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Using Barrier Screens to Characterize Mosquito Composition, Flight Activity, and Abdominal Status in South Lampung, Indonesia Jenna R

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Using Barrier Screens to Characterize Mosquito Composition, Flight Activity, and Abdominal Status in South Lampung, Indonesia Jenna R Davidson et al. Parasites & Vectors (2018) 11:440 https://doi.org/10.1186/s13071-018-3031-1 RESEARCH Open Access Using barrier screens to characterize mosquito composition, flight activity, and abdominal status in South Lampung, Indonesia Jenna R. Davidson1*†, Supratman Sukowati2†ˆ, Shinta2, Puji Budi Setia Asih3, Din Syafruddin3, Robert N. Baskin1, Brandy St. Laurent1, William A. Hawley4, Fang Liu1, Thomas R. Burkot5, Frank H. Collins1 and Neil F. Lobo1* Abstract Background: Mosquito sampling methods target different aspects of mosquito behavior and are subject to trap and location specific biases. The barrier screen sampling method was developed and tested to sample free-flying, blood-fed, and host-seeking mosquitoes. During a pilot study, this method was useful in obtaining an unbiased sample of mosquitoes flying between outdoor larval habitats, and sites where blood meals were obtained. However, a relatively small number of blood-fed Anopheles mosquitoes were collected in Indonesia during the pilot study. The sampling method was extended in South Lampung, Indonesia, to enable the collection of blood-fed mosquitoes. This study aimed to intercept mosquitoes flying between human habitations and larval habitats with a barrier screen and to characterize mosquito composition, flight characteristics (direction, height and time), abdominal status, and parity. Results: Barrier screens intercepted 15 different mosquito species in South Lampung: eight Anopheles spp. and seven Culex spp. Species compositions varied among the villages in South Lampung. About 15% of Anopheles spp. caught were blood-fed, of which 28.2% of those tested had fed on humans. This is the first time human blood-fed anophelines have been collected in Indonesia using barrier screens. Blood meals identified included cow, dog, goat, and human, as well as mixed blood meals. Activity of unfed An. subpictus, the primary vector collected, flying towards human habitations peaked between 20:00–12:00 h, with a slow decline in activity until 18:00 h. Unfed and fed An. sundaicus, had a different activity profile compared to An. subpictus. Other species demonstrated varied peak activity times, with earlier activity occurring as a general trend. For the Anopheles mosquitoes collected, 55.5% were collected below 0.5 m and 83.9% were captured resting < 1 m from the ground. Parity dissections enabled age structure by species, which revealed species-specific traits such as nulliparous An. subpictus being more active early in the night relative to An. sundaicus. Conclusions: This study demonstrates that barrier screens are an effective mosquito sampling method that can be used to gain insights into local mosquito species composition, flight characteristics (direction, height and time), abdominal status, and parity. Keywords: Anopheles, Barrier screens, Bionomics, Culex * Correspondence: [email protected]; [email protected] †Jenna R. Davidson and Sukowati Supratman contributed equally to this work. ˆDeceased 1Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556, USA Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Davidson et al. Parasites & Vectors (2018) 11:440 Page 2 of 11 Background Spatial and temporal information regarding mosquito Malaria is transmitted by Anopheles mosquitoes; this populations can be gathered with relatively limited effort genus includes 465 recognized species and more - an advantage the barrier screen provides compared to unidentified members of species complexes [1]. For- other methods, which may require significant time and ty-one of these species are considered dominant malaria effort in exchange for a low rate of return and limited vectors [2, 3]. Besides being a ubiquitous biting nuisance, directional data [27]. Barrier screens provide an easy and Culex mosquitoes transmit several arboviral diseases and economical way to collect mosquitoes and gather infor- filarial worms [4–8]. Interventions such as long-lasting in- mation about flight time, direction, and height. The pilot secticidal nets (LLINs) and indoor residual spraying (IRS) study in Indonesia, Solomon Islands, and Papua New are often applied regardless of the local vector bionomics, Guinea [14] concluded that the barrier screen trapping even though intervention efficacy depends on mosquito be- method