Sexual Proportion and Egg Hatching of Vector Mosquitos in an Atlantic Forest Fragment in Rio de Janeiro, Brazil
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Study Areas
2.3. Sampling Design and Egg Rearing
2.4. Statistical Analysis
3. Results
3.1. Sexual Proportion x Site and Season
3.2. Egg Immersion Event x Mosquito Species x Sex
3.3. Co-Occurrence of Mosquito Species
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Forattini, O.P. Entomologia médica. Culicini: Culex, Aedes e Psorophora|Mosquito Taxonomic Inventory; Edusp—Editora da Universidade de São Paulo: São Paulo, Brazil, 1965. [Google Scholar]
- Mittermeier, R.A.; Turner, W.R.; Larsen, F.W.; Brooks, T.M.; Gascon, C. Global Biodiversity Conservation: The Critical Role of Hotspots. In Biodiversity Hotspots; Springer: Berlin/Heidelberg, Germany, 2011; pp. 3–22. [Google Scholar]
- Didham, R.K.; Ghazoul, J.; Stork, N.E.; Davis, A.J. Insects in fragmented forests: A functional approach. Trends Ecol. Evol. 1996, 11, 255–260. [Google Scholar] [CrossRef]
- Forattini, O.P. Culicidologia Médica: Identificação, Biologia, Epidemiologia; Edusp—Editora da Universidade de São Paulo: São Paulo, Brazil, 2002. [Google Scholar]
- Alencar, J.; Fereira, Z.M.; Lopes, C.M.E.; Serra-Freire, N.M.; De Mello, R.P.; Silva, J.D.S.; Guimarães, A.É. Biodiversity and times of activity of mosquitoes (Diptera: Culicidae) in the biome of the atlantic forest in the state of Rio de Janeiro, Brazil. J. Med. Entomol. 2011, 48, 223–231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alencar, J.; De Mello, C.F.; Guimarães, A.É.; Gil-Santana, H.R.; Dos Santos Silva, J.; Santos-Mallet, J.R.; Gleiser, R.M. Culicidae community composition and temporal dynamics in Guapiaçu ecological reserve, Cachoeiras de Macacu, Rio de Janeiro, Brazil. PLoS ONE 2015, 10, 1–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marcondes, C.B.; Alencar, J. Revisão de mosquitos Haemagogus Williston (Diptera: Culicidae) do Brasil. Rev. Biomed. 2010, 21, 221–238. [Google Scholar]
- Arnell, J.H. Mosquito studies (Diptera, Culicidae). XXXII. A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst. 1973, 10, 1–174. [Google Scholar]
- Pinheiro, F.P.; Travassos Da Rosa, A.P.A.; Moraes, M.A.P.; Almeida Neto, J.C.; Camargo, S.; Filgueiras, J.P. An epidemic of yellow fever in Central Brazil, 1972-1973. I. Epidemiological studies. Am. J. Trop. Med. Hyg. 1978, 27, 125–132. [Google Scholar] [CrossRef]
- Degallier, N.; da Rosa, A.T.; Hervé, J.-P.; Vasconcelos, P.F.; Rodrigues, S.; Dias, L. A comparative study of yellow fever in Africa and South America. Ciênc. Cult. 1992, 44, 143–151. [Google Scholar]
- Culicidae, B.D.; Alencar, J.; Castro, F.C.; Monteiro, H.A.O.; Orlando, V.; Dégallier, N.; Marcondes, C.B.; Guimarães, A.E. New records of Haemagogus (Haemagogus) from Northern and Northeastern Brazil (Diptera: Culicidae, Aedini). Zootaxa 2008, 68, 65–68. [Google Scholar]
- Aragão, N.C.; Müller, G.A.; Balbino, V.Q.; Costa Junior, C.R.L.; Figueirêdo Júnior, C.S.; Alencar, J.; Marcondes, C.B. A list of mosquito species of the Brazilian State of Pernambuco, including the first report of Haemagogus janthinomys (Diptera: Culicidae), yellow fever vector and 14 other species (Diptera: Culicidae). Rev. Soc. Bras. Med. Trop. 2010, 43, 458–459. [Google Scholar] [CrossRef] [Green Version]
