INTRODUCTION
Aceh Province in Indonesia experienced the most severe earthquake and tsunami disaster in 2004. After the tsunami infrastructure development occurred rapidly in Banda Aceh City. Banda Aceh City became the administrative center of Aceh Province and was the most tsunami-affected area. Residential settlement development continues to increase yearly in Banda Aceh City (Gadeng et al., 2019). The return of the community to new settlements with all the activities of daily life has created a habitat for Aedes and an explosion of cases of dengue hemorrhagic fever (DHF). Reports from the Ministry of the Health Republic of Indonesia revealed that cases of dengue fever in Aceh continued to increase after the tsunami (Ministry of Health Indonesia, 2007). Cases of dengue fever in Banda Aceh City after the tsunami from 2005 to 2007 experienced a significant increase. The explosion of very high dengue cases occurred in 2010, with 759 cases after the return of the community to new housing in 2009 (Agustina et al., 2021).
This condition is related to the high population of Aedes and other supporting factors that caused the presence of Aedes in the tsunami’s neighborhood area of Banda Aceh City. Aedes is an invasive species that can adapt to and interact with the surrounding environment. The invasive species interactions vary in space and time and depend on local conditions (Cunze et al., 2018).
Mosquitoes exist around humans because of the availability of breeding places, eating, and resting habitats. Therefore, it is necessary to have control efforts oriented to the habitat conditions and the necessities of life for it. The life of Aedes depends on plants. Plants are resting places and sources of food for male and female Aedes aegypti L. and Aedes albopictus Skuse (Agustina et al., 2019). Plants can serve as attractors or repels, and each type has a different attraction. Mosquitoes come to plants because smells or colors attract them to get food (Barredo and DeGennaro, 2020).
The selection of plant species by various mosquitoes is related to the volatile compounds produced by each plant. The olfactory systems of A. aegypti, Aedes mcintoshi Huang, and Anopheles gambiae l. can detect different volatile compounds in plants (Nyasembe et al., 2018) because they have an affinity for certain plant species (host plants). Their olfactory system influences the selection of host plants. Plants that attract mosquitoes or are called attractants are very limited in the study, even though these attractant plants also have the potential to control mosquitoes (Nyasembe et al., 2015). Other studies also revealed that eliminating the mesquite plant [Prosopis juliflora (Sw.) DC.], which is the food source of Anopheles, can reduce the population of malaria vector mosquitoes by 69% (Muller et al., 2017). Plant attractant compounds can serve as an effective biological control strategy. The content of secondary metabolites in plants that attract mosquitoes can as act bait in mosquito surveillance and control programs (Dormon et al., 2021). Parts of the plants have attractions such as flowers, sharp aromas, and high nectar content that can attract mosquitoes.
A repellent is an insecticide that is repelling and nonkilling. Every plant has a composition of chemical compounds called secondary metabolites. Essential oils, flavonoids, alkaloids, and aromatic compounds are metabolites in plants that have the potential to be mosquito repellents (Boate and Abalis, 2020). Essential oils, also called volatile oils, are secondary metabolites of volatile plants. This oil exists in fruits, seeds, leaves, flowers, stems, bark, roots, and rhizomes (Sengül Demirak and Canpolat, 2022). Therefore, plants as a place for mosquito feeding and resting activities also have a favorable opportunity to become one of the mosquito control strategies by utilizing secondary metabolite compounds. Plants around us have the potential insecticides, but it is necessary to identify which bioactive molecules in repellent plants have a higher effect on disease-transmitting mosquitoes (Athuman et al., 2016).
House yard plants not only support the life of mosquitoes but also have the potential to control the mosquito population. Based on the content of plant compounds, these plants can act as repellents or attractants for Aedes. This information is necessary to know an effective and targeted control strategy. This study was to determine the potential of house yard plants as an alternative to dengue vector control in the tsunami area settlements of Banda Aceh City.
MATERIALS AND METHODS
Study area
The study is in Banda Aceh City, as it was severely affected by the earthquake and tsunami disasters in 2004 (Fig. 1). Banda Aceh City is between 5°30? – 05°35? north latitude and 95°30? – 99°16? east longitude, with an average elevation of 0.80 meters above sea level, with an area of 61.36 km2 (BPS, 2019). The city of Banda Aceh consists of nine subdistricts, and the research sites are the Meuraxa Subdistrict and Syiah Kuala Subdistrict. The Meuraxa and Syiah Kuala Subdistricts were chosen as the research sites because of the endemic areas for dengue cases. In addition, these two areas were also the worst affected by the tsunami.
