Zika virus does not alter locomotor activity of Aedes albopictus (Diptera: Culicidae)

Tamara Nunes Lima-Camara; Pâmela dos Santos Andrade; Vivian Petersen; Antônio Ralph Medeiros-Sousa; Anderson Vicente de Paula; Paulo Roberto Urbinatti; Rosa Maria Marques de Sá Almeida

doi:10.11606/s15188787.2025059006968

Authors

Tamara Nunes Lima-Camara Universidade de São Paulo. Faculdade de Saúde Pública. Departamento de Epidemiologia. São Paulo, SP, Brazil https://orcid.org/0000-0003-3133-8592
Pâmela dos Santos Andrade Universidade de São Paulo. Faculdade de Saúde Pública. Programa de Pós-Graduação em Saúde Pública. São Paulo, SP, Brazil https://orcid.org/0000-0001-5213-7592
Vivian Petersen University of Florida. Florida Medical Entomology Laboratory. Vero Beach, FL, United States of America https://orcid.org/0000-0003-1045-7381
Antônio Ralph Medeiros-Sousa Universidade de São Paulo. Faculdade de Saúde Pública. Departamento de Epidemiologia. São Paulo, SP, Brazil https://orcid.org/0000-0002-9493-8731
Anderson Vicente de Paula Universidade de São Paulo. Instituto de Medicina Tropical. Laboratório de Virologia. São Paulo, SP, Brazil https://orcid.org/0000-0002-7919-3516
Paulo Roberto Urbinatti Universidade de São Paulo. Faculdade de Saúde Pública. Departamento de Epidemiologia. São Paulo, SP, Brazil https://orcid.org/0000-0001-5757-9576
Rosa Maria Marques de Sá Almeida Universidade de São Paulo. Faculdade de Saúde Pública. Departamento de Epidemiologia. São Paulo, SP, Brazil https://orcid.org/0009-0002-4394-8371

DOI:

https://doi.org/10.11606/s15188787.2025059006968

Keywords:

Aedes albopictus, Zika Virus, Locomotor Activity, Infection

Abstract

OBJECTIVE: To investigate the effect of Zika virus on the locomotor activity of a Brazilian population of Aedes albopictus under laboratory conditions. METHODS: Females of Aedes albopictus were infected with Zika virus orally or by intrathoracic injection. The locomotor activity was monitored using a Drosophila activity monitor under controlled conditions of 25°C and a 12h light/dark cycle. The infection status was determined using reverse transcription followed by real-time polymerase chain reaction (RT-qPCR). Statistical analyses were conducted using generalized linear mixed models (GLMMs). RESULTS: The locomotor activities of Zika virus-infected and uninfected Aedes albopictus females were diurnal and bimodal, with peaks at lights on and off. The infection did not significantly alter the total activity, diurnal and nocturnal, or the light-on and light-off peaks of infected females compared with uninfected females, regardless of the method of infection (intrathoracic injection or orally). CONCLUSION: This finding indicates that Zika virus infection does not affect the daily activity pattern of this species under laboratory conditions, which reinforces the importance of this species as a competent and adaptable vector in urban and rural areas, confirming the importance of ongoing surveillance and control strategies.

References

Lounibos LP, Kramer LD. Invasiveness of Aedes aegypti and Aedes albopictus and Vectorial Capacity for Chikungunya Virus. J Infect Dis. 2016 Dec;214(suppl 5):S453–8. https://doi.org/10.1093/infdis/jiw285

Lima-Camara TN. Emerging arboviruses and public health challenges in Brazil. Rev Saúde Pública. 2016 Mar; 50:36. https://doi.org/10.1590/S1518-8787.2016050006791

Hawley WA. The biology of Aedes albopictus. J Am Mosq Control Assoc Suppl. 1988 Dec;1:1–39.

