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      Reducing the cost and assessing the performance of a novel adult mass-rearing cage for the dengue, chikungunya, yellow fever and Zika vector, Aedes aegypti (Linnaeus)

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          Abstract

          Introduction

          The widespread emergence of resistance to insecticides used to control adult Aedes mosquitoes has made traditional control strategies inadequate for the reduction of various vector populations. Therefore, complementary vector control methods, such as the Sterile Insect Technique, are needed to enhance existing efforts. The technique relies on the rearing and release of large numbers of sterile males, and the development of efficient and standardized mass-rearing procedures and tools is essential for its application against medically important mosquitoes.

          Methods

          In the effort to reduce the cost of the rearing process, a prototype low-cost plexiglass mass-rearing cage has been developed and tested for egg production and egg hatch rate in comparison to the current Food and Agriculture Organization/International Atomic Energy Agency (FAO/IAEA) stainless-steel cage. Additionally, an adult-index was validated and used as a proxy to estimate the mosquito survival rates by counting the number of male and female mosquitoes that were resting within each of the 6 squares at a given point of time each day in the cage.

          Results

          The study has shown that the prototype mass-rearing cage is cheap and is as efficient as the FAO/IAEA stainless-steel cage in terms of egg production, with even better overall egg hatch rate. The mean numbers of eggs per cage, after seven cycles of blood feeding and egg collection, were 969,789 ± 138,101 and 779,970 ± 123,042, corresponding to 81 ± 11 and 65 ± 10 eggs per female over her lifespan, in the prototype and the stainless-steel-mass-rearing cages, respectively. The longevity of adult male and female mosquitoes was not affected by cage type and, the adult-index could be considered as an appropriate proxy for survival. Moreover, the mass-rearing cage prototype is easy to handle and transport and improves economic and logistic efficiency.

          Conclusion

          The low-cost mass-rearing prototype cage can be recommended to produce Ae. aegypti in the context of rear and release techniques. The proposed adult-index can be used as a quick proxy of mosquito survival rates in mass-rearing settings.

          Author summary

          Dengue, among other arboviral infections, is a neglected disease and a major health issue that is re-emerging in tropical countries due to the poor efficacy of conventional vector control methods. Therefore, there is a growing need for more sustainable techniques to control Aedes mosquito species, while reducing the dependence on insecticides. The sterile insect technique, which relies on the mass-production of sterile males, can be used as part of area- wide integrated pest management (AW-IPM) programmes to reduce the vector population below the disease transmission threshold. Therefore, innovations in mosquito mass-rearing techniques including the development of low-cost adult holding cages are essential in the quest to promote an economical and logistically efficient mass -rearing system for the vectors of dengue, chikungunya, yellow fever and Zika diseases.

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          Most cited references32

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          Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), vectors of malaria.

          In four Anopheles species, An. albimanus, An. gambiae, An. stephensi, and An. quadrimaculatus Say, total protein, lipid, and carbohydrate present at eclosion, after feeding on sucrose, and after extreme starvation were quantified to study the effect of teneral and maximal reserves on subsequent fecundity and to judge the extent of reserve mobilization and the minimal irreducible amounts required for survival. All parameters were regressed on body size, presented as the cubic value of wing length. Teneral reserves were isometric with body size, were considerably lower than previously reported for Aedes aegypti (L.) and were sexually dimorphic with respect to reserves and body size, all being slightly reduced in males. On the average, up to 70% of the teneral female lipids and up to 50% of their teneral protein could be mobilized during nutritive stress. Conversely, access to sucrose for a few days led to a pronounced glycogenesis (up to 509%) and lipogenesis (up to 450% of the teneral values), depending on the species. In absolute terms, lipogenesis prevailed over glycogenesis. On a caloric basis, up to 30% of the blood meal protein was utilized for synthesis of yolk protein and lipid, and another 15% was deposited as an extra-ovarian, maternal protein and lipid store, perhaps compensating for the limited teneral reserves. A complete nitrogen budget revealed that in a given class of body size, roughly 80% of the blood meal protein was catabolized and excreted through the three major pathways of uricotely, ureotely, and ammonotely. Quantification of the hematin in fecal samples allowed a stoichiometrical determination of the amount of blood ingested. Eco-physiological aspects of larval feeding, teneral reserves, blood meal utilization, and possible behavioral adaptations to these physiological constraints are discussed and compared with previous data on culicine mosquitoes, stressing the invalidity of generalizations among these taxa.
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            Oviposition, dispersal, and survival in Aedes aegypti: implications for the efficacy of control strategies.

