Isotopic evidence that aestivation allows malaria mosquitoes to persist through the dry season in the Sahel.

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    • Source:
      Publisher: Springer Nature Country of Publication: England NLM ID: 101698577 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2397-334X (Electronic) Linking ISSN: 2397334X NLM ISO Abbreviation: Nat Ecol Evol Subsets: MEDLINE
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      Original Publication: [London] : Springer Nature
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    • Abstract:
      Data suggest that the malaria vector mosquito Anopheles coluzzii persists during the dry season in the Sahel through a dormancy mechanism known as aestivation; however, the contribution of aestivation compared with alternative strategies such as migration is unknown. Here we marked larval Anopheles mosquitoes in two Sahelian villages in Mali using deuterium ( 2 H) to assess the contribution of aestivation to persistence of mosquitoes through the seven-month dry season. After an initial enrichment period, 33% of An. coluzzii mosquitoes were strongly marked. Seven months following enrichment, multiple analysis methods supported the ongoing presence of marked mosquitoes, compatible with the prediction that the fraction of marked mosquitoes should remain stable throughout the dry season if local aestivation is occurring. The results suggest that aestivation is a major persistence mechanism of An. coluzzii in the Sahel, contributing at least 20% of the adults at the onset of rains. This persistence strategy could influence mosquito control and malaria elimination campaigns.
      (© 2022. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.)
    • Comments:
      Comment in: Nat Ecol Evol. 2022 Nov;6(11):1593-1594. (PMID: 36216904)
      Comment in: Trends Parasitol. 2023 Jan;39(1):1-3. (PMID: 36470782)
    • References:
      Adamou, A. et al. The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar. J. 10, 151 (2011). (PMID: 216453853123247)
      Huestis, D. L. et al. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J. Exp. Biol. 215, 2013–2021 (2012). (PMID: 226231893359115)
      Huestis, D. L. et al. Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. J. Exp. Biol. 214, 2345–2353 (2011). (PMID: 216974263120220)
      Lehmann, T. et al. Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Am. J. Trop. Med. Hyg. 83, 601–606 (2010). (PMID: 208108272929058)
      Yaro, A. S. et al. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 58, 1050–1059 (2012). (PMID: 226094214789105)
      Omer, S. M. & Cloudsley-Thompson, J. L. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull. World Health Organ. 42, 319 (1970). (PMID: 53101442427450)
      Omer, S. M. & Cloudsley-Thompson, J. L. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 217, 879–880 (1968).
      Holstein, M. H. Biology of Anopheles gambiae (1954). World Health Organization.
      Andrade, C. M. et al. Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. Nat. Med. 26, 1929–1940 (2020). (PMID: 33106664)
      Coulibaly, D. et al. Spatio-temporal dynamics of asymptomatic malaria: bridging the gap between annual malaria resurgences in a Sahelian environment. Am. J. Trop. Med. Hyg. 27, 1761–1769 (2017).
      Gillies, M. & Wilkes, T. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in north-eastern Tanzania. Bull. Entomol. Res. 56, 237–262 (1965). (PMID: 5854754)
      Gillies, M. T. & De Meillon, B. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region) (Johannesburg: South African Institute for Medical Research, 1968).
      Dao, A. et al. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516, 387–390 (2014). (PMID: 254700384306333)
      Thomson, J. G. Malaria in Nyasaland. Proc. R. Soc. Med. 28, 391–404 (1934).
