Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

Potential breeding sites and abundance of filariasis vector mosquitoes in buton district, Southeast Sulawesi Province

Raden Ajeng Wigati1*, Mujiyono Mujiyono1, Nurhidayati Nurhidayati1, Siti Diniarsih2, Hening Triandika3, Setyo Sulistyono3

1Institute of Vector and Reservoir Control Research and Development, Salatiga 2Biolaska Study Club, Biology Department of UIN Sunan Kalijaga Yogyakarta 3Faculty of Mathematics and Natural Sciences, Yogyakarta State University (UNY)

*Corresponding author: Raden Ajeng Wigati Institute of Vector and Reservoir Control Research and Development National Institute of Health Research and Development Ministry of Health, Hasanudin 123, Salatiga 50721 Central Java, Telephone number/Fax : (0298)-327096/ (0298)-322604 Email address: [email protected]

Abstract Background: Lymphatic filariasis is one of tropical diseases, transmitted by mosquitoes. It is important to know the distribution, ecology, and biology of mosquitoes that depend on the genus and species. High populations are associated with the availability of mosquito breeding sites. Not all breeding sites are clearly visible to humans. Some species prefer temporary water bodies, while others prefer more permanent ones. Potential habitat is a major factor of the diversity and abundance of vector mosquito populations in Buton Regency, Southeast Sulawesi. Aims: The study aimed to determine ’ abundance and describe mosquitoes breeding sites. Methods: Tools used for collecting mosquitos’ larvae were mosquito dipper, aquatic nets, and larvae pipette. The survey was performed in two filariasis-endemic villages, which were Bonelalo and Mabulugo with explorative descriptive methods. Results: Based on the results, there are nine types of mosquito breeding sites in two villages, namely ditches, wellsprings, river banks, rice fields, puddles, coconut shells, irrigation channels, mangroves, and estuary. Potential breeding sites that support mosquito development stage include muddy beaches, rocky beaches, mangrove, community plantations, crop, paddy fields, and secondary forest. In Bonelalo and Mabulugo Village, quinquefasciatus and Cx. vishnui were the most abundant species. Those were supported by the existence of potential breeding sites dominant in Bonelalo and Mabulugo villages, namely ditches and puddles. Conclusions: potential breeding sites of filarial vector mosquitoes will promote their life stage that will directly relate to the transmission of filariasis. Keywords: potential breeding sites, abundance, mosquitoes, filariasis, Buton District

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

How to cite this article: Wigati RA, Mujiyono M, et al (2021): Potential breeding sites and abundance of filariasis vector mosquitoes in Buton district, Southeast Sulawesi province, Ann Trop Med & Public Health; 24 (S01): SP24147. DOI: http://doi.org/10.36295/ASRO.2021.24147

Introduction Mosquitoes live in almost all natural ecosystems. To maintain the ecosystem balance, mosquitoes are influenced by biotic (predators, parasites) and abiotic (temperature, rainfall, climate) factors. Likewise, each species has specific habitats 1. Distribution of breeding sites and diversity mosquito in various ecosystems can change as a result of human activities. So, it is important to know breeding sites distribution and diversity of mosquitoes for ecosystems which have been managed by humans. Some mosquitoes are cosmopolitan and live near human habitations 2. Mosquitoes have been known as one of haematophagus and some of them can serve as vectors for transmitting protozoan, worms, or virus, which become agent of human diseases in many parts of the world, including in Indonesia3; 4. There are more than 457 types of mosquitoes from 18 genera in Indonesia. These species are mainly dominated by genera Aedes, Anopheles and Culex, which are 287 species. These three genera get more attention because they are generally zoophilic or anthropophilic, which can be a disease vector. Some viruses, plasmodia or filarial can be transmitted by those genera Aedes, Anopheles and Culex. However, it does not mean that other types are not important, for instance a fitophilic species (sucking plant fluids) 5. In Sulawesi island, 134 species of mosquitoes have been recorded, or about 25 percent of the total number of mosquitoes in Indonesia 6. Lymphatic filariasis, commonly called elephantiasis, is one of the neglected tropical diseases. Lymphatic filariasis is an infectious disease caused by Nematode worm infections and is transmitted by mosquitoes 7. Various mosquitoes have been found to act as filariasis vectors, namely Anopheles, Culex, Mansonia, Aedes and Armigeres8 whose distribution, ecology, biology and transmission potential vary greatly. There are 23 species of mosquitoes from 5 genera known to act as filariasis vectors. Therefore, it is necessary to know vector bionomic which includes feeding behaviour, resting behaviour and mosquito breeding sites. It is important to know where the breeding sites are. The sites depend on the genus and species of mosquito and they vary widely. Not all breeding sites are clearly visible to humans, especially as some species prefer temporary water bodies, while others prefer more permanent ones. Potential breeding site is a major factor determining the diversity and abundance of vector mosquito populations in Buton Regency, Southeast Sulawesi. In Buton Regency, between 2006 and 2007, the prevalence of filariasis increased from 0.56/10,000 to 0.58/10,000. Meanwhile, within the period of 2008-2013, the prevalence of filariasis tended to decrease, as follows 0.43/10,000 (2008); 0.49/10,000 (2009); 0.47/10,000 (2010); 0.30/10,000 (2011); 0.30/10,000 (2012); 0.30/10,000 (2013). However, the prevalence of filariasis increased from 2014 to 2015, which was about 1.26/10,000 (2014) and 2.33/10,000 (2015) and in 2016 it decreased to 0.6/10,000, whereas in 2017 there were no cases of filariasis 9. The study aimed to determine mosquitoes abundance and describe mosquitoes breeding sites. The correlation between mosquitoes and their breeding sites is important for understanding the risk of

