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Am. J. Trop. Med. Hyg., 68(6), 2003, pp. 748-752
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

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ENHANCEMENT OF DEVELOPMENT OF LARVAL ANOPHELES ARABIENSIS BY PROXIMITY TO FLOWERING MAIZE (ZEA MAYS) IN TURBID WATER AND WHEN CROWDED

YEMANE YE-EBIYO, RICHARD J. POLLACK, ANTHONY KISZEWSKI, AND ANDREW SPIELMAN
Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, Massachusetts; Center for International Development, Kennedy School of Government, Harvard University, Cambridge, Massachusetts


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To determine whether proximity to flowering maize enhances the development of larval anopheline mosquitoes breeding in turbid water and when crowded, we evaluated the development of larval Anopheles arabiensis under various conditions of turbidity, larval density, and proximity to pollen-shedding maize in simulated breeding puddles in a malaria-endemic site. In naturally formed puddles, water turbidity, as well as larval density, increased as the rainy season progressed. In sites remote from flowering maize, more pupae developed and the resulting adults were larger in relatively clear water than in turbid water, and larval crowding inhibited development. In close proximity to flowering maize, however, larval development was little affected by water turbidity and larval crowding. Larvae of this member of the African An. gambiae complex of mosquitoes develop readily in turbid water and when crowded, provided that their breeding sites are located where maize pollen is abundant.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The larval stages of the mosquitoes that comprise the Anopheles gambiae complex of species frequently dwell in transient bodies of water in which suspended soil particles are abundant,1 particularly towards the end of the rainy season when these puddles begin to contract. Although the presence of these mosquitoes correlates with turbidity,2 their development does not depend on the presence of suspended soil particles.3 They exploit turbid water as frequently as clear water. In contrast, many other kinds of mosquitoes appear to develop more readily in clear water than in turbid water.4 Such turbid breeding media present difficulties because insects feeding there might ingest large volumes of soil particles, and such inert, non-nutritive material would tend to overwhelm the ability of larvae to imbibe nutritious material. Few other multicellular organisms share this peculiar ecologic niche.

Larval mosquitoes feed in diverse ways; anophelines mainly harvest particles suspended at the water’s surface. Pollen5 as well as algae and bacteria6,7 contribute to their development. Maize pollen, in particular, constitutes an important source of nutriment for An. arabiensis in Ethiopia.5 Larvae appear to locate such pollen by following the strand of viscous material that descends from pollen grains that settle on the water’s surface, a strategy that seems well suited for selective feeding in a field of non-nutritive particles. Such a feeding strategy might place a premium on the density of pollen or algae present in the breeding site, and several variables might alter these relationships including proximity to flowering maize, algal density, the presence of other microorganisms and organic particles in the medium and density of competing larvae. The relationship between water turbidity and food availability for members of the An. gambiae complex of vector mosquitoes remains unknown.

It may be that larvae of the An. gambiae complex of mosquitoes require access to more food particles in turbid water than in clear water, and maize pollen may provide a particularly rich source of such food in nature. Accordingly, we determined whether larvae contained in turbid water may develop more successfully where food is readily available than in crowded or food-deprived situations. In particular, we compared the development of larval An. arabiensis in water containing graded concentrations of suspended particles, graded larval densities, and with varying proximity to maize.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This study was conducted in a semi-arid malaria-endemic district in central Ethiopia where An. arabiensis is the principal malaria vector and temporary rain pools constitute the main breeding sites. Experiments were performed in Zwai in the Great Rift Valley at an altitude of 1,640 meters above sea level and at 9°N latitude. The site is generally semi-arid and the terrain is relatively flat. Its vegetation mainly consists of acacia and low thorn bush, and is subject to intensive grazing and agriculture. Annual rainfall is approximately 740 mm, with one main rainy season between June and September. Rainfall is most intense during July.

Anopheles arabiensis is the sole known member of the An. gambiae complex present in the vicinity of Zwai8, a finding that was confirmed by polymerase chain reaction analyses.9 Although An. pharoensis is also abundant in the region, none of the adults produced during the course of these experiments bore the distinctive morphologic characteristics of these mosquitoes. Their larvae exploit permanent bodies of water and would not be present in the transient puddles from which our experimental materials were harvested. The only other member of the An. gambiae complex reported from Ethiopia is An. quadriannulatus, which is restricted to limited foci in the southern and northwestern part of the country.10,11 Anopheles gambiae s.s. has never been reported from Ethiopia.

