Agricultural chemicals: life changer for mosquito vectors in agricultural landscapes?

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Abstract

Background

Although many mosquito species develop within agricultural landscapes where they are potentially exposed to agricultural chemicals (fertilizers and pesticides), the effects of these chemicals on mosquito biology remain poorly understood. This study investigated the effects of sublethal concentrations of four agricultural chemicals on the life history traits of Anopheles arabiensis and Culex quinquefasciatus mosquitoes.

Methods

Field and laboratory experiments were conducted to examine how sublethal concentrations of four agricultural chemicals: an insecticide (cypermethrin), a herbicide (glyphosate), and two nitrogenous fertilizers (ammonium sulfate and diammonium phosphate) alter oviposition site selection, emergence rates, development time, adult body size, and longevity of An. arabiensis and Cx. quinquefasciatus.

Results

Both mosquito species had preference to oviposit in fertilizer treatments relative to pesticide treatments. Emergence rates for An. arabiensis were significantly higher in the control and ammonium sulfate treatments compared to cypermethrin treatment, while emergence rates for Cx. quinquefasciatus were significantly higher in the diammonium phosphate treatment compared to glyphosate and cypermethrin treatments. For both mosquito species, individuals from the ammonium sulfate and diammonium phosphate treatments took significantly longer time to develop compared to those from cypermethrin and glyphosate treatments. Although not always significant, males and females of both mosquito species tended to be smaller in the ammonium sulfate and diammonium phosphate treatments compared to cypermethrin and glyphosate treatments. There was no significant effect of the agrochemical treatments on the longevity of either mosquito species.

Conclusions

These results demonstrate that the widespread use of agricultural chemicals to enhance crop production can have unexpected effects on the spatial distribution and abundance of mosquito vectors of malaria and lymphatic filariasis.

Related collections

Most cited references 65

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Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya

M. Nabie Bayoh, Derrick K. Mathias, Maurice R. Odiere … (2010)

Background High coverage of insecticide-treated bed nets in Asembo and low coverage in Seme, two adjacent communities in western Nyanza Province, Kenya; followed by expanded coverage of bed nets in Seme, as the Kenya national malaria programme rolled out; provided a natural experiment for quantification of changes in relative abundance of two primary malaria vectors in this holoendemic region. Both belong to the Anopheles gambiae sensu lato (s.l.) species complex, namely A. gambiae sensu stricto (s.s.) and Anopheles arabiensis. Historically, the former species was proportionately dominant in indoor resting collections of females. Methods Data of the relative abundance of adult A. gambiae s.s. and A. arabiensis sampled from inside houses were obtained from the literature from 1970 to 2002 for sites west of Kisumu, Kenya, to the region of Asembo ca. 50 km from the city. A sampling transect was established from Asembo (where bed net use was high due to presence of a managed bed net distribution programme) eastward to Seme, where no bed net programme was in place. Adults of A. gambiae s.l. were sampled from inside houses along the transect from 2003 to 2009, as were larvae from nearby aquatic habitats, providing data over a nearly 40 year period of the relative abundance of the two species. Relative proportions of A. gambiae s.s. and A. arabiensis were determined for each stage by identifying species by the polymerase chain reaction method. Household bed net ownership was measured with surveys during mosquito collections. Data of blood host choice, parity rate, and infection rate for Plasmodium falciparum in A. gambiae s.s. and A. arabiensis were obtained for a sample from Asembo and Seme from 2005. Results Anopheles gambiae s.s. adult females from indoor collections predominated from 1970 to 1998 (ca. 85%). Beginning in 1999, A. gambiae s.s decreased proportionately relative to A. arabiensis, then precipitously declined to rarity coincident with increased bed net ownership as national bed net distribution programmes commenced in 2004 and 2006. By 2009, A. gambiae s.s. comprised proportionately ca. 1% of indoor collections and A. arabiensis 99%. In Seme compared to Asembo in 2003, proportionately more larvae were A. gambiae s.s., larval density was higher, and more larval habitats were occupied. As bed net use rose in Seme, the proportion of A. gambiae larvae declined as well. These trends continued to 2009. Parity and malaria infection rates were lower in both species in Asembo (high bed net use) compared to Seme (low bed net use), but host choice did not vary within species in both communities (predominantly cattle for A. arabiensis, humans for A. gambiae s.s.). Conclusions A marked decline of the A. gambiae s.s. population occurred as household ownership of bed nets rose in a region of western Kenya over a 10 year period. The increased bed net coverage likely caused a mass effect on the composition of the A. gambiae s.l. species complex, resulting in the observed proportionate increase in A. arabiensis compared to its closely related sibling species, A. gambiae s.s. These observations are important in evaluating the process of regional malaria elimination, which requires sustained vector control as a primary intervention.

