Larval habitats of the Anopheles farauti and Anopheles lungae complexes in the Solomon Islands

Malaria Journal, Mar 2016

Background There is an urgent need for vector control tools to supplement long-lasting insecticidal nets (LLINs) and indoor residual spraying; particularly in the Solomon Islands where the primary vector, Anopheles farauti, is highly anthropophagic and feeds mainly outdoors and early in the evening. Currently, the only supplementary tool recommended by the World Health Organization is larval source management (LSM). The feasibility and potential effectiveness of LSM requires information on the distribution of anophelines, the productivity of larval habitats and the potential impacts of larval control on adult fitness. Methods The distribution of anophelines in Central and Western Provinces in the Solomon Islands was mapped from cross-sectional larval habitat surveys. The composition and micro-distribution of larval instars within a large permanent river-mouth lagoon was examined with a longitudinal survey. Density-dependent regulation of An. farauti larvae was investigated by longitudinally following the development and survival of different densities of first instars in floating cages in a river-mouth lagoon. Results Five anopheline species were molecularly identified from a range of fresh and brackish water habitats: An. farauti s.s., An. hinesorum, An. lungae, An. nataliae and An. solomonis. The most common habitats used by the primary malaria vector, An. farauti, were coastal lagoons and swamps. In the detailed study of lagoon micro-productivity, An. farauti was non-uniformly distributed with highest densities found at collections sites most proximal and distal to the mouth of the lagoon. The survival of An. farauti larvae was more than twofold lower when larvae were held at the highest experimental density (1 larva per 3.8 cm 2 ) when compared with the lowest density (1 larva per 38 cm 2 ). Conclusions The only documented major malaria vector collected in larval surveys in both Central and Western Provinces was An. farauti. Lagoons and swamps, the most common, largest and (potentially) most productive larval sites of this malaria vector, were “few, fixed and findable” and theoretically, therefore, amenable to successful LSM. However, the immense scale and complexity of these ecosystems in which An. farauti larvae are found raises questions regarding the ability to effectively control the larvae, as incomplete larviciding could trigger density dependent effects resulting in increased larval survivorship. While LSM has the potential to significantly contribute to malaria control of this early and outdoor biting vector, more information on the distribution of larvae within these extensive habitats is required to maximize the effectiveness of LSM.

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Larval habitats of the Anopheles farauti and Anopheles lungae complexes in the Solomon Islands

