Explaining the host-finding behavior of blood-sucking insects: computerized simulation of the effects of habitat geometry on tsetse fly movement

Abstract

Background: Male and female tsetse flies feed exclusively on vertebrate blood. While doing so they can transmit the diseases of sleeping sickness in humans and nagana in domestic stock. Knowledge of the host-orientated behavior of tsetse is important in designing bait methods of sampling and controlling the flies, and in understanding the epidemiology of the diseases. For this we must explain several puzzling distinctions in the behavior of the different sexes and species of tsetse. For example, why is it that the species occupying savannahs, unlike those of riverine habitats, appear strongly responsive to odor, rely mainly on large hosts, are repelled by humans, and are often shy of alighting on baits?

Methodology/principal findings: A deterministic model that simulated fly mobility and host-finding success suggested that the behavioral distinctions between riverine, savannah and forest tsetse are due largely to habitat size and shape, and the extent to which dense bushes limit occupiable space within the habitats. These factors seemed effective primarily because they affect the daily displacement of tsetse, reducing it by up to ∼70%. Sex differences in behavior are explicable by females being larger and more mobile than males.

Conclusion/significance: Habitat geometry and fly size provide a framework that can unify much of the behavior of all sexes and species of tsetse everywhere. The general expectation is that relatively immobile insects in restricted habitats tend to be less responsive to host odors and more catholic in their diet. This has profound implications for the optimization of bait technology for tsetse, mosquitoes, black flies and tabanids, and for the epidemiology of the diseases they transmit.

Figure 1. Simulated areas covered of visual and olfactory stimuli.

A: areas within a single cell around a lizard and tiny odorless target. B: groups of cells around and near a kudu, pig and large target used with odor.

Figure 2. Effect of band and block width on movement.

Mean displacement after 1000 steps in landscapes in which good habitat was restricted to various widths of bands surrounded by no-go area, or to square blocks in a checker-board with poor habitat. Displacement is expressed as a percent of the displacement in a large block of homogeneous, good habitat.

Figure 3. Effect of bushes on movement.

A: various arrangements of bushes in sections of a band of habitat 50 m (5 cells) wide, surrounded by no-go area. B: displacement after 1000 steps with no bushes (Nil) or bushes in arrangements I–IV, in good habitat consisting of a large block or a band 50 m wide. Displacement is expressed as a percent of the displacement in a large block of good habitat containing no bushes.

Figure 4. Efficacy of various targets at various density.

Percent of the tsetse population killed per hunger cycle by three different types of target at various densities, in a large block of habitat (A) or in a band 10 m wide (B).

Figure 5. Feeding success with various hosts at various density.

Cumulative percent of tsetse that had fed after four days (A) or six days (B), in a large block of habitat or in a band 10 m wide.