- Alencar, J.; Morone, F.; De Mello, C.F.; Dégallier, N.; Lucio, P.S.; Da Serra-Freire, N.M.; Guimarães, A.É. Flight Height Preference for Oviposition of Mosquito (Diptera: Culicidae) Vectors of Sylvatic Yellow Fever Virus Near the Hydroelectric Reservoir of Simplício, Minas Gerais, Brazil. J. Med. Entomol. 2013, 50, 791–795. [Google Scholar] [CrossRef] [Green Version]
- Alencar, J.; de Mello, C.F.; Barbosa, L.S.; Gil-Santana, H.R.; Maia, D.d.A.; Marcondes, C.B.; Silva, J.d.S. Diversity of yellow fever mosquito vectors in the Atlantic Forest of Rio de Janeiro, Brazil. Rev. Soc. Bras. Med. Trop. 2016, 49, 351–356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vinogradova, E.B. Diapause in Aquatic Insects, with Emphasis on Mosquitoes. In Diapause in Aquatic Invertebrates Theory and Human Use; Springer: Dordrecht, The Netherlands, 2007; pp. 83–113. [Google Scholar]
- Durden, M. Medical and Veterinary Entomology; Academic Press: Cambridge, MA, USA, 2009. [Google Scholar]
- Gillet, J.D. Variation in the Hatching-Response of Aedes Eggs (Diptera: Culicidae); Cambridge University Press: Cambridge, UK, 1955. [Google Scholar]
- Serpa, L.L.N.; Monteiro, S.D.C.B.; Voltolini, J.C. Efeito da água de criação larval na oviposição de Aedes aegypti em laboratório. Rev. Soc. Bras. Med. Trop. 2008, 41, 515–517. [Google Scholar] [CrossRef] [Green Version]
- Bastos, A.Q.; Leite, P.J.; dos Santos-Mallet, J.R.; de Mello, C.F.; Serdeiro, M.; dos Silva, J.S.; Figueiró, R.; Docile, T.; Alencar, J. Spawning behavior of Aedini (Diptera: Culicidae) in a remnant of Atlantic Forest in the state of Rio de Janeiro. Parasit. Vectors 2021, 14, 591. [Google Scholar] [CrossRef] [PubMed]
- Dietz, J.M.; Hankerson, S.J.; Alexandre, B.R.; Henry, M.D.; Martins, A.F.; Ferraz, L.P.; Ruiz-Miranda, C.R. Yellow fever in Brazil threatens successful recovery of endangered golden lion tamarins. Sci. Rep. 2019, 9, 12926. [Google Scholar] [CrossRef] [PubMed]
- INPE Dados Meteorológicos. Available online: https://www.gov.br/agricultura/pt-br/assuntos/inmet?r=estacoes/estacoesAutomaticas (accessed on 19 January 2021).
- Alencar, J.; de Mello, C.F.; Rodríguez-Planes, L.; dos Santos Silva, J.; Gil-Santana, H.R.; Bastos, A.Q.; Albuquerque, H.G.; Rodrigues, W.C.; Guimarães, A.É. Ecosystem diversity of mosquitoes (Diptera: Culicidae) in a remnant of Atlantic Forest, Rio de Janeiro state, Brazil. Austral Entomol. 2021, 60, 244–256. [Google Scholar] [CrossRef]
- Alencar, J.; De Almeida, H.M.; Marcondes, C.B.; Guimarães, A.É. Effect of multiple immersions on eggs and development of immature forms of Haemagogus janthinomys from south-eastern Brazil (Diptera: Culicidae). Entomol. News 2008, 119, 239–244. [Google Scholar] [CrossRef] [Green Version]
- Barbosa, A.A.; Silva, M.A.N. da Preferência por local de oviposição de Aedes albopictus (Skuse) (Diptera, Culicidae), em relação à presença de imaturos da própria espécie, sob condições de laboratório. Rev. Bras. Zool. 2002, 19, 1147–1152. [Google Scholar] [CrossRef] [Green Version]
- Reinert, J.F. List of abbreviations for currently valid generic-level taxa in family Culicidae (Diptera). J. Eur. Mosq. Control Assoc. 2009, 27, 68–76. [Google Scholar]
- Crawley, M.J. Statistics; Wiley: Hoboken, NJ, USA, 2005; ISBN 9780470022979. [Google Scholar]
- Brooks, M.E.; Kristensen, K.; Benthem, J.V.; Magnusson, A.; Berg, C.W.; Nielsen, A.; Skaug, H.J.; Mächler, M.; Bolker, B.M. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling. R J. 2017, 9, 378. [Google Scholar] [CrossRef] [Green Version]
- R Core Team R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2019.