Malaria Journal Russell et al. Malar J (2016) 15:164 DOI 10.1186/s12936-016-1196-7 Open Access RESEARCH Larval habitats of the Anopheles farauti and Anopheles lungae complexes in the Solomon Islands Tanya L. Russell1* , Thomas R. Burkot1, Hugo Bugoro2, Allan Apairamo2, Nigel W. Beebe3,4, Weng K. Chow5, Robert D. Cooper5, Frank H. Collins6 and Neil F. Lobo6 Abstract Background: There is an urgent need for vector control tools to supplement long-lasting insecticidal nets (LLINs) and indoor residual spraying; particularly in the Solomon Islands where the primary vector, Anopheles farauti, is highly anthropophagic and feeds mainly outdoors and early in the evening. Currently, the only supplementary tool recommended by the World Health Organization is larval source management (LSM). The feasibility and potential effectiveness of LSM requires information on the distribution of anophelines, the productivity of larval habitats and the potential impacts of larval control on adult fitness. Methods: The distribution of anophelines in Central and Western Provinces in the Solomon Islands was mapped from cross-sectional larval habitat surveys. The composition and micro-distribution of larval instars within a large permanent river-mouth lagoon was examined with a longitudinal survey. Density-dependent regulation of An. farauti larvae was investigated by longitudinally following the development and survival of different densities of first instars in floating cages in a river-mouth lagoon. Results: Five anopheline species were molecularly identified from a range of fresh and brackish water habitats: An. farauti s.s., An. hinesorum, An. lungae, An. nataliae and An. solomonis. The most common habitats used by the primary malaria vector, An. farauti, were coastal lagoons and swamps. In the detailed study of lagoon micro-productivity, An. farauti was non-uniformly distributed with highest densities found at collections sites most proximal and distal to the mouth of the lagoon. The survival of An. farauti larvae was more than twofold lower when larvae were held at the highest experimental density (1 larva per 3.8 cm2) when compared with the lowest density (1 larva per 38 cm2). Conclusions: The only documented major malaria vector collected in larval surveys in both Central and Western Provinces was An. farauti. Lagoons and swamps, the most common, largest and (potentially) most productive larval sites of this malaria vector, were “few, fixed and findable” and theoretically, therefore, amenable to successful LSM. However, the immense scale and complexity of these ecosystems in which An. farauti larvae are found raises questions regarding the ability to effectively control the larvae, as incomplete larviciding could trigger density dependent effects resulting in increased larval survivorship. While LSM has the potential to significantly contribute to malaria control of this early and outdoor biting vector, more information on the distribution of larvae within these extensive habitats is required to maximize the effectiveness of LSM. Keywords: Solomon Islands, Malaria, Anopheles farauti, Species distribution, Density dependent development *Correspondence: 1 Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD 4870, Australia Full list of author information is available at the end of the article © 2016 Russell et al. 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. Russell et al. Malar J (2016) 15:164 Background The Solomon Islands is currently implementing countrywide intensified malaria control using universal distribution of long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS). Unfortunately, the main malaria vector in the Solomon Islands, Anopheles farauti, displays behavioural resistance to indoor vector control by blood feeding predominantly when people are outdoors [1]. This behavioural shift first occurred in response to IRS with DDT in the 1970s [2, 3] and has persisted in the Solomon Islands with LLINs being the primary malaria vector control strategy [4–7]. Despite the early and outdoor biting behaviour of An. farauti, LLINs and IRS have had a significant impact on malaria transmission. However, achieving malaria elimination will require additional vector control to minimize outdoor transmission. The only outdoor strategy recommended by the World Health Organization is larval source management (LSM) [8] and this has the potential to limit transmission both indoors and outdoors. Larval source management is only recommended in areas where the larval habitats are few in number, fixed in location and easily accessible [9]. To ascertain the feasibility of implementing LSM in the Solomon Islands, information on the types of larval habitats utilized by vectors including their location in proximity to villages is needed. Nine species of anophelines occur in the Solomon Islands: six members of the An. punctulatus group: An. farauti, An. irrenicus, An. hinesorum, An. punctulatus, An. koliensis and An. rennellensis [10, 11]; as well as three members of the An. lungae complex: An. lungae, An. solomonis and An. nataliae [12]. Of these, the only known malaria vectors in the Solomon Islands are An. farauti, An. punctulatus and An. koliensis. Anopheles punctulatus and An. koliensis became uncommon after IRS with DDT was extensively used for malaria vector control tool in the 1970s [13]. Larvae of An. farauti, are found within a kilometre of the coast in both fresh and brackish water (≥70 % seawater) [14, 15]. Freshwater larval habitats of An. farauti include both natural and man-made depressions such as drains, vehicle tracks, foot prints, pig wallows and ground-pools [5, 16] that are dependent on rainfall [17, 18]. Large numbers of An. farauti are believed to be associated with large, permanent, brackish water lagoons or swamps that form behind sandbars that block the flow of water into the sea [17–19] as high adult biting densities and malaria parasite rates are associated with villages proximal to these coastal habitats [20, 21]. The population dynamics of mosquitoes are influenced by both intrinsic and exogenous processes [22–25]. If density effects operate on mosquito larvae in large larval habitats, the impact of interventions targeting anopheline larval abundance will be disproportionate to the density of the Page 2 of 9 anopheline populations’ (linear reductions in populations may not result in linear redu (...truncated)


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Tanya Russell, Thomas Burkot, Hugo Bugoro, Allan Apairamo, Nigel Beebe, Weng Chow, Robert Cooper, Frank Collins, Neil Lobo. Larval habitats of the Anopheles farauti and Anopheles lungae complexes in the Solomon Islands, Malaria Journal, 2016, pp. 164, 15, DOI: 10.1186/s12936-016-1196-7