Garamszegi LZ. Host diversity of Aedes albopictus in relation to invasion history: a meta-analysis of blood-feeding studies. Parasites Vectors. 2024 Oct;17(1):411. https://doi.org/10.1186/s13071-024-06490-4

Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D. Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes and Infection. 2009 Dec;11(14–15):1177–85. https://doi.org/10.1016/j.micinf.2009.05.005

Giunti G, Becker N, Benelli G. Invasive mosquito vectors in Europe: From bioecology to surveillance and management. Acta Tropica. 2023 mar;239:106832. https://doi.org/10.1016/j.actatropica.2023.106832

Veronesi E, Paslaru A, Ettlin J, Ravasi D, Flacio E, Tanadini M, Guidi V. Estimating the Impact of Consecutive Blood Meals on Vector Competence of Aedes albopictus for Chikungunya Virus. Pathogens. 2023 jun;12(6):849. https://doi.org/10.3390/pathogens12060849

Damasceno-Caldeira R, Nunes-Neto JP, Aragão CF, Freitas MNO, Ferreira MS, Castro PHGD, et al. Vector Competence of Aedes albopictus for Yellow Fever Virus: Risk of Reemergence of Urban Yellow Fever in Brazil. Viruses. 2023;15(4):1019. https://doi.org/10.3390/v15041019

Fortuna C, Severini F, Marsili G, Toma L, Amendola A, Venturi G, et al. Assessing the Risk of Dengue Virus Local Transmission: Study on Vector Competence of Italian Aedes albopictus. Viruses. 2024;16(2):176. https://doi.org/10.3390/v16020176

Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, et al. Chikungunya Virus in Aedes albopictus, Italy. Emerg Infect Dis. 2008;14(5):852–4. https://doi.org/10.3201/eid1405.071144

Grandadam M, Caro V, Plumet S, Thiberge J, Souarès Y, Failloux A, et al. Chikungunya Virus, Southeastern France. Emerg Infect Dis. 2011;17(5):910-13. https://doi.org/10.3201/eid1705.101873

Grard G, Caron M, Mombo IM, Nkoghe D, Mboui Ondo S, Jiolle D, et al. Zika Virus in Gabon (Central Africa) – 2007: A New Threat from Aedes albopictus? PLoS Negl Trop Dis. 2014 Feb 6;8(2):e2681. https://doi.org/10.1371/journal.pntd.0002681

Rocha RC, Cardoso AS, Souza JL, Pereira ES, Amorim MF, Souza MSM, et al. First official record of Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the Acre State, Northern Brazil. Rev Inst Med Trop S Paulo. 2023;65:e20. https://doi.org/10.1590/S1678-9946202365020

Castro MG, Nogueira RMR, Schatzmayr HG, Miagostovich MP, Lourenço-de-Oliveira R. Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz [internet]. 2004 Dec;99(8):809–14. https://doi.org/10.1590/S0074-02762004000800005

Chouin-Carneiro T, Vega-Rua A, Vazeille M, Yebakima A, Girod R, Goindin D, et al. Differential Susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika Virus. PLoS Negl Trop Dis. 2016 Mar;10(3):e0004543. https://doi.org/10.1371/journal.pntd.0004543

Ferreira-de-Lima VH, Câmara DCP, Honório NA, Lima-Camara TN. The Asian tiger mosquito in Brazil: Observations on biology and ecological interactions since its first detection in 1986. Acta Tropica. 2020 May;205:105386. https://doi.org/10.1016/j.actatropica.2020.105386

Rezende HR, Romano CM, Claro IM, Caleiro GS, Sabino EC, Felix AC, et al. First report of Aedes albopictus infected by Dengue and Zika virus in a rural outbreak in Brazil. PLOS ONE. 2020 Mar;15(3):e0229847. https://doi.org/10.1371/journal.pone.0229847

Pancetti FGM, Honório NA, Urbinatti PR, Lima-Camara TN. Twenty-eight years of Aedes albopictus in Brazil: a rationale to maintain active entomological and epidemiological surveillance. Rev Soc Bras Med Trop. 2015 Jan; 48(1):87–9. https://doi.org/10.1590/0037-8682-0155-2014

Lima-Camara TN. Activity patterns of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) under natural and artificial conditions. Oecol Austr. 2010 Sept;14(3):737–44. https://doi.org/10.4257/oeco.2010.1403.09

Lima-Camara TN, Lima JBP, Bruno RV, Peixoto AA. Effects of insemination and blood-feeding on locomotor activity of Aedes albopictus and Aedes aegypti (Diptera: Culicidae) females under laboratory conditions. Parasites Vectors. 2014 Jul;7(304):1–8. https://doi.org/10.1186/1756-3305-7-304

Lima-Camara TN, Bruno RV, Luz PM, Castro MG, Lourenço-de-Oliveira R, Sorgine MHF, et al. Dengue Infection Increases the Locomotor Activity of Aedes aegypti females. PLoS ONE. 2011 Mar;6(3):e17690. https://doi.org/10.1371/journal.pone.0017690