- Alho, C.J.R. Importância da biodiversidade para a saúde humana: Uma perspectiva ecológica. Estud. Avançados 2012, 26, 151–166. [Google Scholar] [CrossRef] [Green Version]
- Docile, T.N.; Figueiró, R.; Portela, C.; Nessimian, J.L. Macroinvertebrate diversity loss in urban streams from tropical forests. Environ. Monit. Assess. 2016, 188. [Google Scholar] [CrossRef] [PubMed]
- Silva, S.O.F.; de Mello, C.F.; Figueiró, R.; Docile, T.; Serdeiro, M.; Fumian, F.F.; Alencar, J. Oviposition behavior of wild yellow fever vector mosquitoes (Diptera: Culicidae) in an Atlantic Forest fragment, Rio de Janeiro state, Brazil. Sci. Rep. 2021, 11, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Alencar, J.; Ferreira de Mello, C.; Silva, S.O.F.; Guimarães, A.É.; Müller, G.A. Effects of seasonality on the oviposition activity of potential vector mosquitoes (Diptera: Culicidae) from the São João River Basin Environmental Protection Area of the state of Rio de Janeiro, Brazil. Eur. Zool. J. 2022, 89, 1018–1025. [Google Scholar] [CrossRef]
- Freitas Silva, S.; de Mello, C.; Machado, S.; Leite, P.; Alencar, J. Interaction of Haemagogus leucocelaenus (Diptera: Culicidae) and Other Mosquito Vectors in a Forested Area, Rio de Janeiro, Brazil. Trop. Med. Infect. Dis. 2022, 7, 94. [Google Scholar] [CrossRef]
- Fikrig, K.; Harrington, L.C. Understanding and interpreting mosquito blood feeding studies: The case of Aedes albopictus. Trends Parasitol. 2021, 37, 959–975. [Google Scholar] [CrossRef]
- Mangudo, C.; Aparicio, J.P.; Rossi, G.C.; Gleiser, R.M. Tree hole mosquito species composition and relative abundances differ between urban and adjacent forest habitats in northwestern Argentina. Bull. Entomol. Res. 2018, 108, 203–212. [Google Scholar] [CrossRef]
- Pinto, C.S.; Confalonieri, U.E.C.; Mascarenhas, B.M. Ecology of Haemagogus sp. and Sabethes sp. (Diptera: Culicidae) in relation to the microclimates of the Caxiuanã National Forest, Pará, Brazil. Mem. Inst. Oswaldo Cruz 2009, 104, 592–598. [Google Scholar] [CrossRef] [Green Version]
- Alencar, J.; Serra-Friere, N.M.; Marcondes, C.B.; Silva, J.D.S.; Correa, F.F.; Guimarães, A.É. Influence of Climatic Factors on the Population Dynamics of Haemagogus janthinomys (Diptera: Culicidae), a Vector of Sylvatic Yellow Fever. Entomol. News 2010, 121, 45–52. [Google Scholar] [CrossRef]
- de Abreu, F.V.S.; Ribeiro, I.P.; Ferreira-de-Brito, A.; dos Santos, A.A.C.; de Miranda, R.M.; Bonelly, I.d.S.; Neves, M.S.A.S.; Bersot, M.I.; dos Santos, T.P.; Gomes, M.Q.; et al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016–2018. Emerg. Microbes Infect. 2019, 8, 218–231. [Google Scholar] [CrossRef] [Green Version]
- Hickey, W.A.; Craig, G.B. Genetic Distortion Of Sex Ratio in A Mosquito, Aedes aegypti. Genetics 1966, 53, 1177–1196. [Google Scholar] [CrossRef]
- Lounibos, L.P.; Escher, R.L. Sex Ratios of Mosquitoes from Long-Term Censuses of Florida Tree Holes. J. Am. Mosq. Control Assoc. 2008, 24, 11–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galizi, R.; Doyle, L.A.; Menichelli, M.; Bernardini, F.; Deredec, A.; Burt, A.; Stoddard, B.L.; Windbichler, N.; Crisanti, A. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat. Commun. 2014, 5, 3977. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alencar, J.; Gleiser, R.M.; Morone, F.; de Mello, C.F.; dos Silva, J.S.; Serra-Freire, N.M.; Guimarães, A.