Abstract
BackgroundIn Loreto Department, Peru, a successful 2005–2010 malaria control programme (known as PAMAFRO) included massive distribution of long-lasting insecticidal nets (LLINs). Additional local distribution of LLINs occurred in individual villages, but not between 2012 and 2015. A 2011–2012 study of the primary regional malaria vector Anopheles darlingi detected a trend of increased exophagy compared with pre-PAMAFRO behaviour. For the present study, An. darlingi were collected in three villages in Loreto in 2013–2015 to test two hypotheses: (1) that between LLIN distributions, An. darlingi reverted to pre-intervention biting behaviour; and, (2) that there are separate sub-populations of An. darlingi in Loreto with distinct biting behaviour.ResultsIn 2013–2015 An. darlingi were collected by human landing catch during the rainy and dry seasons in the villages of Lupuna and Cahuide. The abundance of An. darlingi varied substantially across years, villages and time periods, and there was a twofold decrease in the ratio of exophagic:endophagic An. darlingi over the study period. Unexpectedly, there was evidence of a rainy season population decline in An. darlingi. Plasmodium-infected An. darlingi were detected indoors and outdoors throughout the night, and the monthly An. darlingi human biting rate was correlated with the number of malaria cases. Using nextRAD genotyping-by-sequencing, 162 exophagic and endophagic An. darlingi collected at different times during the night were genotyped at 1021 loci. Based on model-based and non-model-based analyses, all genotyped An. darlingi belonged to a homogeneous population, with no evidence for genetic differentiation by biting location or time.ConclusionsThis study identified a decreasing proportion of exophagic An. darlingi in two villages in the years between LLIN distributions. As there was no evidence for genetic differentiation between endophagic and exophagic An. darlingi, this shift in biting behaviour may be the result of behavioural plasticity in An. darlingi, which shifted towards increased exophagy due to repellence by insecticides used to impregnate LLINs and subsequently reverted to increased endophagy as the nets aged. This study highlights the need to target vector control interventions to the biting behaviour of local vectors, which, like malaria risk, shows high temporal and spatial heterogeneity.
Highlights
In Loreto Department, Peru, a successful 2005–2010 malaria control programme included massive distribution of long-lasting insecticidal nets (LLINs)
Primary reliance on LLINs and indoor residual spraying (IRS) for vector control has driven physiological resistance to insecticides [6, 7], and behavioural resistance or resilience. Such behavioural modifications have enhanced residual transmission, or transmission that persists despite the reduction of vector populations through control activities [8], including outdoor and non-nighttime transmission, in several malaria-endemic areas [9,10,11,12,13,14,15,16], there are counter-examples [17,18,19]. It is unclear whether shifting biting behaviour after exposure to LLINs and/or IRS is the result of genetically differentiated populations of anophelines with different feeding behaviours, or of behavioural plasticity, the ability of individuals of the same genotype to adopt different behaviour in response to different environments
If anophelines are deterred by the presence of insecticide from feeding successfully at their preferred time or location, they may continue to quest for a blood meal, shifting the overall biting behaviour of the population [13]
Summary
In Loreto Department, Peru, a successful 2005–2010 malaria control programme (known as PAMAFRO) included massive distribution of long-lasting insecticidal nets (LLINs). Over the past ~ 10 years, the most effective vector intervention has been long-lasting insecticidal nets (LLINs), which, alone or in combination with IRS, and together with rapid diagnosis and treatment and combination drug therapy, have reduced malaria such that elimination is being considered feasible [3,4,5] Despite these advances, primary reliance on LLINs and IRS for vector control has driven physiological resistance to insecticides [6, 7], and behavioural resistance or resilience (e.g., increased exophagy and early evening or daytime biting). Understanding whether distinct sub-populations of malaria vectors with different biting behaviour exist could help predict responses to vector control measures and advise vector control programmes as to the most efficient use of their resources
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