Data collection
This research begins with a preliminary survey using an explorative method to determine the condition of the houses in the Meuraxa Subdistrict and Syiah Kuala Subdistrict, Banda Aceh City. Purposive sampling was used to sample 200 sample houses. The selection was houses suspected of having an Aedes breeding place and plants in the yard. The collection of house yard plants involved the larva monitoring community in each village. To determine secondary metabolites that attract or repel Aedes using a literature study, all plants found in the house yards were collected and documented. The data were then summarized, and the results of the studies arranged in the tabular form of the list of secondary metabolites in plants that can function as repellents or attractants.
Data analysis
The data from this research are presented and analyzed using descriptive statistics.
Statistical analysis
Statistical analysis for calculation of graph and table data was carried out with Microsoft Excel.
RESULTS AND DISCUSSION
The results of 200 houses in the tsunami area settlement of Banda Aceh City found 150 species and 63 families of house yard plants (Fig. 2). The category of plant habitus found in the study area comprised herbs (44%), shrubs (32%), and trees (24%) (Fig. 3). The tsunami disaster caused the coast to be badly damaged, and almost all the vegetation was destroyed and lost. After the tsunami, much vegetation of the damaged coastal area naturally changed (succession), namely, the emergence of pioneer plant species such as herbs, shrubs, and trees (Suryawan, 2007).
The family’s highest number of species are from the group Araceae (14 species), Euphorbiaceae (8 species), Asparagaceae (7 species), Lamiaceae (6 species), Apocynaceae (5 species), Arecaceae (5 species), Fabaceae (4 species), Myrtaceae (4 species), Portulacaceae (4 species), Solanaceae (4 species), and Zingiberaceae (4 species) (Fig 2). Many species in this family found at the research sites are related to the COVID-19 pandemic. Restrictions on activities outside the home during the COVID-19 pandemic have provided much free time at home and made many people take up new hobbies such as caring for ornamental plants and business opportunities for buying and selling plants. Plants in pots are obtained easily by ordering through online media or direct purchase. Residents in the tsunami area of Banda Aceh City planted the Araceae family such as Aglaonema and other species because they follow trends and other aspects such as the benefits that they can filter air pollution at home and are easy to maintain (Zahara and Win, 2020).
The families Apocynaceae, Arecaceae, Asparagaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Myrtaceae, Portulacaceae, Solanaceae, and Zingiberaceae are species commonly grown by communities in tsunami areas for various needs or uses such as food crops, medicine, ornamental plants, and traditional ceremonies. Home gardens have contributed to increasing food security, social, cultural, health, and economic community (Du Toit et al., 2022 ; Galhena et al., 2013). Table 1 and Figure 4 shows that 63 families have potential as Aedes mosquito repellent plants. 16 families have potential as Aedes attractants. Analysis of the determination of the plant acting as a repellent or attractant based on the content of secondary metabolites obtained information from the literature study sought.
Figure 1. Location of study area. [Click here to view] |
Potential of house yard plants as repellent of Aedes spp.
The repellants used by the public to prevent mosquito bites are synthetic repellants, one of which contains diethyltoluamide (DEET). These compounds can protect longer than other synthetic and botanical repellents. This synthetic active ingredient has health effects such as contact urticaria, skin eruptions, and encephalopathy. Plants around us have potential as insecticides, but it is necessary to identify bioactive molecules that have the effect of repelling or killing disease-transmitting vectors (Athuman et al., 2016).
Plant parts studied for their repellant content were the roots, stems, leaves, and flowers. Research on protecting from the bites of A. aegypti, Anopheles minimus Theobald, and Culex quinquefasciatus Say using essential oils showed different responses from mosquito species. The group of plant essential oils used was Zingiber cassumunar Roxb. (Zingiberaceae), Ocimum basilicum L. (Lamiaceae), and Cymbopogon nardus L. (Poaceae). These three essential oils are effective as repellents and food inhibitors against A. minimus, C. quinquefasciatus, and A. aegypti. However, the period of protection against A. Aegypti is lower than other mosquito species (Phasomkusolsil and Soonwera, 2010). The Z. cassumunar essential oil consists of sabinene, b-pinene, caryophyllene oxide, and caryophyllene (Bhuiyan et al., 2008). In the basil leaf extract of O. basilicum, the active compounds are flavonoids, saponins, tannins, and essential oils, which are considered toxic to mosquitoes (Ramayanti et al., 2017). The stems and leaves of citronella contain a toxin, and that substance can act as a repellant (Arcani et al., 2017). Essential oil Z. cassumunar was tested at several concentrations showing that the higher the concentration, the higher the activity to repel mosquitoes (Yulianis et al., 2018).