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01 disease transmission to apply appropriate mosquito management. These are important steps in characterizing the risk of transmission and consequences of vector-borne diseases.

Subjects and Methods Data collection was carried out two times using exploration method for one month interval, in September and October 2017. The study sites were 2 filariasis endemic villages namely Bonelalo Village, Lasalimu Sub-district and Mabulugo Village, Kapontori Sub-district. Each potential habitat was surveyed to find mosquito breeding sites at a radius of ± 1 km from the house of patients identified positive in finger blood test. The collection of mosquito larvae was done by dipper, trays and pipettes. Types of mosquito breeding sites were then recorded and grouped in terms of habitat and location for data collection. Data on vector mosquito abundance were collected using a modified human landing collection method inside mosquito nets. Catching mosquitoes was carried out by 3 catchers inside mosquito nets inside the house and 3 catchers inside mosquito nets outside the house that were different in each village. Mosquito nets used consisted of 2 mosquito nets namely outdoor open mosquito nets and an inside mosquito net that was smaller than an outdoor mosquito net. Human bait was placed in a mosquito net inside. Every ten minutes, a mosquito catcher came out of mosquito net inside to catch mosquitoes that were between two mosquito nets. Mosquitoes that were collected then identified using a dissecting microscope and mosquito identification key book. The data on mosquito breeding places and potential habitats were analyzed descriptively while mosquito abundance data were analyzed by adding up all mosquitoes which were collected in every village.

Results a. Potential habitat and mosquito breeding sites Based on results, there were six potential habitats and nine breeding sites in two study villages (Table 1).In Bonelalo, there were 7 (seven) types of mosquito breeding sites that was in different habitats. Bonelalo is located on East Coast of Buton which is closed to Banda Sea. The beaches in Bonelalo are coral and rocky. The beach full of sludge substrate mixed with sand which is located near by estuary and the vegetation dominated by mangroves. Residents were concentrated on South Coast, while areas that are more inland are usually used as fields and gardens. Gardens around Bonelalo residents, planted cashew, areca nut, and coconut trees. While the fields are planted with cassava, vegetables and watermelon. In the West of residents, there was a hill whose vegetation was dominated by big and heterogeneous trees. Behind the hill, there is a spring whose stream becomes a ditch that leads to Southern Coast. During heavy rain, water pressure was increasing. In the North of village, which is 500 metre, there is a river by flowing water. Water flow comes out from the forest to the East Cost where there were mangrove forests. Fields resident were not only found around the village, but some were far from. Resident usually stay in the fields during harvest or planting season. The fields remote from

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01 settlement were border on with teak woods and underbrush. Most residents have cattle and goats left in the garden. Mabulugo village is located on West Buton, on the edge of West Coast. Location for collecting vector data was approximately 300 metre from coastal area. The type of beach is sludge and is not direct into offshore. It is a strait that separates by Panjang Ocean. Seashore is covered by small mangrove. The plantation is between residents houses’ usually only planted with bananas, coconuts, mango, talok, silk cotton trees and dominated by cashew trees. Behind the residents’ village, there is an irrigation water flowing which flow from East to West towards ocean. The ditch with water conditions welled and dirty which comes from waste bathroom resident’s many found among residents' backyard plantation behind settlement. To the South, away from the village, there is a secondary forest with heterogeneous composition of tree plants. The distance is about 500 m from the village. One kilometer to the south, away from secondary forest, there are paddy fields whose water flew to irrigation behind residents' village. Paddy fields were quite wide and at the time of survey, they had been harvested and condition of water was stagnant. Around paddy fields, there was brick-making house which is usually keep working during daytime. The tree that dominated was Naucleaorientalis which was planted by residents and the wood is used. There are no residents of Mabulugo village that raising big mammals like some cattle and goat. that were kept such as chickens, cats and dogs. Otherwise, at the West of village (about 2 kilometre to the East) which belongs to Wakalambe Village administrative area, which Balinese residents were raising cattle and pigs. Balinese residents who manage to making of red bricks and occupying house at the edge of paddy fields. b. Abundance of filariasis vector mosquito species The mosquito collection was showed on Table 2. Twenty three species of seven genera mosquitoes were collected from two village of study site. Genera of Culex was the most varied species among them, namely 9 species. The abundance of mosquitoes-caught by using a modified human landing collection method inside mosquito nets is presented on Table 2. Based on Table 2, mosquito species which abundant in Bonelalo village was Culex quinquefasciatus, while in Mabulugo village were Culex vishnui and Culex quinquefasciatus.