      Huestis, D. L. et al. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature 574, 404–408 (2019). (PMID: 31578527)
      Lambert, B., North, A., Burt, A. & Godfray, H. C. J. The use of driving endonuclease genes to suppress mosquito vectors of malaria in temporally variable environments. Malar. J. 17, 154 (2018). (PMID: 296183675885365)
      Verhulst, N. O., Loonen, J. A. C. M. & Takken, W. Advances in methods for colour marking of mosquitoes. Parasit. Vectors 6, 200 (2013). (PMID: 238350913708792)
      Hagler, J. R. & Jackson, C. G. Methods for marking insects: current techniques and future prospects. Annu. Rev. Entomol. 46, 511–543 (2001). (PMID: 11112178)
      Hamer, G. L. et al. Dispersal of adult culex mosquitoes in an urban West Nile virus hotspot: a mark–capture study incorporating stable isotope enrichment of natural larval habitats. PLoS Negl. Trop. Dis. 8, e2768 (2014). (PMID: 246762123967984)
      Hamer, G. L. et al. Evaluation of a stable isotope method to mark naturally-breeding larval mosquitoes for adult dispersal studies. J. Med. Entomol. 49, 61–70 (2012). (PMID: 22308772)
      Opiyo, M. A. et al. Using stable isotopes of carbon and nitrogen to mark wild populations of Anopheles and Aedes mosquitoes in south-eastern Tanzania. PLoS ONE 11, e0159067 (2016). (PMID: 273920834938253)
      Hood-Nowotny, R., Mayr, L. & Knols, B. Use of carbon-13 as a population marker for Anopheles arabiensis in a sterile insect technique (SIT) context. Malar. J. 5, 6 (2006). (PMID: 164458651373641)
      Hood-Nowotny, R. & Knols, B. G. J. Stable isotope methods in biological and ecological studies of arthropods. Entomol. Exp. Appl. 124, 3–16 (2007).
      Hood-Nowotny, R. et al. Intrinsic and synthetic stable isotope marking of tsetse flies. J. Insect Sci. 11, 79 (2011). (PMID: 218709653281438)
      Atzrodt, J., Derdau, V., Kerr, W. J. & Reid, M. Deuterium- and tritium-labelled compounds: applications in the life sciences. Angew. Chem. Int. Ed. 57, 1758–1784 (2018).
      Copia, L., Wassenaar, L. I., Terzer-Wassmuth, S., Belachew, D. L. & Araguas-Araguas, L. J. Comparative evaluation of 2 H- versus 3 H-based enrichment factor determination on the uncertainty and accuracy of low-level tritium analyses of environmental waters. Appl. Radiat. Isot. 176, 109850 (2021). (PMID: 34246163)
      Begon, M., Harper, J. & Townsend, C. Ecology: Individuals, Populations and Communities (Blackwell Science, 1996).
      Faiman, R. et al. Marking mosquitoes in their natural larval sites using 2 H-enriched water: a promising approach for tracking over extended temporal and spatial scales. Methods Ecol. Evol. 10, 1274–1285 (2019). (PMID: 328557837449266)
      Florkin, M. Chemical Zoology: Arthropoda Part B (Academic Press, 2014).
      Hackman, R. H. & Goldberg, M. Studies on chitin VI. The nature of alpha-and beta-chitins. Aust. J. Biol. Sci. 18, 935–946 (1965). (PMID: 5861258)
      Faiman, R. et al. Quantifying flight aptitude variation in wild Anopheles gambiae in order to identify long-distance migrants. Malar. J. 19, 263 (2020). (PMID: 326988427374819)
      Huestis, D. L. & Lehmann, T. Ecophysiology of Anopheles gambiae s.l.: persistence in the Sahel. Infect. Genet. Evol. 28, 648–661 (2014). (PMID: 249334614257857)
      Lehmann, T. et al. Seasonal variation in spatial distributions of Anopheles gambiae in a Sahelian village: evidence for aestivation. J. Med. Entomol. 51, 27–38 (2014). (PMID: 24605449)
      Costantini, C. et al. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med. Vet. Entomol. 10, 203–219 (1996). (PMID: 8887330)
      Toure, Y. T. et al. Mark–release–recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med. Vet. Entomol. 12, 74–83 (1998). (PMID: 9513942)
      Faiman, R. et al. A novel fluorescence and DNA combination for versatile, long-term marking of mosquitoes. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13592 (2021).
      Brattström, O., Bensch, S., Wassenaar, L. I., Hobson, K. A. & Åkesson, S. Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography 33, 720–729 (2010).
      Hobson, K. A., Jinguji, H., Ichikawa, Y., Kusack, J. W. & Anderson, R. C. Long-distance migration of the globe skimmer dragonfly to Japan revealed using stable hydrogen (δ  2 H) isotopes. Environ. Entomol. 50, 247–255 (2020).
      Schilling, E. G. et al. Phenological and isotopic evidence for migration as a life history strategy in Aeshna canadensis (family: Aeshnidae) dragonflies. Ecol. Entomol. 46, 209–219 (2021).
      Girard, P., Hillaire-Marcel, C. & Oga, M. S. Determining the recharge mode of Sahelian aquifers using water isotopes. J. Hydrol. 197, 189–202 (1997).
