Seasonal occurrence of S. (S.) sigiti larva in three different collection sites in Puncak Bogor

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Number of Individu

U

Fig 10. Seasonal occurrence of S. (S.) upikae larva in three different collection sites in Puncak Bogor

EP

Month P2 P3

P1

A

CC

Fig 12. Seasonal occurrence of S. (S.) iridescens larva in three different collection sites in Puncak Bogor

20 15 10 5

SC RI PT

Number of Individu

25

0

P1

Month P2

P3

A

CC

EP

TE

D

M

A

N

U

Fig 13. Seasonal occurrence of S. (S.) nebulicola larva in three different collection sites in Puncak Bogor

1.2 1 0.8 0.6

SC RI PT

0.4 0.2 0

P1

P2

P3

A

CC

EP

TE

D

M

A

N

U

Fig 14. Seasonal occurrence of S. (S.) celsum larva in three different collection sites in Puncak Bogor

Tabel 1. GPS coordinate of sampling location Location P1

GPS coordinate S6°42'27.57" E106°59'9.73"

Altitude (masl) 1275

2

P2

S6°42'11" E 106°58'44"

1151

3

P3

S6°41'14" E 106°57'28"

894

A

CC

EP

TE

D

M

A

N

U

SC RI PT

Number 1

Table 2. Distribution of Simuliidae in three different collection areas of Puncak from July 2013 to April 2014 Location

Jul

Aug

Sep

Oct

Nov

Dec

Jan

Feb

Mar

Apr

S. aureohirtum

P1

-

-

-

-

-

-

-

-

-

-

P2 P3 P1

-/+ -

+ -

+ -/+

+ -

+ -

+ -

+ -

+ -

+/-

+ +/-

P2

+

+

+

+

+

+

+

+

+

+

P3

+

+

+

+

+

+

+

+

+

+

P1

-

-/+

+

+

+/-

+/-

+/-

-

+/-

-

P2

+

-/+

+

+

+/-

+

+

+

+/-

-

P3

+

+

+

+

+

+

+

+

+

+

S. eximium

-

-/+

-

+

-

-

-

-

+/-

-/+

-/+

-/+

+

+

+

+

-

P3

+

+

+/-

+

+

+

-

+

+

+

P1

-

-

+

-

P2

-

-

-

-

P3

-

-/+

+/-

-

P1

-/+

+

-

P2

-/+

+/-

-

P3

+/-

-/+

P1

-

-

P2

-

-

P3

-

-

-

-

-

-

-

-

-

-

P1

-

-

-/+

-/+

+

-/+

-/+

+/-

+/-

+

P2

-

-

-

-

-

-

-

-

-

-

P3

-

-

-

-

-

-

-

-

-

-

P1

-

-

-

-

-

+/-

+

-

-

-

P2

-

-

-

-

-

-

-

-

-

-

P3

-

-

-

-

-

-

-

-

-

-

P1

-

+

+

+

+

+

+

+

+

+/-

P2

-

-/+

-

-

-/+

+

+/-

-

-

+

P3

-

+

+/-

-

-

-

+

+

+

+

P1

+

+

+

+

+

+

+

+

+

-

P2

-

-/+

-

-

-/+

+

-

-

-

-

P3

-

+

-

-

-

-

+

+

+

+

P1

-/+

-

-

-

-

-

-/+

-

-

-

P2

-

-

-

-

-

-

-

-

-

-

P3

-

-

-

-

-

-

-

-

-

-

TE

S. upikae

-

+

EP

S. sigiti

CC

S. iridescens

A

S. nebulicola

S. celsum

U

S. argyrocinctum

-

P2

+

+

-

-

-

-

+/-

+

+

+

+

-/+

+

+

-/+

+

+

-/+

+

+

+

+

+

+

-

+/-

+/-

-/+

+

+

+

+/-

+

+/-

+

+

+

+

+

+

-/+

+

+

-

+

+/-

-

-

-

-

-

-

-

-

-

N

S. atratoides

P1

+

A

S. gyorkosae

M

S. sundaicum

D

S. feuerborni

SC RI PT

Species

Note: - absent, -/+ absent on the first/ present on the second observations, + present, P1 = the natural forest area with elevation more than 1200 m above the sea level, P2 = the tea plantation area with elevation about 900-1200 m, and P3 = the housing area which surrounded by the tea plantation with elevation about 900 m.

Table 3. Dominance index of black fly species in three different collection areas in Puncak, Bogor, from July 2013 to April 2014 Stage

ST

Α

NT

Nmax

d

Dominant species

P1

Larva Pupa

9 8

0.484 0.430

218 40

124 18

0.569 0.450

S.(S.) argyrocinctum S.(S.) argyrocinctum

P2

Larva Pupa

7 6

0.754 0.734

196 78

147 65

0.750 0.833

S.(S.) feuerborni S.(S.) feuerborni

P3

Larva Pupa

8 7

0.564 0.673

168 40

168 40

0.333 0.364

S.(S.) argyrocinctum S.(S.) feuerborni

U

SC RI PT

Locations

A

CC

EP

TE

D

M

A

N

Notes: ST = Total species; A = Dominance index; NT = Total number of individuals; Nmax = Total catch this is due to dominant species; d = Berger – Parker Dominance index