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

Table 1. Potential habitat and breeding sites of mosquitoes in Bonelalo and Mabulugo Village, Buton District, September - October 2107 Study site (village) No Potential Habitat Breeding Sites

Bonelalo 1 Secondary Forest Wellspring 2 Secondary Forest Riverside 3 Community Plantation Puddle 4 Community Plantation Coconut Shell 5 Community Plantation Ditch 6 Rocky/Coral Beach Mangroves 7 Rocky/Coral Beach Estuary 8 Field Ditch Mabulugo 9 Paddy Field Paddy Field 10 Paddy Field Irrigation Canals 11 Community Plantation Puddle 12 Community Plantation Ditch 13 Secondary Forest Ditch 14 Muddy Beach Mangroves

Table 2. Abundance mosquitoes species in Bonelalo and Mabulugo Village in Buton, September-October 2017 Bonelalo A Number Mabulugo A Number No Species Sept Okt of Sept Okt of 1 Aedes aegypti 4 5 9 0 0 0 2 Aedes albopictus 1 0 1 0 0 0 3 Aedes amesii 0 0 0 0 1 1 4 Anopheles barbirostris 0 0 0 12 2 14 5 Anopheles flavirostris 2 1 3 0 0 0 6 Anopheles kochi 0 0 0 0 1 1 7 Anopheles subpictus 0 0 0 0 1 1 8 Anopheles tesselatus 0 0 0 0 1 1 9 Anopheles vagus 0 0 0 2 0 2 10 Armigeres malayi 1 0 1 0 0 0 11 Armigeres subalbatus 1 25 26 0 0 0 12 Coquilettidia crassipes 0 0 0 1 0 1 13 Culex bitaeniorhynchus 1 0 1 0 0 0 14 Culex mammilifer 2 0 2 0 0 0 15 Culex mimulus 0 1 1 0 0 0 16 Culex nigropunctatus 3 1 4 2 0 2 17 Culex pallidothorax 0 1 1 0 0 0 18 Culex quinquefasciatus 97 150 247 183 140 323 19 Culex sitiens 0 1 1 0 2 2 20 Culex tritaeniorhynchus 0 0 0 10 3 13 21 Culex vishnui 0 2 2 324 112 436 22 Mansonia uniformis 0 0 0 2 0 2 23 lateralis 2 0 2 0 0 0 Total 114 187 301 536 263 799

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

Figure 1. Potential breeding sites of mosquito in Bonelalo and Mabulugo village, Buton District

Discussions Geographically, mosquitoes are cosmopolite insects, which are widespread in the tropic and sub- tropic regions 2. Seasonally, the changing environment also affects their activity, diversity, distribution, and density. Research has shown that mosquitoes can be competent vectors, efficient distributors, and reinforcing agents for various parasites in and human populations 2;10.

