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Cited by 41Malaria Research and ControlEnvironmental Toxicology and EcotoxicologyHeavy Metal Exposure and Toxicity

Second generation effects of larval metal pollutant exposure on reproduction, longevity and insecticide tolerance in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

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Jeanrenaud, Alexander C. S. N., Brooke, Basil D., Oliver, Shüné V.·2020·Parasites & Vectors
DOI 10.1186/s13071-020-3886-9PMC PMC6947826
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Abstract

Background: Members of the Anopheles gambiae complex breed in clean, sunlit temporary bodies of water. Anthropogenic pollution is, however, altering the breeding sites of the vectors with numerous biological effects. Although the effects of larval metal pollution have previously been examined, this study aims to assess the transgenerational effects of larval metal pollution on the major malaria vector An. arabiensis . Methods: Two laboratory strains of An. arabiensis , SENN (insecticide-susceptible) and SENN-DDT (insecticide-resistant), were used in this study. After being bred in water polluted with either cadmium chloride, copper nitrate or lead nitrate, several life history characteristics that can have epidemiological implications (fertility, apoptotic damage to reproductive structures, adult longevity and insecticide tolerance) were examined in the adults and compared to those of adults bred in clean water. Results: All metal treatments reduced fecundity in SENN, but only lead treatment reduced fertility in SENN-DDT. Cadmium chloride exposure resulted in apoptosis and deformation of the testes in both strains. After breeding generation F0 in polluted water, F1 larvae bred in clean water showed an increase in longevity in SENN-DDT adult females. In contrast, after breeding the F0 generation in polluted water, longevity was reduced after cadmium and copper exposure in the F1 generation. Larval metal exposure resulted in an increase in insecticide tolerance in adults of the SENN strain, with SENN-DDT adults gaining the greatest fold increase in insecticide tolerance. Conclusions: This study demonstrates that a single exposure to metal pollution can have transgenerational effects that are not negated by subsequent breeding in clean water.

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  • In Central Africa, larvae of An. arabiensis that developed in organic wastewater developed faster, resulting in adults that had longer longevity and larger phenotypic sizes, as well as increased resistance to insecticides.

    “In Central Africa, larvae of An. arabiensis that developed in organic wastewater developed faster, resulting in adults that had longer longevity and larger phenotypic sizes, as well as increased resistance to insecticides [64].”

    From Sibling species of the major malaria vector Anopheles gambiae display divergent preferences for aquatic breeding sites in southern Nigeria (2024) · cites this paper as [64]

    The Methods describe laboratory An. arabiensis strains reared in water containing heavy-metal salts, not larvae developing in organic wastewater in Central Africa. The Conclusions support increased insecticide tolerance, but the Results and Discussion report reduced—not longer—adult longevity after repeated exposure. The paper does not report faster development or larger adult size in these experiments. (LLM, conf=0.88)

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  • Organic wastes probably served as food for An. arabiensis larvae in southern Nigeria.

    “these organic wastes probably served as food for An. arabiensis larvae in southern Nigeria.”

    From Sibling species of the major malaria vector Anopheles gambiae display divergent preferences for aquatic breeding sites in southern Nigeria (2024) · cites this paper as [64]

    The Background (page unavailable) says An. arabiensis thrives on maize and rice pollen and reports its urban incidence in Nigeria. It does not say that organic wastes served as larval food or place that feeding in southern Nigeria. (LLM, conf=0.78)

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Research works printed but not linked: 49