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Chemical ecology and behavioral aspects of mosquito oviposition.

Christy Bentley, Tyler Day (1988)

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Impact of irrigation on malaria in Africa: paddies paradox.

Timothy Lindsay, Jasper Ijumba (2001)

The high population growth rate of the African continent has led to an increased demand for food and is in danger of outstripping agricultural production. In order to meet this need, many governments have sought ways of improving food production by initiating large-scale irrigation projects, involving reclamation of arid and semi-arid areas for the cultivation of crops. Although crop irrigation promises one solution to alleviating hunger and encourages economic growth, irrigation has often been blamed for aggravating disease in local communities. Malaria is one of the major tropical diseases associated with irrigation schemes, and changes in the transmission pattern of this disease following irrigation development have been a perennial subject of debate. It has often been assumed that high numbers of malaria vector Anopheles mosquitoes (Diptera: Culicidae) resulting from irrigation schemes lead inevitably to increased malaria in local communities. However, recent studies in Africa have revealed a more complex picture. Increased numbers of vectors following irrigation can lead to increased malaria in areas of unstable transmission, where people have little or no immunity to malaria parasites, such as the African highlands and desert fringes. But for most of sub-Saharan Africa, where malaria is stable, the introduction of crop irrigation has little impact on malaria transmission. Indeed, there is growing evidence that for many sites there is less malaria in irrigated communities than surrounding areas. The explanation for this finding is still unresolved but, in some cases at least, can be attributed to displacement of the most endophilic and anthropophilic malaria vector Anopheles funestus Giles by An. arabiensis Patton with lower vectorial capacity, as the latter thrives more than the former in ricefields. Similarly, among members of the An. gambiae complex, some cytotypes of An. gambiae sensu stricto are more vectorial than others. For example, the Mopti form has high vectorial capacity and breeds perennially in irrigated sites, whereas the savanna form is often sympatric but more seasonal. Also we suggest that many communities near irrigation schemes benefit from the greater wealth created by these schemes. Consequently irrigation communities often have greater use of bednets, better access to improved healthcare and receive fewer infective bites compared with those outside such development schemes. Thus, in most cases, irrigation schemes in Africa do not appear to increase malaria risk, except in areas of unstable transmission. However, developers should take the opportunity to improve health-care facilities for local communities when planning irrigation schemes wherever they occur.

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Author and article information

Contributors

Tabitha W. Kibuthu: tabwamboi@yahoo.com

Sammy M. Njenga: sammynjenga@gmail.com

Amos K. Mbugua: ambugua@jkuat.ac.ke

Ephantus J. Muturi: ephajumu@yahoo.com

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 13 September 2016

Publication date PMC-release: 13 September 2016

Publication date Collection: 2016

Volume: 9

Issue: 1

Electronic Location Identifier: 500

Affiliations

[1 ]Institute of Tropical Medicine, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya

[2 ]Eastern and Southern Africa Centre of International Parasite Control, Kenya Medical Research Institute, Nairobi, Kenya

[3 ]College of Health Sciences, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya

[4 ]Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, USA

[5 ]Present Address: U.S.D.A., Agricultural Research Service, National Center for Agricultural Utilization Research, Crop Bioprotection Research Unit, 1815 N. University St., Peoria, IL 61604 USA

Article

Publisher ID: 1788

DOI: 10.1186/s13071-016-1788-7

PMC ID: 5022241

PubMed ID: 27624456

SO-VID: eb384595-5055-49bd-b4b0-14971b83d4fb

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 29 March 2016

Date accepted : 2 September 2016

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: agricultural chemicals,sublethal concentrations,life history traits,anopheles arabiensis,culex quinquefasciatus

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ScienceOpen disciplines: Parasitology

Keywords: agricultural chemicals, sublethal concentrations, life history traits, anopheles arabiensis, culex quinquefasciatus

Agricultural chemicals: life changer for mosquito vectors in agricultural landscapes?

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Abstract

Background

Methods

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Conclusions

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Malaria vaccine development

Most cited references 65

Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya

Chemical ecology and behavioral aspects of mosquito oviposition.

Impact of irrigation on malaria in Africa: paddies paradox.

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