      Gutiérrez-Expósito, C., Ramírez, F., Afán, I., Forero, M. & Hobson, K. A. Toward a deuterium feather isoscape for sub-Saharan Africa: progress, challenges and the path ahead. PLoS ONE https://doi.org/10.1371/journal.pone.0135938 (2015).
      Lutz, A., Thomas, J. M. & Panorska, A. Environmental controls on stable isotope precipitation values over Mali and Niger, West Africa. Environ. Earth Sci. 62, 1749–1759 (2011).
      Risi, C. et al. Understanding the Sahelian water budget through the isotopic composition of water vapor and precipitation. J. Geophys. Res. Atmos. 115, 1–23 (2010).
      Tremoy, G. et al. A 1-year long δ 18 O record of water vapor in Niamey (Niger) reveals insightful atmospheric processes at different timescales. Geophys. Res. Lett. 39, 1–5 (2012).
      Terzer‐Wassmuth, S., Wassenaar, L. I., Welker, J. M., Araguás-Araguás, L. J. Improved high‐resolution global and regionalized isoscapes of δ 18 O, δ 2 H and d‐excess in precipitation. Hydrol. Process. 35 (2021).
      Hobson, K. A. et al. A multi-isotope (δ 13 C, δ 15 N, δ 2 H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere 3, art44 (2012).
      Diuk-Wasser, M. A. et al. Effect of rice cultivation patterns on malaria vector abundance in rice-growing villages in Mali. Am. J. Trop. Med. Hyg. 76, 869–874 (2007). (PMID: 17488907)
      Sogoba, N. et al. Malaria transmission dynamics in Niono, Mali: the effect of the irrigation systems. Acta Trop. 101, 232–240 (2007). (PMID: 17362859)
      Florio, J. et al. Diversity, dynamics, direction, and magnitude of high-altitude migrating insects in the Sahel. Sci. Rep. 10, 20523 (2020). (PMID: 332396197688652)
      Wilkins, E. E., Howell, P. I. & Benedict, M. Q. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar. J. 5, 125 (2006). (PMID: 171779931769388)
      Wassenaar, L. I. & Hobson, K. A. Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ. Health Stud. 39, 211–217 (2003). (PMID: 14521282)
      Chesson, L. A., Podlesak, D. W., Cerling, T. E. & Ehleringer, J. R. Evaluating uncertainty in the calculation of non-exchangeable hydrogen fractions within organic materials. Rapid Commun. Mass Spectrom. 23, 1275–1280 (2009). (PMID: 19306283)
      Schimmelmann, A. Determination of the concentration and stable isotopic composition of nonexchangeable hydrogen in organic matter. Anal. Chem. 63, 2456–2459 (1991).
      Speakman, J. Doubly Labelled Water: Theory and Practice (Chapman & Hall, 1997).
      Base SAS 9.4 Procedures Guide (SAS Institute, 2015).
      Cade, B. S. & N, B. R. A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1, 412–420 (2003).
      SAS/STAT® 15.1 User’s Guide (SAS Institute, 2018).
      Mcclintock, B. T. et al. Uncovering ecological state dynamics with hidden Markov models. Ecol. Lett. 23, 1878–1903 (2020). (PMID: 330739217702077)
      Issam, M., Naulet, N., Martin, M. L. & Martin, G. J. A site-specific and multielement approach to the determination of liquid–vapor isotope fractionation parameters: the case of alcohols. J. Phys. Chem. 94, 8303–8309 (1990).
      Linderstrøm-Lang, C. U. & Vaslow, F. Isotope effect on the vapor pressures of water–ethanol and deuterium oxide–ethanol-d mixtures. J. Phys. Chem. 72, 2645–2650 (1968).
      Ventura, M. & Jeppesen, E. Effects of fixation on freshwater invertebrate carbon and nitrogen isotope composition and its arithmetic correction. Hydrobiologia 632, 297–308 (2009).
    • Molecular Sequence:
      figshare 10.6084/m9.figshare.20387328.v1
    • Publication Date:
      Date Created: 20221010 Date Completed: 20221104 Latest Revision: 20230227
    • Publication Date:
      20240829
    • Accession Number:
      10.1038/s41559-022-01886-w
    • Accession Number:
      36216903