            There is compelling evidence that Aedes aegypti distributes small numbers of eggs among many sites, and that this "skip oviposition" is a driver for dispersal. The behavior is compatible with published results of mark-release-recapture studies, although many of these have been interpreted as evidence for limited dispersal. Skip oviposition also extends the duration of the gonotrophic cycle, the key parameter in the use of parous rates to estimate physiologic age. In addition, contact with multiple oviposition sites was probably a factor in the remarkable success of "perifocal" treatments with DDT in the campaign to eradicate Ae. aegypti from the Americas and the mobility of the vector probably limits the efficacy of attempts to suppress dengue transmission by source reduction and "focal" treatments with aerosols. Innovative approaches that exploit or negate this behavior may be required before effective Ae. aegypti control can become a reality.
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              Pilot field trials with Aedes albopictus irradiated sterile males in Italian urban areas.

              The pilot field studies here presented are part of a long-term research program aimed to develop a cost-effective sterile insect technique (SIT) methodology to suppress Aedes albopictus (Skuse) populations. Aedes albopictus is a mosquito species mainly developing in man-made containers and with an island-like urban and suburban distribution. These two features make the application of the sterile insect technique a possible control strategy. Five trials have been performed in three small towns from 2005 to 2009 (Emilia-Romagna region, northern Italy). Reared male pupae, sexed by a sieving technique allowing the recovery of approximately 26-29% of males, were exposed to gamma rays and immediately released in the field. Adult population density was estimated based on a weekly monitoring of egg density in the ovitraps, whereas induced sterility was estimated by measuring the hatching percentage of weekly collected eggs in SIT and control areas. Results showed that sterile males released at the rate of 896-1,590 males/ha/wk induced a significant sterility level in the local population. In addition, when the sterility level achieved values in the range of 70-80%, a similar reduction also was found for the egg density in the ovitraps. We could estimate that the minimum egg sterility value of 81% should be maintained to obtain suppression of the local population. Immigration of mated females was not a main issue in the small villages where trials have been run.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: Writing – review & editing
                Role: MethodologyRole: Writing – review & editing
                Role: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SoftwareRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: Writing – review & editing
                Role: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                25 September 2019
                September 2019
                : 13
                : 9
                : e0007775
                Affiliations
                [1 ] Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, International Atomic Energy Agency, Vienna, Austria
                [2 ] Institut de Recherche en Sciences de la Santé/Direction Régionale de l’Ouest, Bobo‑Dioulasso, Burkina Faso
                [3 ] Institut de Recherche Agricole pour le Développement, Yaoundé, Cameroun
                [4 ] Technical School of Design, Architecture and Engineering, University CEU Cardenal Herrera, Valencia, Spain
                USDA-ARS Center for Medical Agricultural and Veterinary Entomology, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-8662-4700
                http://orcid.org/0000-0002-3082-0312
                Article
                PNTD-D-18-01749
                10.1371/journal.pntd.0007775
                6779276
                31553724
                6af67ca9-459e-456c-8a1b-b31b628d1522
                © 2019 Maïga et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 November 2018
                : 11 September 2019
                Page count
                Figures: 6, Tables: 6, Pages: 21
                Funding
                Funded by: United States of America
                Award ID: The research presented in this paper was partially funded by the United States of America under the grant to the IAEA entitled: Surge expansion for the sterile insect technique to control mosquito populations that transmit the Zika virus
                The research presented in this paper was partially funded by the United States of America under the grant to the IAEA entitled: Surge expansion for the sterile insect technique to control mosquito populations that transmit the Zika virus. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Engineering and Technology
                Technology Development
                Prototypes
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Pupae
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Death Rates
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-10-07
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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