Volatile oils from four plant species Curcuma longa L. (Zingiberaceae), Citrus hystrix DC. (Rutaceae), Cymbopogon winterianus Jowitt, and Ocimum americanum added with 5% the vanillin showed a repellent effect against A. aegypti, Anopheles dirus Peyton & Harrison, and C. quinquefasciatus. The volatile oils of turmeric, lemongrass, and basils were able to repel the three mosquito types for 8 hours, while the kaffir lime oil was effective in repelling mosquitoes for up to 3 hours (Tawatsin et al., 2001). One of the plants that contain biologically active ingredients and can be used as an alternative controller is turmeric. The essential oils of turmeric can be used as natural insecticides to replace chemicals to kill mosquito larvae. In addition, the essential oil is also effective as a mosquito repellent for Aedes (Aseptianova, 2019). The essential oil content in kaffir lime leaves is citronellal, citronellol, linalool, and geraniol compounds (Munawaroh and Astuti, 2010). The largest components produced in citronella oil are citronellal, citronellol, and geraniol (Eden et al., 2018). The components of basil oil (O. americanum) are linalool, neral, citral, β-caryophyllene, α-humulene, and germacrene-d (Hapsari and Feroniasanti, 2019). The compounds contained in all the plants above have the potential and act as mosquito repellents and larvicides.
Figure 2. Plant families found in study area. [Click here to view] |
Figure 3. Category of habitus plants in study are. [Click here to view] |
Table 1. Families of plants that have the potential dengue vector control in the tsunami area settlement of Banda Aceh City. [Click here to view] |
Figure 4. Families of plants that have the potential dengue vector control in study area. [Click here to view] |
The community has traditionally used Tagetes minuta L. (Asteraceae) to repel mosquitoes. The essential oil from T. minuta showed the presence of limonene, camphene, and verbenone as the main constituents. The essential oil of T. minuta is effective in repelling mosquitoes (Athuman et al., 2016). Mentha piperita L. (Lamiaceae) oil has potential as a larvicidal and repellant of A. aegypti (Manh and Tuyet, 2020). The M. piperita oil contains pulegone, menthone, menthol, carvone, 1,8-cineole, limonene, and β-caryophyllene (Singh and Pandey, 2018). The study of the potential of O. Americanum and Blumea alata (D.Don) DC. (Asteraceae) extracts as a source of mosquito repellent showed that O. Americanum gave 100% repellency for 1.5 hours, B. alata for 2 hours, and a mixture of O. Americanum and Blumea alata for 2.5 hours. The O. Americanum extract contains linalool, neral, citral, isocaryophyllene, and humulent, while B. alata contains terpinene-4-ol, germacrene-D, sabinene, and terpinene. The compound components contained in both types of plants potentially have mosquito protection power (Kazembe et al., 2012). The addition of the concentration of Evodia suaveolens Scheff (Rutaceae) essential oil increases the protection power as a repellant. The addition of 1.5 ml of E. suaveolens essential oil has 81% protection against A. aegypti. The ingredients in Evodia leaves are linalool, and pinene can repel mosquitoes such as A. aegypti, which causes DHF (Simaremare et al., 2017).