First instar larval An. arabiensis that were used in these experiments were collected from natural breeding sites located near Zwai, separated from any culicine larvae that may have been present, and counted in batches of 100 into holding pans. Larvae collected from several breeding sites were pooled in large containers before they were counted and placed in smaller containers for transport to our experimental sites.

For experimental observations, plastic pans 40 cm wide and 15 cm deep were half-buried in the ground and approximately two liters of washed sand were placed in each. Pans were then filled with three liters of water of specified turbidity, and specified numbers of larval mosquitoes were placed in them. All pans were covered with 16-mesh household screening each evening to prevent other mosquitoes from depositing eggs in the enclosed water. Each site was fenced to exclude animals, and a roof of corrugated iron sheeting was erected over each array of pans to exclude rain when necessary. Water was added daily to replenish that which was lost due to evaporation and to maintain a uniform water level.

To provide stocks of turbid water, water was taken from naturally formed puddles in the vicinity of Zwai and stored in open buckets for six days to allow for evaporation to increase turbidity. This stock was then diluted with clear lake water to provide graduated turbidities of 8,000, 4,000, 2,000, 1,000, 500, and 15 nephelometric turbidity units (NTU). Turbidity was measured by means of a portable battery-operated turbidimeter (DRT-15CE; HF Scientific, Inc., Fort Myers, FL).

Filamentous green algae for use in these experiments was harvested from the margin of a nearby lake (Lake Zwai) and allowed to settle in basins. After one day, 20-mL samples of the resulting sedimented material were placed in experimental pans, as specified.

To record the size of adult mosquitoes deriving from these experiments, the left wing of each female was removed, spread in a drop of distilled water on a microscope slide, and its length was measured from the alular notch to the tip of the wing margin, excluding the fringe scale, using an ocular micrometer fitted to a dissecting microscope.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In a preliminary series of observations, we described the turbidity of the water that puddled naturally near Zwai when larval An. arabiensis were most abundant. We recorded the mean size, turbidity, water temperature, and larval density of seven puddles that remained standing for three months and that contained some of these larvae. The surface area of these puddles was most extensive in July 2001, soon after the rains commenced, and diminished as the season progressed (Table 1Go). Puddled water initially was moderately turbid (2,730 NTU), became relatively clear (345 NTU) within a few weeks and intensely turbid (9,750 NTU) after the rains ceased and the diameter of the pools diminished. The noon temperature of the water in these puddles frequently approached 36°C. Larval density increased as the rainy season progressed, reaching 200 per liter at the margins of the puddles and was greatest in opaque water that approached 10,000 NTU.


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TABLE 1
Characteristics of seven naturally formed puddles that contained larval Anopheles arabiensis in the vicinity of Zwai, Ethiopia during July through September*
 
We then determined whether water turbidity and the nature of the food available to these larvae correlates with their development. Three arrays of seven water-filled pans were placed in the study site, each containing water of a different turbidity (15–8,000 NTU). One array was placed within five meters of a field of flowering maize and the others were placed approximately 100 meters from the edge of any such field. Green filamentous algae were added into one array of pans that was located remote from the maize field. The other array received no such food supplement. Each pan was stocked with 100 first instar larval An. arabiensis. Pupae were removed daily and adults were permitted to emerge in the laboratory where the lengths of their wings were measured. Larvae reared in clear water developed readily, regardless of the availability of maize pollen or algal supplementation, and those reared near flowering maize were least inhibited by excessive turbidity (Figure 1Go). Few pupae developed from larvae that were reared in turbid water that was distant from flowering maize and that received no algal food supplementation. The largest adults developed in water of moderate turbidity (500–1,000 NTU), regardless of proximity to maize or algal supplementation, and adults derived from larvae developing in more turbid water were smaller (Table 2Go). Larvae developing in the vicinity of flowering maize, however, produced adults that were larger than those developing away from maize and with or without algal supplement but in water of similar turbidity. Those reared with algal supplements produced somewhat smaller adults (by a 0.32-mm increment; 95% confidence interval [CI] = 0.29–0.35), and those that lacked either food source produced the smallest adults (by a 0.48-mm increment; 95% CI = 0.43–0.52). Although larval An. arabiensis develop best in moderately turbid water, excessive turbidity impedes the production of numerous and large adults, and proximity to flowering maize compensates for this developmental failure.