  1. [1]Vareda JP Valente AJM Duraes L Assessment of heavy metal pollution from anthropogenic activities and remediation strategies: a review J Environ Manage. 2019 246 101 118 10.1016/j.jenvman.2019.05.126 31176176 · DOI
  2. [2]Lekfeldt JDS Holm PE Kjaergaard C Magid J Heavy metal leaching as affected by long-time organic waste fertilizer application J Environ Qual. 2017 46 871 878 10.2134/jeq2016.11.0458 28783778 · DOI
  3. [3]He ZL Yang XE Stoffella PJ Trace elements in agroecosystems and impacts on the environment J Trace Elem Med. 2005 19 125 140 10.1016/j.jtemb.2005.02.010 16325528 · DOI
  4. [4]Ma L Sun J Yang Z Wang L Heavy metal contamination of agricultural soils affected by mining activities around the Ganxi River in Chenzhou, southern China Environ Monit Assess. 2015 187 731 10.1007/s10661-015-4966-8 26547321 · DOI
  5. [5]Tariq SR Shafiq M Chotana GA Distribution of heavy metals in the soils associated with the commonly used pesticides in cotton fields Scientifica (Cairo) 2016 2016 7575239 27051560 PMC4804093
  6. [6]Arambourou H Planello R Llorente L Fuertes I Barata C Delorme N Chironomus riparius exposure to field-collected contaminated sediments: from subcellular effect to whole-organism response Sci Total Environ. 2019 671 874 882 10.1016/j.scitotenv.2019.03.384 30947058 · DOI
  7. [7]Plachetka-Bozek A Kafel A Augustyniak M Reproduction and development of Spodoptera exigua from cadmium and control strains under differentiated cadmium stress Ecotoxicol Environ Safety. 2018 166 138 145 10.1016/j.ecoenv.2018.09.016 30265877 · DOI
  8. [8]Sowa G Skalski T Effects of chronic metal exposure on the morphology of beetles species representing different ecological niches Bull Environ Contam Toxicol. 2019 102 191 197 10.1007/s00128-018-02532-7 30666388 PMC6394555 · DOI
  9. [9]Mwangangi J Shililu J Muturi E Gu W Mbogo C Kabiru E Dynamics of immature stages of Anopheles arabiensis and other mosquito species (Diptera: Culicidae) in relation to rice cropping in a rice agro-ecosystem in Kenya J Vector Ecol. 2006 31 245 251 10.3376/1081-1710(2006)31[245:DOISOA]2.0.CO;2 17249341 · DOI
  10. [10]Ye-Ebiyo Y Pollack RJ Kiszewski A Spielman A Enhancement of development of larval Anopheles arabiensis by proximity to flowering maize (Zea mays) in turbid water and when crowded Am J Trop Med Hyg. 2003 68 748 752 10.4269/ajtmh.2003.68.748 12887038 · DOI · Paper page
  11. [11]Antonio-Nkondjio C Fossog BT Ndo C Djantio BM Togouet SZ Awono-Ambene P Anopheles gambiae distribution and insecticide resistance in the cities of Douala and Yaounde (Cameroon): influence of urban agriculture and pollution Malar J. 2011 10 154 10.1186/1475-2875-10-154 21651761 PMC3118161 · DOI
  12. [12]Awolola TS Oduola AO Obansa JB Chukwurar NJ Unyimadu JP Anopheles gambiae s.s. breeding in polluted water bodies in urban Lagos, southwestern Nigeria J Vector Borne Dis. 2007 44 241 244 18092529
  13. [13]Mireji PO Keating J Hassanali A Mbogo CM Nyambaka H Kahindi S Beier JC Heavy metals in mosquito larval habitats in urban Kisumu and Malindi, Kenya, and their impact Ecotoxicol Environ Saf. 2008 70 147 153 10.1016/j.ecoenv.2007.03.012 17532467 PMC2673497 · DOI
  14. [14]Jeanrenaud ACSN Brooke BD Oliver SV The effects of larval organic fertiliser exposure on the larval development, adult longevity and insecticide tolerance of zoophilic members of the Anopheles gambiae complex (Diptera: Culicidae) PLoS One. 2019 14 e0215552 10.1371/journal.pone.0215552 30998732 PMC6472872 · DOI
  15. [15]Kibuthu TW Njenga SM Mbugua AK Muturi EJ Agricultural chemicals: life changer for mosquito vectors in agricultural landscapes? Parasit Vectors. 2016 9 500 10.1186/s13071-016-1788-7 27624456 PMC5022241 · DOI
  16. [16]Mireji PO Keating J Hassanali A Mbogo CM Muturi MN Githure JI Beier JC Biological cost of tolerance to heavy metals in the mosquito Anopheles gambiae Med Vet Entomol. 2010 24 101 107 10.1111/j.1365-2915.2010.00863.x 20374478 PMC2921613 · DOI
  17. [18]Bara JJ Montgomery A Muturi EJ Sublethal effects of atrazine and glyphosate on life history traits of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) Parasitol Res. 2014 113 2879 2886 10.1007/s00436-014-3949-y 24853538 · DOI
  18. [19]Oliver SV Brooke BD The effect of commercial herbicide exposure on the life history and insecticide resistance phenotypes of the major malaria vector Anopheles arabiensis (Diptera: culicidae) Acta Trop. 2018 188 152 160 10.1016/j.actatropica.2018.08.030 30179608 · DOI
  19. [20]Oliver SV Brooke BD The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae) Malar J. 2017 16 73 10.1186/s12936-017-1720-4 28193292 PMC5307775 · DOI
  20. [21]Oliver SV Brooke BD The effect of larval nutritional deprivation on the life history and DDT resistance phenotype in laboratory strains of the malaria vector Anopheles arabiensis Malar J. 2013 12 44 10.1186/1475-2875-12-44 23368928 PMC3570311 · DOI
  21. [22]Hunt RH Brooke BD Pillay C Koekemoer LL Coetzee M Laboratory selection for and characteristics of pyrethroid resistance in the malaria vector Anopheles funestus Med Vet Entomol. 2005 19 271 275 10.1111/j.1365-2915.2005.00574.x 16134975 · DOI
  22. [23]Musasia FK Isaac AO Masiga DK Omedo IA Mwakubambanya R Ochieng R Mireji PO Sex-specific induction of CYP6 cytochrome P450 genes in cadmium and lead tolerant Anopheles gambiae Malaria J. 2013 12 97 10.1186/1475-2875-12-97 PMC3601984 23497268 · DOI
