The Invasive American Weed Parthenium hysterophorus Can Negatively Impact Malaria Control in Africa

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.

Fig 1. Probing and survival on intact plant.

A) Invasive weed, Parthenium hysterophorus, B) Female Anopheles gambiae probing on the flowers of P. hysterophorus, and C) Proportion of female An. gambiae surviving after exposure to different nutritional regimes. Glucose solution (6%) and water were used as positive and negative controls, respectively. The surviving mosquitoes from each treatment were censored on day 15 (survival curves marked + symbol).

Fig 2. Major secondary metabolites and their effect on An. gambiae survival.

A) Mass spectrum and chemical structures of three known plant metabolites detected in the mid-guts of mosquitoes: parthenin from P. hysterophorus; ricinine from R. communis, and phenylheptatriyne from B. pilosa; B) Proportion of female An. gambiae surviving after exposure to different plant toxins detected in mosquito mid-guts. Glucose solution (6%) and water were used as positive and negative controls, respectively, with the toxins dissolved in 6% glucose solution. The toxins were presented dissolved in 6% glucose solution and acetone. The surviving mosquitoes from each treatment were censored on day 8 (survival curves marked + symbol).

Fig 3. Energy reserves (sugar, glycogen and lipid content) of female An. gambiae exposed to different nutritional regimes after 7 days.

Bars capped with different letters are significantly different.