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  		    FIGURE 1. Effect of turbidity on the proportion of larval Anoph-eles arabiensis developing to the pupal stage under conditions of differing nutriment availability. NTU = nephelometric turbidity units. Bars show the mean ± SE.

 

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TABLE 2
Effect of water turbidity on the development of female adults developing from 100 larval Anopheles arabiensis subject to conditions of differing nutriment availability*
 
To determine whether crowding inhibits larval development and whether food availability ameliorates this effect, we recorded the size of adult An. arabiensis reared under conditions of nutrient availability similar to those applied in the earlier experiment. Water turbidity was held constant at 2,000 NTU, somewhat greater than what proved to be optimal in those experiments. Pupal productivity was recorded each day by harvesting all pupae present in the site. Crowded larvae that were reared in moderately turbid water located close to flowering maize produced pupae more frequently than did larvae that were located remote from such a food source but that received algal food supplements and far more than larvae that were denied both pollen and algal food (Figure 2Go). Larvae in sparsely populated breeding sites developed readily, regardless of food supplementation. Adult size correlated inversely with the density of the larvae from which they developed (Table 3Go). Adults derived from sites remote from the maize and that received no algal supplement were the smallest (mean wing size was 0.64 mm smaller; 95% CI = 0.60–0.69) and those receiving algae (mean wing size was 0.46 mm lower; 95% CI = 0.42–0.49) were smaller than those in close proximity to pollen releasing maize and under similar conditions of crowding. The inhibitory effect of crowding was most evident in adults that were reared remote from flowering maize and that received no algal food supplement. Although crowding inhibits the developmental of larval An. arabiensis, proximity to flowering maize compensates for this failure to produce numerous and large adults.



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  		    FIGURE 2. Effect of larval density on the proportion of larval Anopheles arabiensis developing to the pupal stage under conditions of differing nutriment availability. Bars show the mean ± SE.

 

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TABLE 3
Effect of larval density on the size of adult females developing from first-stage larval Anopheles arabiensis subject to conditions of differing nutriment availability in turbid water (2,000 NTU)*
 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The quality of the environment in which insects develop influences the quality of the resulting adults. The beetle Rhizoptera dominica, for example, develops more effectively and produces more eggs when reared from larvae that are well nourished and not crowded.12 In the case of mosquitoes, food availability is particularly important in determining larval developmental success, rapidity of development, and the size of the resulting adults.13–16 Large adults live longer than those that are smaller, producing more eggs and imbibing more blood, properties that crucially influence the force of malaria transmission.17–19 Various environmental, physiochemical, and biologic factors may influence the suitability of a site for larval anopheline mosquitoes.1–3 The pollen produced by maize, in particular, provides nutriment that appears to be important for the development of An. arabiensis.5 Longer-lived mosquitoes, of course, would contribute most powerfully to the force of transmission of any pathogens that they may carry. Well-nourished larval mosquitoes produce adults that most effectively transmit infection.20

The presence of inert particles suspended in the larval environment may prevent larval mosquitoes from feeding effectively. Anopheles gambiae complex mosquitoes might be particularly vulnerable to such rearing conditions because they generally exploit turbid puddles of rainwater that contract and become increasingly muddy toward the end of the rainy season. Anopheline larvae, similar to those of other mosquitoes, appear to ingest particles in their aquatic habitat indiscriminately,21 and it is not known how the concentration of inert particles in the larval habitat affects the ability of these mosquitoes to extract nutriment. Water turbidity results largely from suspended organic and inorganic particles in the water column. Turbidity-induced changes that can occur in a water body may affect the diversity of the aquatic community.22 Because light fails to penetrate turbid water, few photosynthetic organisms develop there, and this restricts food availability for many invertebrates.23 In our study site, turbidity appears mainly to be due to soil-derived silt. Turbidity may also interfere with larval feeding; under experimental conditions, larval An. arabiensis fail to thrive in turbid media unless food is delivered directly to the water’s surface (Ye-Ebiyo Y, unpublished data).