  23. [24]Oliver SV Brooke BD The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae) PLoS One 2018 13 e0192551 10.1371/journal.pone.0192551 29408922 PMC5800662 · DOI
  24. [25]Itai T Otsuka M Asante KA Muto M Opoku-Ankomah Y Ansa-Asare OD Tanabe S Variation and distribution of metals and metalloids in soil/ash mixtures from Agbogbloshie e-waste recycling site in Accra Ghana. Sci Total Environ. 2014 470–471 707 716 10.1016/j.scitotenv.2013.10.037 24184547 · DOI
  25. [26]Nkya TE Akhouayri I Kisinza W David JP Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects Insect Biochem Mol Biol. 2013 43 407 416 10.1016/j.ibmb.2012.10.006 23123179 · DOI · Paper page
  26. [27]Abrams JM White K Fessler LI Steller H Programmed cell death during Drosophila embryogenesis Development. 1993 117 29 43 8223253
  27. [28]Kaplan EL Meier P Nonparametric estimation from incomplete observations J Am Stat Assoc. 1958 53 457 481 10.1080/01621459.1958.10501452 · DOI · Paper page
  28. [30]Finney DJ Probit analysis 1952 2 New York Cambridge University Press
  29. [31]Shapiro SS Wilk MB An analysis of variance test for normality (complete samples) Biometrika 1965 52 591 611 10.1093/biomet/52.3-4.591 · DOI · Paper page
  30. [32]Tukey JW Comparing individual means in the analysis of variance Biometrics 1949 5 99 114 10.2307/3001913 18151955 · DOI
  31. [33]Bland JM Altman DG The logrank test BMJ. 2004 328 1073 10.1136/bmj.328.7447.1073 15117797 PMC403858 · DOI
  32. [34]Alaraby M Romero S Hernandez A Marcos R Toxic and genotoxic effects of silver nanoparticles in Drosophila Environ Mol Mutagen. 2019 60 277 285 10.1002/em.22262 30353950 · DOI
  33. [35]Morais GDS Vieira TB Santos GS Baika LM Cestari MM Grassi MT Navarro da Silva MA Biological, biochemical and genotoxic effects of Sb in the midge Chironomus sancticaroli Strixino and Strixino, 1981 (Diptera: Chironomidae) Ecotoxicol Environ Saf. 1981 2019 176 196 203 30928891
  34. [36]Sahlmann A Lode T Heuschele J Borga K Titelman J Hylland K Genotoxic response and mortality in three marine copepods exposed to waterborne copper Environ Toxicol Chem. 2019 38 2224 2232 10.1002/etc.4541 31343775 · DOI
  35. [37]de Angelis C Galdiero M Pivonello C Salzano C Gianfrilli D Piscitelli P The environment and male reproduction: the effect of cadmium exposure on reproductive function and its implication in fertility Reprod Toxicol. 2017 73 105 127 10.1016/j.reprotox.2017.07.021 28774687 · DOI
  36. [38]Siu ER Mruk DD Porto CS Cheng CY Cadmium-induced testicular injury Toxicol Appl Pharmacol. 2009 238 240 249 10.1016/j.taap.2009.01.028 19236889 PMC2804910 · DOI
  37. [40]Boyd MF Kitchen SF The duration of the intrinsic incubation period in falciparum malaria in relation to certain factors affecting the parasites Am J Trop Med Hyg. 1937 s1–17 845 848 10.4269/ajtmh.1937.s1-17.845 · DOI
  38. [41]Garrett-Jones C Shidrawi GR Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology Bull World Health Organ. 1969 40 531 545 5306719 PMC2556109
  39. [42]Poupardin R Reynaud S Strode C Ranson H Vontas J David JP Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides Insect Biochem Mol Biol. 2008 38 540 551 10.1016/j.ibmb.2008.01.004 18405832 · DOI
  40. [43]Otali D Novak RJ Wan W Bu S Moellering DR De Luca M Increased production of mitochondrial reactive oxygen species and reduced adult life span in an insecticide-resistant strain of Anopheles gambiae Bull Entomol Res. 2014 104 323 333 10.1017/S0007485314000091 24555527 PMC4008687 · DOI
  41. [44]Kamdem C Fouet C Gamez S White BJ Pollutants and insecticides drive local adaptation in African malaria mosquitoes Mol Biol Evol. 2017 34 1261 1275 10.1093/molbev/msx087 28204524 PMC5400387 · DOI
  42. [45]Drzewiecka D Significance and roles of Proteus spp. bacteria in natural environments Microb Ecol. 2016 72 741 758 10.1007/s00248-015-0720-6 26748500 PMC5080321 · DOI
  43. [46]Wang H Sangwan N Li HY Su JQ Oyang WY Zhang ZJ The antibiotic resistome of swine manure is significantly altered by association with the Musca domestica larvae gut microbiome ISME J. 2017 11 100 111 10.1038/ismej.2016.103 27458785 PMC5315468 · DOI
  44. [47]Kalappa DM Subramani PA Basavanna SK Ghosh SK Sundaramurthy V Uragayala S Influence of midgut microbiota in Anopheles stephensi on Plasmodium berghei infections Malaria J. 2018 17 385 10.1186/s12936-018-2535-7 PMC6203276 30359252 · DOI
  45. [48]Song X Wang M Dong L Zhu H Wang J PGRP-LD mediates A stephensi vector competency by regulating homeostasis of microbiota-induced peritrophic matrix synthesis PLoS Pathog. 2018 14 e1006899 10.1371/journal.ppat.1006899 29489896 PMC5831637 · DOI
  46. [49]Wu P Sun P Nie K Zhu Y Shi M Xiao C A gut commensal bacterium promotes mosquito permissiveness to arboviruses Cell Host Microbe. 2019 25 101 112 10.1016/j.chom.2018.11.004 30595552 · DOI
  47. [50]Alout H Djegbe I Chandre F Djogbenou LS Dabire RK Corbel V Cohuet A Insecticide exposure impacts vector-parasite interactions in insecticide-resistant malaria vectors Proc Biol Sci. 2014 281 20140389 10.1098/rspb.2014.0389 24850924 PMC4046407 · DOI
  48. [51]Alout H Ndam NT Sandeu MM Djegbe I Chandre F Dabire RK Insecticide resistance alleles affect vector competence of Anopheles gambiae s.s. for Plasmodium falciparum field isolates PLoS One. 2013 8 e63849 10.1371/journal.pone.0063849 23704944 PMC3660590 · DOI
  49. [52]Dieme C Rotureau B Mitri C Microbial pre-exposure and vectorial competence of Anopheles mosquitoes Front Cell Infect Microbiol. 2017 7 508 10.3389/fcimb.2017.00508 29376030 PMC5770632 · DOI