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

The environment has an impact on distribution of filariasis cases and transmission. The study results showed that around residential areas found plantation areas, secondary forests, beaches, fields, and paddy fields which have a role as breeding sites and mosquito resting place. In every habitat, found one or more types of potential mosquito breeding sites which its mosquito preference to lay eggs. Water bodies that are temporary such as ditches and puddles neither nor does it dry through a year like paddy fields, springs, and irrigation canal which provide microhabitat supported the development of mosquito pre-adults. All members of genera Aedes, Anopheles, Culex, Mansonia, and Armigeres potentially as a vector of filariasis. Some species have been shown containing microfilaria worms on their bodies.Nine species of them were found in this study namely; An. barbirostris, An. kochi, An. subpictus, An. vagus, Ar. subalbatus, Cx. bitaeniorhynchus, Cx. quinquefasciatus, Cx. vishnui dan Ma. uniformis was assumed as filariasis vector in Buton 11. GeneraAedeswere not so many collected,while they are prefer diurnal mosquito. There are not many containers that are preferred by this group of mosquitoes to lay eggs except for a coconut shell. Anopheles mosquitoes collected are quite diverse, but amount of each type was not abundant. Genera Culex were quite diverse and dominated by Cx. quinquefasciatus and Cx. vishnui.Culexquinquefasciatus to be the dominant in the area of study. The dominancy this mosquito also is showed in the different endemic areas. Culexquinquefasciatus was abundant and it was the most frequent active. Cx. quinquefasciatus caughted more frequently during the time of collection rather than other species. Every mosquito species has its own distribution, behaviour pattern and character of its habitat different from others 12. Cx. quinquefasciatus is a vector of the Wuchereriabancrofti urban type. Indonesia, it has been confirmed that Cx. quinquefasciatus is a W.bancrofti vector 13. In the research conducted by Safitri on Cx. quinquefasciatus from Barito Kuala District, Kalimantan, Brugiamalayi larva were found 14. This finding can happen because the environment in this places is suitable for Cx. quinquefasciatus and Brugiamalayi worms. Research conducted by Yahya etal.,(2014) showed that Cx. quinquefasciatus had more potential to be a Brugiamalayi vector than Armigeressubalbatus15. Other species, Cx. tritaeniorhyncus were known as Japanese Encephalitis (JE) virus 4; 16. In this area, the occurrence of abundance Cx. tritaeniorhyncus species was low. This may because of it more like the animal rather than human as its source of blood,such as chicken and domestic birds. Genera Mansonia found was only one species namely Ma. uniformis. Mansonialives in swamps or paddy fields with aquatic plants. Mansoniauniformis collected were only 2 mosquitoes in Mabulugo Village where there were paddy fields breeding sites. However, it was not the season for planting paddy,but many aquatic plants grow. So, it remains a potential for breeding sites of Mansonia mosquitoes. The existence of plants greatly affects a life of mosquito, among others as a place to lay eggs, a place to find food, a shelter for larvae and for resting to adult mosquito as long as gonotropic cycle. The previous study showed that Ma.uniformis in Banyuasin, South Sumatra, were the dominant mosquito 17; 18. The Indonesian Ministry of Health reported that in South Sumatra, filariasis is caused by B.malayi and the vector is Ma.uniformis19. The character of Ma. uniformis breeding sites can affect the incidence of lymphatic filariasis. The research of Sapada etal., in Banyuasin (South Sumatra) and Zen in East Lampung showed that environmental conditions with many aquatic plants such as swamps and

Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147

Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01 ponds can beideal breeding sites for Mansonia spp and are associated with the incidence of lymphatic filariasis 20; 21. Periodic Brugiamalayi was transmitted by An.barbirostris which was paddy fields as breeding sites. Brugiatimori was transmitted by An.barbirostris which was paddy fields, both near and remote beach area. Prevention of filariasis, by breaking chain of transmission through vectors is very important. Filariasis transmission occurs when there are mosquitoes (vector) as intermediaries or host of filarial worms. The high density of mosquito species in an area is one of the success factors in transmitting vector borne diseases. High mosquito populations are associated with the availability of mosquito breeding sites. All mosquito species have their own distribution, behaviour pattern, and characteristics of its habitat, which are different from others. The daily behaviour pattern of mosquito activities will occur at day or night time depending on the species. Each mosquito species needs specific ecological requirement for their survival, distribution, and abundance 16; 22. Moise etal., (2018), has stated that Cx.quinquefasciatus abundance increased significantly in May and June annually as their observed in 2006 to 2010, and temperature was positively affected for the mosquito abundance. Many factors can influence potential vectors to be positive for microfilariae including the amount of microfilariae that are sucked is sufficient or not to develop in the body of a mosquito. The requirements for mosquitoes to become vectors include the age of mosquitoes, contact between humans and animals (hosts) with mosquitoes, the frequency of bloodsucking, and the susceptibility of mosquitoes to parasites 23. The estimated capacity to be a vector is influenced by environmental, behavioural, biochemical, and cellular factors that influence the relationship between vectors, pathogens that will be transmitted by vectors, and hosts where the pathogen will be transmitted. Behavior and environmental factors have a role in distinguishing the mosquitos’ capacity as vectors 24. The mosquito existence is important for transmitting the parasite. Some studies reported that the environment around settlement and human activities in the night time had a significant effect for increasing the risk factor of people to get the infection 25; 12. Windiastuti et al., (2013) said that the existence of breeding sites, resting places around houses, will increase the risk of infection, even it would be more to get infection for people who has active in the night time 26.

Conclusions The environment plays an important role inthe process of transmittingfilariasis. There are still many breeding sites and mosquito resting places in both villages endemic filariasis. Both in Bonelalo and Mabulugo Village, Culex quinquefasciatus and Cx. vishnui were the most abundant species, supported by potential breeding sites, namely ditches and puddles.

Acknowledgements The authors would like to thank the Center for Public Health Efforts, Jakarta, and the Institute of Vector and Reservoir Control Research and Development, Salatiga, for their support.

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Wigati et al (2021): Potential breeding filariasis vector Jan 2021 Vol. 24 Issue 01

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Annals of Tropical Medicine & Public Health http://doi.org/10.36295/ASRO.2021.24147