The infusion of the leaves of the fragrant Pandanus amaryllifolius Roxb. (Pandanaceae) has the power to repel the laying of the eggs of the Aedes spp. The optimum concentration effective for repelling mosquito eggs is in the range of 4.5 to 5 ml/l. Pandanus leaves have a fragrant aroma that affects preventing oviposition against Aedes spp. The contents of compounds in Pandanus are alkaloids, saponins, flavonoids, tannins, and polyphenols (Cahyadi et al., 2016). Illicium verum Hook.f. (Illiciaceae) contains an essential oil that can be used as a repellent of A. aegypti. The results showed that the clove flower essential oil at concentrations of 10%, 20%, 30%, 40%, and 50% was able to protect against the bites of A. aegypti for 1–2 hours. The contents of the essential oil of the clove flower are cineole, linalool, and limonene. The clove flower extract contains the linalool compound that has mosquito repellent properties from the distinctive aroma it produces. The linalool compound is a kind of stable alkali. The clover flower oil often is used as a fragrance for soaps and perfumes. Mosquitoes do not like the aroma of the clove flower essential oil and linalool compounds because they cause irritation to the mosquito’s body parts and damage the mosquito’s nervous system (Lestari et al., 2019). The Pogostemon cablin Benth (Lamiaceae) oil has major (patchouli alcohol) and minor (patchoulen, guaien, sychellen, and caryophyllene) components. These minor components can potentially act as repellants or as attractants to insects. The activity of Culex sp. using patchouli oil showed that the repellency activity had better protection than synthetic DEET (Nidianti et al., 2014).
Insect bioassay results showed that the essential oil and extract of Nepeta parnassica Heldr & Sart (Lamiaceae) were highly active against Aedes cretinus Edwards and Culex pipiens L. The protective power of N. parnassica extracts against A. cretinus was for 3 hours, while for C. pipiens the protective power was up to 2 hours after application. Analysis essential oil N. parnassica, dominated by oxygenated monoterpenes, 4aα,7α,7aβ-nepetalactone, 1,8-cineole, dichloromethane-methanol, and 4aα,7β,7aβ-nepetalactone as the main constituents. The content of dichloromethane-methanol and 4aα,7α,7aβ-nepetalactone isolated from N. parnassica showed very high mosquito repellency for at least 2 hours against both types of mosquitoes. This study demonstrated the potential use of essential oil extracts, especially dichloromethane-methanol and 4aα,7α,7aβ-nepetalactone N. parnassica, as control agents for A. cretinus and C. pipiens (Gkinis et al., 2014).
The Angelica sinensis Oliv. (Apiaceae) extract has potential as a repellent against female A. aegypti. The results of the GC-MS analysis revealed that the A. sinensis extract contains at least 21 phytochemical compounds, and the main constituent is 3-N-butylphthalide. The protective power of the A. sinensis extract provides an average protection time of 2.0–6.5 hours against A. aegypti. The combination of A. sinensis extracts with 5% vanillin can increase to 4.0–8.5 hours (Champakaew et al., 2016).
Potential of houses yard plants as attractant of Aedes spp.
One of the effective biological control strategies is necessary to do by finding and identifying attractant compounds produced by plants. Attractive flowers, intense aromas, and nectar content need to find metabolites that attract or repel mosquitoes (Peach and Gries, 2020). If plant-based chemicals can be identified, especially those from plants that are attractive to mosquitoes, these plants can serve as bait in mosquito control and surveillance programs (Nyasembe et al., 2012). Each mosquito species has a particular preference for plant sources of nutrients. Mosquitoes can detect general and plant-specific chemical cues within their ecological range. The ability of mosquitoes to detect chemical compounds in certain plants will find suitable host plants for them. The interaction of mosquitoes with plants provides information on mosquito control strategies that target plant-eating behavior like attractive toxic sugar baits and the resulting odor (Nyasembe et al., 2018).
The volatile compound released by the host plant is attractive to mosquitoes. This compound attracts both male and female mosquitoes. Mosquitoes prefer volatile compounds produced by plants; for example, A. gambiae can detect certain chemical compounds from plants (Pachuwah, 2016). The visual appearance of flowers and the volatile compounds released by them are cues for mosquitoes to distinguish and locate host plants. Some species of mosquitoes, such as A. gambiae, C. Pipiens, and A. aegypti, can detect and respond to certain compounds from plants and detect and respond to volatile compounds from plants. Flower volatile organic compounds are mainly composed of four chemical groups: aromatics, monoterpenes, sesquiterpenes, and fatty acid derivatives (Yu et al., 2015).
Female A. aegypti prefer ovitrap with jenu [Derris elliptica (Wall.) Benth.] leaf extract to lay their eggs compared to other ovitraps. This plant from the Fabaceae family has the potential to be an attractant to A. aegypti in the oviposition process. Methyl eugenol compounds such as sex pheromones are effective at attracting insects and influencing insect behavior, such as searching for a mate, searching for food, and laying eggs. Visual and olfactory integration affects oviposition search media behavior, but the olfactory signal is more influential than visuals. The olfactory organ of the mosquito is the sensilla (hair), and these spread all over its body surface. Sensilla are mostly in many mosquito antennae, and this organ is sensitive to the smell of chemical compounds (Wibowo and Astuti, 2015).