Padilha KP, Resck MEB, Cunha OAT, Teles-de-Freitas R, Campos SS, Sorgine MHF, et al. Zika infection decreases Aedes aegypti locomotor activity but does not influence egg production or viability. Mem Inst Oswaldo Cruz. 2018;113(10):e180290. https://doi.org/10.1590/0074-02760180290

Tallon AK, Lorenzo MG, Moreira LA, Martinez Villegas LE, Hill SR, Ignell R. Dengue infection modulates locomotion and host seeking in Aedes aegypti. PLoS Negl Trop Dis. 2020 Sept;14(9):e0008531. https://doi.org/10.1371/journal.pntd.0008531

Diehlmann H. Laboratory Rearing of Mosquitoes Using a Hemotek Feeding System. Hronov: Czech Republic Grafické závody; 1999.

Lima-Camara TN, Medeiros-Sousa AR, Coelho RR, Marrelli MT. Body size does not affect locomotor activity of Aedes aegypti and Aedes albopictus females (Diptera: Culicidae). Acta Tropica. 2022 Jul;231:106430. https://doi.org/10.1016/j.actatropica.2022.106430

Patel P, Landt O, Kaiser M, Faye O, Koppe T, Lass U, et al. Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J. 2013 Feb;10(58):1–11. https://doi.org/10.1186/1743-422X-10-58

Williams CB. The use of logarithms in the interpretation of certain entomological problems. Annals of Applied Biology – AAB. 1937 May;24(2):404–14. https://doi.org/10.1111/j.1744-7348.1937.tb05042.x

Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith, GM. Mixed effects models and extensions in ecology with R. New York, NY: Springer; 2009.

Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Soft. 2015 Oct;67(1): 1–48. https://doi.org/10.18637/jss.v067.i01

Hrong-Tai Fai A, Cornelius PL. Approximate F-tests of multiple degree of freedom hypotheses in generalized least squares analyses of unbalanced split-plot experiments. J Stat Comput Simul. 1996 May;54(4): 363–78. https://doi.org/10.1080/00949659608811740

Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest Package: Tests in Linear Mixed Effects Models. J Stat Soft. 2017 Dec;82(13):1–26. https://doi.org/10.18637/jss.v082.i13

Feitoza TS, Ferreira-de-Lima VH, Câmara DCP, Honório NA, Lounibos LP, Lima-Camara TN. Interspecific Mating Effects on Locomotor Activity Rhythms and Refractoriness of Aedes albopictus (Diptera: Culicidae) Females. Insects. 2020 Dec;11(12):1–13. https://doi.org/10.3390/insects11120874

Nakazato BM, Macoris MLG, Urbinatti PR, Lima-Camara TN. Locomotor activity in Aedes aegypti with different insecticide resistance profiles. Rev saúde pública. 2021 Apr; 55:18. https://doi.org/10.11606/s1518-8787.2021055002809

Maia PCR, La Corte R, Pires LB, Banfield L, Logan JG, Lima-Camara TN. Increased Repellent Effect of DEET on Aedes aegypti (Diptera: Culicidae) Field Population. Journal of Medical Entomology. 2022 Jul;59(4):1368–75. https://doi.org/10.1093/jme/tjac068

Costanzo K, Occhino D. Effects of Temperature on Blood Feeding and Activity Levels in the Tiger Mosquito, Aedes albopictus. Insects. 2023 Sept;14(9):752. https://doi.org/10.3390/insects14090752

Gaburro J, Bhatti A, Harper J, Jeanne I, Dearnley M, Green D, et al. Neurotropism and behavioral changes associated with Zika infection in the vector Aedes aegypti. Emerg Microbes Infect. 2018 Apr;7(1):1–11. https://doi.org/10.1038/s41426-018-0069-2

Onyango MG, Bialosuknia SM, Payne AF, Mathias N, Kuo L, Vigneron A, et al. Increased temperatures reduce the vectorial capacity of Aedes mosquitoes for Zika virus. Emerg Microbes Infect. 2020 Jan;9(1):67–7. https://doi.org/10.1080/22221751.2019.1707125

Wang F, Yang C, Wang S, Wu Q, Ochieng C, Yuan Z, et al. Experimental Viral Infection in Adult Mosquitoes by Oral Feeding and Microinjection. JoVE. 2022 Jul;(185):e63830. https://doi.org/10.3791/63830

Zika virus does not alter locomotor activity of Aedes albopictus (Diptera: Culicidae)

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