PUPAL HABITAT PRODUCTIVITY OF ANOPHELES GAMBIAE COMPLEX
MOSQUITOES IN A RURAL VILLAGE IN WESTERN KENYA
FRANCIS M. MUTUKU, M. NABIE BAYOH, JOHN E. GIMNIG, JOHN M. VULULE, LUNA KAMAU,
EDWARD D. WALKER,* EPHANTUS KABIRU, AND WILLIAM A. HAWLEY
Department of Zoology, Kenyatta University, Nairobi, Kenya; Centre for Vector Biology and Control Research, Kenya Medical
Research Institute, Kisumu, Kenya; Department of Molecular Genetics and Microbiology, Michigan State University, East Lansing,
Michigan; Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
Abstract. The productivity of larval habitats of the malaria vector Anopheles gambiae for pupae (the stage preceding
adult metamorphosis) is poorly known, yet adult emergence from habitats is the primary determinant of vector density.
To assess it, we used absolute sampling methods in four studies involving daily sampling for 25 days in 6 habitat types
in a village in western Kenya. Anopheles gambiae s.s. comprised 82.5% of emergent adults and Anopheles arabiensis the
remainder. Pupal production occurred from a subset of habitats, primarily soil burrow pits, and was discontinuous in
time, even when larvae occupied all habitats continuously. Habitat stability was positively associated with pupal pro-
ductivity. In a dry season, pupal productivity was distributed between burrow pits and pools in streambeds. Overall,
these data support the notion that source reduction measures against recognizably productive habitats would be a useful
component of an integrated management program for An. gambiae in villages.
INTRODUCTION
Larvae and pupae of Africa’s primary malaria vector,
Anopheles gambiae, are usually found in small, temporary,
sunlit, and turbid pools created by human or animal activ-
ity.
1–4
The transient nature of these numerous habitats,
coupled with the rapid development rate of larvae, makes
difficult the process of sampling of larvae and pupae and
interpretation of the meaning of sampling data. The conse-
quent lack of quantitative information on habitat productivity
has allowed to remain largely unchallenged the assumption
that all habitats receiving eggs and occupied by larvae are
productive for adults,
5,6
an assumption that has been thor-
oughly examined and placed in epidemiologic context for
population dynamics of Aedes aegypti and dengue virus trans-
mission.
7
Simulation modeling suggests that source reduction
in the sense of habitat elimination would lower transmission.
6
Several lines of evidence are needed to assess the feasibility
of larval control or source reduction for An. gambiae: 1) as-
sessment of the abundance of different types of habitats, 2)
measurement of the productivity of each habitat type, and 3)
knowledge of the way in which habitats of different types are
formed, and the social utility or lack thereof of each habitat
type. The first two measures are quantitative sampling prob-
lems and are addressed in the current paper. The last question
is primarily sociological and is addressed separately.
8
The ob-
jective of the current study was to estimate habitat-specific
pupal productivity of An. gambiae s.l. in a western Kenya
village. From such empirical observations, it might be possible
to determine the extent to which habitat productivity for An.
gambiae can be predicted generally in a typical village. The
feasibility of a source reduction program could logically be
assessed based on such knowledge.
MATERIALS AND METHODS
Study site. The study was conducted in Kisian, a rural vil-
lage located 15 km west of Kisumu town, western Kenya.
Geography, demography, climate, and agriculture are de-
scribed elsewhere.
8–10
In terms of hydrology, surface water
drains well from steep hillsides to an alluvial plane near the
shores of Lake Victoria, which forms the southern border of
the village.
8
Streams meander through the village and empty
into the lake. Malaria is highly endemic in this region, with
transmission occurring throughout the year. The principal
mosquito vectors in the area are Anopheles gambiae and
Anopheles funestus Giles with Anopheles arabiensis playing a
secondary role.
10
Larval habitats of An. gambiae s.l. were
located, censused, mapped, and described elsewhere.
8
Productivity. There were four sampling series in this study.
For each study, a set of habitats was sampled daily for 25 days.
Representative habitats of each type were chosen, in 6 rec-
ognizable categories illustrated elsewhere: 1) soil burrow pits,
2) drainage channels, 3) tire tracks, 4) aggregations of hoof
prints, 5) temporary rain pools, and 6) pools in streambeds.
The sampling periods for the first two sampling series were in
the short rainy season (November–December, 2002, called
Study 1); and the dry season after the short rains (January–
February, 2004; Study 2). Different habitats were selected for
Study 1 (categories 1 through 5) and Study 2 (categories 1, 2,
and 5), owing to the temporary nature of many habitats and
to broaden the study to include pools in streambeds, which
were nonexistent in Study 1 because water in streambeds was
flowing. Sampling was accomplished with a quantitative sys-
tem, involving absolute area sampling and whole habitat cen-
sus. Briefly, an area sampler was used, consisting of a plastic
cylinder 10 cm in diameter (area 78.5 cm
2
) and 12 cm in
height. At every habitat, the sampler was pressed in the sub-
strate such that it could support itself or, if this was not pos-
sible, it was held firmly down into the mud or sand until
sampling was done. Placement of the sampler was systematic
(i.e., based on visual presence of larvae) and was not random
relative to other locations in the habitat. Larvae enclosed in
the sampler were transferred by pipette into a bowl where
they were counted and sorted into their respective instars and
then returned into the habitat. To measure habitat pupal pro-
ductivity, pupae were collected both within the area sampler
and in the remaining part of the habitat as a census by local
area search by eye and with pipette. Pupae were placed in
small tubes with water and transported to the laboratory.
* Address correspondence to Edward D. Walker, Department of
Microbiology and Molecular Genetics, Michigan State University,
East Lansing, MI 48824. E-mail walker@msu.edu
Am. J. Trop. Med. Hyg., 74(1), 2006, pp. 54–61
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene
54