É. A comparative study of the effect of multiple immersions on Aedini (Diptera: Culicidae) mosquito eggs with emphasis on sylvan vectors of yellow fever virus. Mem. Inst. Oswaldo Cruz 2014, 109, 114–117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, S.O.F.; de Mello, C.F.; Gleiser, R.M.; Oliveira, A.A.; Maia, D.d.A.; Alencar, J. Evaluation of Multiple Immersion Effects on Eggs From Haemagogus leucocelaenus, Haemagogus janthinomys, and Aedes albopictus (Diptera: Culicidae) Under Experimental Conditions. J. Med. Entomol. 2018, 55, 1093–1097. [Google Scholar] [CrossRef]
- Alencar, J.; Marcondes, C.B.; Serra-Freire, N.M.; Lorosa, E.S.; Pacheco, J.B.; Guimarães, A.É. Feeding patterns of Haemagogus capricornii and Haemagogus leucocelaenus (Diptera: Culicidae) in two Brazilian states (Rio de Janeiro and Goiás). J. Med. Entomol. 2008, 45, 873–876. [Google Scholar] [CrossRef]
- Alencar, J.; De Mello, C.F.; Serra-Freire, N.M.; Guimarães, A.É.; Gil-Santana, H.R.; Gleiser, R.M. Biodiversity and temporal distribution of immature culicidae in the Atlantic Forest, Rio de Janeiro State. PLoS ONE 2016, 11, e0159240. [Google Scholar] [CrossRef] [Green Version]
- Couto-Lima, D.; Andreazzi, C.S.; Leite, P.J.; Bersot, M.I.L.; Alencar, J.; Lourenço-De-oliveira, R. Seasonal population dynamics of the primary yellow fever vector Haemagogus leucocelaenus (Dyar & shannon) (diptera: Culicidae) is mainly influenced by temperature in the atlantic forest, Southeast Brazil. Mem. Inst. Oswaldo Cruz 2020, 115, 1–13. [Google Scholar] [CrossRef]
Parameters | Sites | ||
---|---|---|---|
FT | MG | TM | |
Hatched eggs | 1850 | 1856 | 2446 |
Unhatched eggs | 10,003 | 5338 | 11,598 |
Proportion of larvae/unhatched eggs | 0.69 | 0.49 | 0.58 |
Proportion of adults/larvae | 0.34 | 0.39 | 0.34 |
Reared adults | |||
Aedes albopictus | 519 | 578 | 180 |
Aedes terrens | 414 | 35 | 344 |
Haemagogus leucocelaenus | 1068 | 445 | 1520 |
Haemagogus janthinomys | 8 | 8 | 73 |
Species | N | Site | Season | |||
---|---|---|---|---|---|---|
FT | MG | TM | Dry | Rainy | ||
Aedes albopictus | Female | 260 | 325 | 91 | 130 | 546 |
Male | 259 | 253 | 89 | 126 | 475 | |
Sex ratio | 1.00 | 0.78 | 0.98 | 0.97 | 0.87 | |
Aedes terrens | Female | 185 | 16 | 133 | 46 | 288 |
Male | 229 | 19 | 211 | 52 | 407 | |
Sex ratio | 1.24 | 1.19 | 1.59 | 1.13 | 1.41 | |
Haemagogus janthinomys | Female | 5 | 3 | 43 | 6 | 45 |
Male | 3 | 5 | 30 | 2 | 36 | |
Sex ratio | 0.60 | 1.67 | 0.70 | 0.33 | 0.80 | |
Haemagogus leucocelaenus | Female | 589 | 233 | 728 | 309 | 1241 |
Male | 479 | 212 | 792 | 273 | 1210 | |
Sex ratio | 0.81 | 0.91 | 1.09* | 0.88 | 0.98 |
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Silva, S.O.F.; de Mello, C.F.; Julião, G.R.; Dias, R.; Alencar, J. Sexual Proportion and Egg Hatching of Vector Mosquitos in an Atlantic Forest Fragment in Rio de Janeiro, Brazil. Life 2023, 13, 13. https://doi.org/10.3390/life13010013
Silva SOF, de Mello CF, Julião GR, Dias R, Alencar J. Sexual Proportion and Egg Hatching of Vector Mosquitos in an Atlantic Forest Fragment in Rio de Janeiro, Brazil. Life. 2023; 13(1):13. https://doi.org/10.3390/life13010013
Chicago/Turabian StyleSilva, Shayenne Olsson Freitas, Cecilia Ferreira de Mello, Genimar Rebouças Julião, Rayane Dias, and Jeronimo Alencar. 2023. "Sexual Proportion and Egg Hatching of Vector Mosquitos in an Atlantic Forest Fragment in Rio de Janeiro, Brazil" Life 13, no. 1: 13. https://doi.org/10.3390/life13010013