Although the abundance of these vector insects appears to correlate with increasing turbidity, such larvae may merely accumulate there because they develop slowly in such water. Indeed, our observations indicate that larval An. arabiensis develop to the pupal stage more readily in relatively clear water than in turbid water, but only when access to food is limited. In the presence of abundant food that is concentrated at the water’s surface, larval development is hardly constrained by turbidity, and maize pollen would provide such nutriment. Although the presence of algae in the medium similarly promotes development, the resulting adults are much smaller than are those having access to maize pollen.

The effect of larval density on the developmental success of An. arabiensis remains controversial. In a laboratory setting, adult body size of An. gambiae s.s. depends on larval density and food quantity,24 and An. gambiae s.s. competes with An. arabiensis when these mosquitoes are reared in the same container.25 However, survival of larval An. gambiae s.s. in nature appears to be hardly affected by crowding.2 Crowded larvae merely extend their development time and results in smaller adults. Our observations confirm that crowded larvae produce relatively small adults, but indicate that pupal productivity among crowded larvae is inhibited where food is scarce. In proximity to flowering maize, larvae develop to the pupal stage effectively and rapidly, regardless of turbidity. The development of larvae when densely crowded, however, is inhibited under such conditions. The presence of alga in the medium only partially compensates for crowding. Crowded larvae readily develop near flowering maize. Larval development thus appears to be inhibited to a certain extent by competition for food resources rather than other factors associated with overcrowding.

Larval An. gambiae s.l. frequently become dense in the small puddles of rainwater that characterize the breeding habitats of these mosquitoes.26 In the relatively dry Ethiopian environment, larval An. arabiensis are present mainly in small, temporary rain pools that are free of vegetation. At the beginning of the rainy season, or upon resumption of the rains after a brief period of interruption, numerous rain puddles develop throughout our study site. The turbidity of these puddles varies according to the kind of soil in the site and the dimensions of the puddle. Such water accumulations occasionally begin to harbor larvae within a few days after the onset of the seasonal rains. At the beginning of the rainy season, larval density appears to be inversely proportional to the frequency of temporary pools. The more numerous are these rain puddles, the fewer the larvae in each. However, toward the end of the rainy season, or when the seasonal rains are interrupted, such puddles become less numerous and those that remain begin to contract. As a result, larval density increases in those puddles that remain. Larval density frequently appears to exceed the carrying capacity of these breeding sites, thereby retarding larval development.

The abundance of adult mosquitoes peaks toward the middle of the rainy season when puddles are most plentiful, water is least turbid, and maize begins to shed pollen. As the seasonal rains diminish, breeding sites become more turbid, and larval density in the few sites that remain increases, mainly due to continued oviposition in these diminishing breeding sites and a concentration of those larvae that failed to develop in their increasingly unfavorable environment. As a result, the abundance of emerging adults sharply decreases, thereby signaling the end of the season of intensive vector proliferation and malaria transmission in the region.

The muddy water that accumulates in the borrow pits, footprints, and tire tracks that mark many African villages provides the ideal developmental niche for various members of the An. gambiae complex of mosquitoes. Their anthropophagic requirement is satisfied by the proximity of sleeping people. Maize cultivation in Africa has intensified greatly during the 20th century, and the introduction of novel hybrid varieties appears to have accelerated this trend (McCann J, unpublished data). The members of the An. gambiae complex of mosquitoes that so effectively exploit the disturbed environments that characterize African villages now find in these sites a ready source of food that will potentiate their development and contribute to the force of transmission of malaria.

Received March 25, 2002. Accepted for publication March 3, 2003.

Acknowledgments: We are grateful to the malaria control team in Zwai and Nazareth (Ethiopia) for their assistance in the fieldwork.

Financial support: This work was supported in part by grant #TW00918 from the Fogarty International Institute, National Institutes of Health.

Authors’ addresses: Yemane Ye-Ebiyo, Richard J. Pollack, Anthony Kiszewski, and Andrew Spielman, Department of Immunology and Infectious Diseases, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02115, Telephone: 617-432-2058, Fax: 617-432-1796, E-mail: aspielma{at}hsph.harvard.edu

Reprint requests: Andrew Spielman, Department of Immunology and Infectious Diseases, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02115.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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