This project concerns a never-investigated dimension of the world's most important insect. Until now, virtually nothing was known about the existence or significance of a plant-vector relationship in African malaria. It was assumed that plants play no significant role in adult Anopheles gambiae biology and therefore would be irrelevant to Plasmodium transmission. Our team, funded mainly by a 2-year R21 exploratory NIH grant, now has credible evidence to the contrary, both from lab and field. For the first time, we have direct evidence of frequent An. gambiae plant-sugar feeding in the field. We also have experimental results on the timing of nectar feeding, host-plant preferences, volatile plant attractants, plant-inhibited Plasmodium development, severely reduced insemination ability of plantdeprived males, and reduced egg production and survival of females lacking plant sugars, but increased biting frequency. What's more, the mosquito shares its plant hosts with a predator that specializes in killing Anopheles. These discoveries put an entirely new spin on An. gambiae ecology. Is the mosquito-plant connection important to malaria? Does it have practical applications for transmission suppression, or for genetic methods of control? Quite likely, so. All of these interconnected plant-focused topics need serious attention and are addressed in this proposal. There exists an extraordinary opportunity to proceed with a novel plant-mosquito investigation, keeping the assembled R21 team and its expertise intact. The first major step will be to determine, through outdoor screenhouse experiments in semi-natural conditions, how big is the effect of the mosquito's natural host plants on 2 key features of vector biology: 1) reproductive output and 2) vectorial capacity. Put as questions: In the field, will plant-host scarcity substantially compromise a male's insemination ability and competitiveness and substantially decrease a female's egg output? And in the field, will plant-host scarcity reduce female survival and, paradoxically, also reduce biting frequency, thereby significantly diminishing vectorial capacity? The answers have practical value, because selective manipulation of plant communities may depress pathogen transmission through both direct and indirect effects and may favor genetic methods of malaria control. Furthermore, innate and learned plant attractants, plant-derived Plasmodium inhibitors, and plant-attracted predators all may have practical value. The plant-dependency angle offers some special vulnerabilities of the Plasmodium-Anopheles relationship, each a potential Achilles'heel: a) inadequate insemination by males, b) reduced female survival and fecundity, and c) vector incompetence.

Public Health Relevance

Plants appear to play a crucial role in the success of the African mosquito that transmits most malaria. If this plant dependency holds true under natural conditions, both plant communities and mosquito populations can be manipulated in ways that drastically reduce their ability to spread this disease pathogen.

Agency
National Institute of Health (NIH)
Institute
National Institute of Allergy and Infectious Diseases (NIAID)
Type
Research Project (R01)
Project #
5R01AI077722-04
Application #
8320883
Study Section
Vector Biology Study Section (VB)
Program Officer
Costero, Adriana
Project Start
2009-08-15
Project End
2014-08-31
Budget Start
2012-09-01
Budget End
2014-08-31
Support Year
4
Fiscal Year
2012
Total Cost
$581,617
Indirect Cost
$108,250
Name
Ohio State University
Department
Zoology
Type
Schools of Arts and Sciences
DUNS #
832127323
City
Columbus
State
OH
Country
United States
Zip Code
43210
Ebrahimi, Babak; Jackson, Bryan T; Guseman, Julie L et al. (2018) Alteration of plant species assemblages can decrease the transmission potential of malaria mosquitoes. J Appl Ecol 55:841-851
Zappia, Simon P W; Chubaty, Alex M; Roitberg, Bernard D (2018) State-dependent domicile leaving rates in Anopheles gambiae. Malar J 17:25
Carvell, Georgina E; Jackson, Robert R; Cross, Fiona R (2017) Ontogenetic shift in plant-related cognitive specialization by a mosquito-eating predator. Behav Processes 138:105-122
Cross, Fiona R; Jackson, Robert R (2016) The execution of planned detours by spider-eating predators. J Exp Anal Behav 105:194-210
Otienoburu, Philip E; Nikbakhtzadeh, Mahmood R; Foster, Woodbridge A (2016) Orientation of Anopheles gambiae (Diptera: Culicidae) to Plant-Host Volatiles in a Novel Diffusion-Cage Olfactometer. J Med Entomol 53:237-40
Nikbakhtzadeh, M R; Terbot 2nd, J W; Foster, W A (2016) Survival Value and Sugar Access of Four East African Plant Species Attractive to a Laboratory Strain of Sympatric Anopheles gambiae (Diptera: Culicidae). J Med Entomol :
Jackson, B T; Stone, C M; Ebrahimi, B et al. (2015) A low-cost mesocosm for the study of behaviour and reproductive potential in Afrotropical mosquito (Diptera: Culicidae) vectors of malaria. Med Vet Entomol 29:104-9
Terbot 2nd, John W; Nikbakhtzadeh, Mahmood R; Foster, Woodbridge A (2015) Evaluation of Bacillus thuringiensis israelensis as a Control Agent for Adult Anopheles gambiae. J Am Mosq Control Assoc 31:258-61
Cross, Fiona R; Jackson, Robert R (2015) Solving a novel confinement problem by spartaeine salticids that are predisposed to solve problems in the context of predation. Anim Cogn 18:509-15
Nikbakhtzadeh, Mahmood R; Terbot 2nd, John W; Otienoburu, Philip E et al. (2014) Olfactory basis of floral preference of the malaria vector Anopheles gambiae (Diptera: Culicidae) among common African plants. J Vector Ecol 39:372-83

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