Analysis of the extract of Silene otitis L. (Caryophyllaceae) using gas chromatography-mass spectrometry identified 35 compounds. Most of the extract compounds are monoterpenoids, fatty acid derivatives, and benzene. Phenyl acetaldehyde was the most dominant compound found in S. otites flowers. The test results of a mixture of S. otites flower aroma extract compounds on male and female Cx. pipiens showed different responses. Oxide compounds linalool (furanoids) and linalool showed strong responses in male and female mosquitoes. The compound (Z)-3-hexenyl acetate had positive responses only from female mosquitoes. Male mosquitoes showed moderate responses to compound (Z)-3-hexenyl acetate. Female mosquitoes have a moderate reaction to benzaldehyde and methyl salicylate compounds. Meanwhile, the lilac aldehyde, lilac alcohol, and linalool oxide (pyranoid) compounds had moderate responses from both sexes of mosquitoes (Jhumur et al., 2008).
The extract Asclepias syriaca L. (Asclepiadaceae) showed significant orientation of male and female Cx. pipiens. The mixture compounds of benzaldehyde, phenylacetaldehyde, and (E)-2-nonenal most attracted mosquito responses. Therefore, we recommend further research to examine the potential use of synthetic floral scent mixtures for monitoring or controlling disease-transmitting mosquitoes (Otienoburu et al., 2012). The maize/Zea mays L. (Poaceae) crop contributes to the prevalence of malaria mosquitoes and exacerbates malaria transmission in sub-Saharan Africa. Pollen from corn serves as a food source for Anopheles larvae and imago. Female mosquitoes can detect breeding sites where corn pollen is abundant. The Anopheles mosquito uses olfactory cues to locate, distinguish, and select breeding sites by utilizing volatile compounds to guide it. The pollen is a source of energy and attractant mosquitoes. Pollen contains pinene, limonene, p-cymene, nonanal, and benzaldehyde compounds (Wondwosen et al., 2017).
The selections of the oviposition site strongly influence the reproductive success and population dynamics of Anopheles, a vector for malaria in female mosquitoes. Mosquitoes choose oviposition sites at different spatial scales, starting with selecting the habitat to search. Anopheles arabiensis Patton larvae were the most common species found in various grassy habitats. The highest larva density in habitats was found overgrown by Echinochloa pyramidalis (Lam.) Hitchc. & Chase (Poaceae). This condition caused the volatile compounds of E. pyramidalis grass to be more attractive than Typha (Typhaceae) and Cyperus (Cyperaceae). The preference is shown by Anopheles coluzzii Coetzee & Wilkerson and A. arabiensis prove volatile grass compounds in larval habitat vegetation have an effect in the selection of oviposition sites (Asmare et al., 2017).
CONCLUSION
This study shows that various house yard plants have secondary metabolites that have the potential to control adult Aedes. Plants in the tsunami settlement area of Banda Aceh City contain secondary metabolites that function as repellents and attractants of adult Aedes. However, further testing is necessary in the laboratory to ensure Aedes’ preference for plants in the yard and the secondary metabolite content of each plant. This research information can be an alternative to Aedes control and elimination. Plants in the house yard in the tsunami settlement area of Banda Aceh City have the potential to be used as a strategy for controlling disease-transmitting vectors.
ACKNOWLEDGMENTS
The authors express their deepest gratitude to the volunteer team “Jumantik instar 3 UINAR” and the residents of the Asoe Nanggroe Village, Meuraxa Subdistrict, and Rukoh Village, Syiah Kuala Subdistrict, in the tsunami area of Banda Aceh City.
AUTHORS’ CONTRIBUTIONS
All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work. All the authors are eligible to be an author as per the international committee of medical journal editors (ICMJE) requirements/guidelines.
FUNDING
This research was supported by the MoRA Scholarship for Islamic Higher Education (MoRA -SIHE).
CONFLICTS OF INTEREST
The authors declare that there are no conflicts of interest.
ETHICAL APPROVALS
This study does not involve experiments on animals or human subjects.
DATA AVAILABILITY
All data generated and analyzed are included within this research article.
PUBLISHER’S NOTE
This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.
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