African Water Storage Pots for the Delivery of the Entomopathogenic Fungus
Metarhizium anisopliae to the Malaria Vectors Anopheles gambiae s.s. and
Anopheles funestus
Marit Farenhorst, Daniela Farina, Ernst-Jan Scholte, Willem Takken, Richard H. Hunt, Maureen Coetzee, and
Bart G. J. Knols*
Laboratory of Entomology, Wageningen University and Research Centre, Wageningen, The Netherlands; Plant Protection Service,
Wageningen, The Netherlands; Vector Control Reference Unit, National Institute for Communicable Diseases, Johannesburg, South
Africa; Animal, Plant and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa; School of
Pathology, University of the Witwatersrand, Johannesburg, South Africa
Abstract. We studied the use of African water storage pots for point source application of Metarhizium anisopliae
against the malaria vectors Anopheles gambiae s.s. and An. funestus. Clay pots were shown to be attractive resting sites
for male and female An. gambiae s.s. and were not repellent after impregnation with fungus. M. anisopliae was highly
infective and virulent after spray application inside pots. At a dosage of 4 × 10
10
conidia/m
2
, an average of 95 ± 1.2%
of An. gambiae s.s. obtained a fungal infection. A lower dosage of 1 × 10
10
conidia/m
2
infected an average of 91.5 ± 0.6%
of An. gambiae s.s. and 91.8 ± 1.2% of An. funestus mosquitoes. Fungal infection significantly reduced mosquito
longevity, as shown by differences between survival curves and LT
50
values. These pots are suitable for application of
entomopathogenic fungi against malaria vectors and their potential for sustainable field implementation is discussed.
INTRODUCTION
Human malaria, transmitted by female mosquitoes of the
genus Anopheles, is a major public health challenge in devel-
oping countries. Malaria is Africa’s major cause of mortality
in those younger than 5 years of age and constitutes 10% of
the continent’s overall disease burden.
1
Anopheles gambiae
s.s. Giles and An. funestus Giles are two of the most important
malaria mosquito vectors in sub-Saharan Africa in terms of
human morbidity and mortality, with high susceptibility to
Plasmodium infection and high degrees of anthropophily.
2
An. gambiae s.s. has a continent-wide distribution, occupies
temporary aquatic habitats, and is considered to be one of the
most efficient species to develop and transmit malaria para-
sites.
3,4
An. funestus is widely distributed throughout tropical
Africa, occupies a wide range of ecological niches, and ex-
tends its activity even into the dry season when other malaria
mosquito vectors are present in much reduced densities.
5,6
Current vector control methods against adult mosquito
populations are mainly based on insecticide application, par-
ticularly indoor residual spraying (IRS) and insecticide-
treated bednets (ITNs). However, insecticide resistance poses
a serious threat to sustainable insecticide-based vector control
in many African countries.
7
Both An. gambiae and An. fu-
nestus populations are showing increasing levels of resistance
to one or more of the insecticide classes used in vector con-
trol.
1
There is a pressing need, therefore, to develop novel
vector control methods that can complement or replace ex-
isting intervention tools.
Metarhizium anisopliae and Beauveria bassiana are hypho-
mycetous insect-pathogenic fungi of which the conidia can
infect insects by penetrating the cuticle, without the need for
ingestion, and kill them within several days.
8
Metarhizium
spp. and Beauveria spp. are endemic worldwide and are not
harmful to birds, fish, or mammals,
9
and because of their
opportunistic nature, lack of association with humans, and
inability to survive at human body temperatures, are consid-
ered to cause no human health risks (S. De Hoog, personal
communication). The US Environmental Protection Agency
has declared no risk to humans when using products contain-
ing M. anisopliae, based on toxicity tests.
10
Hyphomycetous
fungi can be cost-effectively mass-produced,
11
and several
strains are already commercially available
12,13
and in use for
the control of agricultural and veterinary pests.
14,15
Several studies have shown that conidia of M. anisopliae
and B. bassiana are pathogenic to adult Anopheles, Aedes,
and Culex mosquitoes, because fungal infection significantly
reduces their longevity.
16–18
This implies a high potential for
use as biological control agents against vectors transmitting
malaria, dengue, Chikungunya, and other mosquito-borne
diseases. Besides a reduction in daily survival rates, fungal
infection has also shown other effects that are likely to affect
malaria transmission. First, infection of Anopheles with these
fungi has an inhibitory effect on the development of malaria
parasites in mosquitoes.
19
Second, fungal infection reduces a
mosquito’s feeding propensity and fecundity.
20
Another im-
portant potential benefit of biological vector control with en-
tomopathogenic fungi is that fungi are slow-killing agents,
which is considered to reduce the selection pressure on resis-
tance formation by allowing adult mosquitoes partial repro-
ductive success.
21
An international consortium of seven research institutes
was formed in 2005, with the main aim of reducing the burden
of mosquito-borne diseases through the development and de-
livery of novel and sustainable approaches of adult mosquito
control based on fungi.
22
Although research on fundamental
aspects regarding fungus production and fungus–mosquito in-
teractions is underway, gaps remain between the scientific
laboratory discoveries and a successful implementation of
fungi in the field. Practical issues concerning the conidial vi-
ability, infectivity, formulation, and delivery of fungi need to
be resolved before progress toward field research can be
made.
23
The choice of delivery method will be an important
determinant of the overall effectiveness of a fungus-based
vector control method. An optimal delivery system requires
* Address correspondence to Bart G. J. Knols, Laboratory of Ento-
mology, PO Box 8031, 6700 EH, Wageningen University and Re-
search Centre, Wageningen, The Netherlands. E-mail: bart.knols@
wur.nl
Am. J. Trop. Med. Hyg., 78(6), 2008, pp. 910–916
Copyright © 2008 by The American Society of Tropical Medicine and Hygiene
910