A predator from East Africa that chooses malaria vectors as preferred prey

Abstract

Background: All vectors of human malaria, a disease responsible for more than one million deaths per year, are female mosquitoes from the genus Anopheles. Evarcha culicivora is an East African jumping spider (Salticidae) that feeds indirectly on vertebrate blood by selecting blood-carrying female mosquitoes as preferred prey.

Methodology/principal findings: By testing with motionless lures made from mounting dead insects in lifelike posture on cork discs, we show that E. culicivora selects Anopheles mosquitoes in preference to other mosquitoes and that this predator can identify Anopheles by static appearance alone. Tests using active (grooming) virtual mosquitoes rendered in 3-D animation show that Anopheles' characteristic resting posture is an important prey-choice cue for E. culicivora. Expression of the spider's preference for Anopheles varies with the spider's size, varies with its prior feeding condition and is independent of the spider gaining a blood meal.

Conclusions/significance: This is the first experimental study to show that a predator of any type actively chooses Anopheles as preferred prey, suggesting that specialized predators having a role in the biological control of disease vectors is a realistic possibility.

Figure 1. Apparatus for virtual-prey testing.

Spider (not to scale) at top of inclined metal ramp, oriented toward one of two side-by-side virtual mosquitoes. Virtual mosquitoes on small screen (projection screen, see enlarged inset in top right corner) positioned in front of higher end of ramp. Images pass from projector lens (connected to computer; main body of data projector and computer not shown) through second lens (for reducing image size) on to screen. Observer point of view: about 150 degrees from the direct light path from the projector through the projection screen; slightly behind the projection screen at a height of approximately 45 degrees. Inset: virtual mosquitoes in Anopheles resting posture (left) and in non-Anopheles resting posture (right).

Figure 2. Simultaneous-presentation mount tests of sated Evarcha culicivora.

Percentage: spiders that chose prey type at top list of two under bar. E = Evarcha culicivora. J = juvenile. F = adult female. BA = blood-fed Anopheles. SA = sugar-fed Anopheles. Ch = chironomid midge. BC = blood-fed Culex. SC = sugar-fed Culex. Spider body length in mm. N inside each bar. Tests of goodness of fit: chi-square statistic above bar; null hypothesis, 50/50; *** P<0.001.

Figure 3. Simultaneous-presentation mount tests of fasted Evarcha culicivora.

Percentage: spiders that chose prey type at top list of two under bar. E = Evarcha culicivora. J = juvenile. F = adult female. M = male. BA = blood-fed Anopheles. SA = sugar-fed Anopheles. BC = blood-fed Culex. Ch = chironomid midge. Spider body length in mm. N inside each bar. Tests of goodness of fit: chi-square statistic above bar; null hypothesis, 50/50; *** P<0.001.

Figure 4. Simultaneous-presentation virtual-prey tests (blood-fed virtual mosquitoes in Anopheles rest posture and in Culex rest posture) of fasted and sated Evarcha culicivora.

E = Evarcha culicivora. J = juvenile. F = adult female. M = male. Spider body length in mm. N inside each bar. Tests of goodness of fit: chi-square statistic above bar; null hypothesis, 50/50; *** P<0.001, ** P<0.01.

Figure 5. Simultaneous-presentation mount tests of sated Evarcha culicivora females (body length 6.5 mm) from cultures with non-standard feeding regimes (midges only, blood-fed Anopheles only and sugar-fed Anopheles only).

N inside each bar. Tests of goodness of fit: chi-square statistic above bar; null hypothesis, 50/50; *** P<0.001.