Cited by

Sorted by citations

Authors
Jeanrenaud, A. C. S. N., Brooke, B. D., & Oliver, S. V.
Affiliations
National Health Laboratory Service (ZA)
Corresponding author
Oliver, Shüné V.
ORCID
Venue
Parasites & Vectors
Publisher
Springer Science and Business Media LLC
Published
2020-01-07
Volume
13
Issue
1
Pages
4-4
ISSN
1756-3305 (ISSN-L)
DOI
10.1186/s13071-020-3886-9
PMC
PMC6947826
OpenAlex
W3013548101
Cited by
41
References
1
Citations by year
2026: 3 · 2025: 8 · 2024: 16 · 2023: 1 · 2022: 4 · 2021: 7 · 2020: 1 · 2018: 1
FWCI
2.43
Type
journal article
Language
en
Open access
Licence
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Research Foundation (TTK160622173523)
  • NHLS Research Trust (2014-DEV-SOL1)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
Keywords
Anopheles arabiensis, malaria vectors, cadmium, copper, lead, transgenerational effects, insecticide resistance, DDT, fecundity, testicular apoptosis, adult longevity, larval exposure
MeSH terms
Animals, Anopheles, Drug Resistance, Female, Fertility, Insecticides, Larva, Male, Metals, Reproduction, Water Pollutants

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