is sufficient to detain and allow the collection of havior. For example, both LLINs and IRS reduce malaria mosquitoes, especially those with exophilic behaviors. transmission by targeting primarily indoor biting and in- However, the study had a limited amount of collection door resting mosquitoes [9–11], and are therefore subopti- nights and caught few blood-fed anophelines, none of mal intervention strategies for outdoor-biting mosquitoes. which had human blood meals in Indonesia [14]. Understanding species compositions, their bionomic char- In this study, the barrier screen sampling method was acteristics, and their potential susceptibility to intervention extended to four villages in South Lampung, Sumatra. strategies is fundamental to effective disease control. Mosquitoes flying between human habitations and larval Sampling methods have limitations and biases in the habitats were intercepted by a barrier screen and charac- context of specific behaviors of mosquitoes [12–18]. Al- terized for species composition, flight characteristics though human landing catches (HLCs) [19] are the gold (direction, height and time), abdominal status, and par- standard for trapping female, human-biting Anopheles, ity. This study included both Anopheles and Culex mos- they do have several limitations. In addition to ethical quitoes. The aims of this study are to (i) further concerns [20], it is impossible to use HLCs to discern characterize Anopheles and Culex species compositions the rate of human feeding without a using a second in Lampung, Indonesia; (ii) assess information about trapping method. Furthermore, HLCs only partially species’ abdominal status, activity time, height of activity, characterize primarily zoophilic or zoophagic species’ and flight direction as determined by barrier screens; behaviors, which may only be captured through HLCs if (iii) evaluate barrier screens for use in sampling a coincidental opportunistic feeding event occurs. Al- blood-fed mosquitoes outdoors in Indonesia. Lastly, this though efforts to develop a substitute, exposure-free trap study is the first evaluation of implementing barrier are ongoing (e.g. the Ifakara tent trap [21, 22] and the screens to gather information regarding flight direction Electric Grid [23]), none have been found to be compar- into the village from the larval habitat and out of the vil- able to HLCs. Moreover, none of these sampling lage towards the larval habitat. methods (including HLCs) assess the flight direction of mosquitoes with respect to human habitation [22, 24]. Methods There is a need for a method that efficiently samples Study sites mosquitoes outdoors while investigating flight direction. Barrier screen collections took place in four coastal vil- Data on chronological and spatial variances in mosquito lages in the Lampung District of southern Sumatra, in activities, such as the peaks and bases in activity, are a western Indonesia. Local industries include fishing and prerequisite to implement appropriate interventions for shrimp/fish farming. Houses are generally constructed the reduction of disease transmission. Further complicat- with brick or wood and plaster, tiled roofs, and screens on ing the understanding of intervention efficacy, mosquito some windows and eaves. This area has low to intermedi- populations may exhibit behavioral resistance in re- ate malaria endemicity that is seasonal and coincident sponse to control strategies. Behavioral resistance is de- with the rainy season (October to March). Mosquito col- fined as any alteration in behavior that aids evasion of lections took place over 39 nights (8 nights in Lempasing, insecticides [25, 26]. Studying behavioral changes and 10 in Sidodadi, 2 in Hanura, and 19 in Sukaraja villages) other adaptations in vectors [27–30] is becoming more in 2010 and 2011 (Table 1). At each study site, one 10 m vital with the push towards malaria elimination. Due to long barrier screen was utilized per collection night. the lack of unbiased sampling methods for mosquitoes outdoors, the study of vector behavioral resistance re- Barrier screen construction and location mains a significant challenge for researchers. Barrier screens were constructed with grey, 2 m high The barrier screen sampling method was developed polyvinylchloride coated polyester netting (http:// and evaluated successfully [14] to sample free-flying, www.botexsales.com/) secured to wooden poles at 2 m blood-fed, and host-seeking mosquitoes outdoors. intervals for a length of 10 m. Barrier screen mesh was Davidson et al. Parasites & Vectors (2018) 11:440 Page 3 of 11 Table 1 Barrier
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