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ARS Home » Southeast Area » Gainesville, Florida » Center for Medical, Agricultural and Veterinary Entomology » Chemistry Research » Research » Publications at this Location » Publication #321500
Title: The invasive American weed parthenium hysterophorus can negatively impact malaria control in Africa

Author
item NYASEMBE, VINCENT - International Centre Of Insect Physiology And Ecology
item CHESETO, XAVIER - International Centre Of Insect Physiology And Ecology
item KAPLAN, FATMA - University Of Florida
item FOSTER, WOODBRIDGE - The Ohio State University
item Teal, Peter
item TUMLINSON, JAMES - Pennsylvania State University
item BORGEMEISTER, CHRISTIAN - University Of Bonn
item TORTO, BALDWYN - International Centre Of Insect Physiology And Ecology

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/23/2015
Publication Date: 9/14/2015
Citation: Nyasembe, V.O., Cheseto, X., Kaplan, F., Foster, W.A., Teal, P.E., Tumlinson, J.H., Borgemeister, C., Torto, B. 2015. The invasive American weed parthenium hysterophorus can negatively impact malaria control in Africa. PLoS One. doi:10.1371/journal.pone.0137836.

Interpretive Summary: The changing climatic conditions have negatively impacted on human health through emergence and resurgence of infectious diseases, spread of vector borne diseases to new geographical areas and the spread of invasive plant species [1–3]. The spread of invasive plant species is particularly of interest since they often result in widespread replacement of indigenous flora [4,5]. A particularly notorious example is Parthenium hysterophorus (Asteraceae). Native to the subtropics and tropics of North and South America, it has now invaded South, East and Central Africa, Asia and Australia, extensively spreading over both cultivated and pastoral lands [6,7]. The high biotic potential and allelopathic properties of P. hysterophorus favour its fast spread and replacement of other plant species within new areas of distribution [8–11]. A major concern is the potential toxic effects of P. hysterophorus on human and livestock health, with some governments such as those in Australia, Uganda and Ethiopia establishing national agencies to help curb its spread [12–14]. The weed grows well in malaria endemic areas of East Africa and was shown to be one of the preferred host plants for the Afrotropical malaria vector Anopheles gambiae [15,16]. Although An. gambiae was shown to be highly attracted to and feed frequently on P. hysterophorus, there was no evidence of it improving survival and fecundity of these vectors. This raised the question as to what attracts mosquitoes to the plant [15]? In general, little is known about the impact of invasive plants on disease-transmitting arthropods. Knowledge of these interactions can serve as a pre-requisite to better assess the potential contribution of invasive plants to the dynamics of vector-borne diseases and associated public health risks. The success of mosquitoes as disease vectors is dependent on their prolonged survival, ability to feed on multiple hosts and support pathogen development [17]. Feeding on nectar and honeydew enhances mosquito longevity and also serves as a ready source of energy for flight [18,19]. Evidence of sugar feeding in An. gambiae continues to accumulate [15,18,20,21], and the significance of sugar availability within Anopheles mosquitoes’ localities in relation to their population dynamics and vector potential has gained considerable attention [22–26]. In this study, the contribution of the highly aggressive invasive Neotropical weed P. hysterophorus and two other adapted plant species that are abundant in malaria endemic regions in western Kenya, Bidens pilosa (Asteraceae) and Ricinus communis (Euphorbiaceae), to the survival and energy reserves of An. gambiae was investigated. Since the chemical analysis of mid-gut contents of mosquitoes fed on the three plant species revealed that they ingested plant specific secondary metabolites, some of which have been shown to be toxic [27–29], we isolated and identified these secondary metabolites from the three plant species as follows: the sesquiterpene lactone parthenin from P. hysterophorus, the alkaloid ricinine from R. communis, and the polyyne 1-phenylhepta-1, 3, 5-triyne (henceforth referred to as phenylheptatriyne) from B. pilosa. The compounds were then tested for their effect on vector survival. The fate of these metabolites once ingested by An. gambiae was further evaluated by monitoring their presence in the mid-gut at 24, 48 and 72 h post feeding. In addition, four ingested plant sugars detected in the gut of mosquitoes that had fed on the three plant species were identified and quantified to confirm nectar feeding.

Technical Abstract: The direct negative effects of invasive plant species on agriculture and biodiversity are well known, but their indirect effects on human health, and particularly their interactions with disease-transmitting vectors, remains poorly explored. This study sought to investigate the impact of the invasive Neotropical weed Parthenium hysterophorus and its toxins on the survival and energy reserves of the malaria vector Anopheles gambiae. In this study, we compared the fitness of An. gambiae fed on three differentially attractive mosquito host plants and their major toxins; the highly aggressive invasive Neotropical weed Parthenium hysterophorus (Asteraceae) in East Africa and two other adapted weeds, Ricinus communis (Euphorbiaceae) and Bidens pilosa (Asteraceae). Our results showed that female An. gambiae fitness varied with host plants as females survived better and accumulated substantial energy reserves when fed on P. hysterophorus and R. communis compared to B. pilosa. Females tolerated parthenin and 1-phenylhepta-1, 3, 5-triyne, the toxins produced by P. hysterophorus and B. pilosa, respectively, but not ricinine produced by R. communis. Given that invasive plants like P. hysterophorus can suppress or even replace less competitive species that might be less suitable host-plants for arthropod disease vectors, the spread of invasive plants could lead to higher disease transmission. Parthenium hysterophorus represents a possible indirect effect of invasive plants on human health, which underpins the need to include an additional health dimension in risk-analysis modelling for invasive plants.