Thermal behaviour of Anopheles stephensi in response to infection with malaria and fungal entomopathogens

Abstract

Background: Temperature is a critical determinant of the development of malaria parasites in mosquitoes, and hence the geographic distribution of malaria risk, but little is known about the thermal preferences of Anopheles. A number of other insects modify their thermal behaviour in response to infection. These alterations can be beneficial for the insect or for the infectious agent. Given current interest in developing fungal biopesticides for control of mosquitoes, Anopheles stephensi were examined to test whether mosquitoes showed thermally-mediated behaviour in response to infection with fungal entomopathogens and the rodent malaria, Plasmodium yoelii.

Methods: Over two experiments, groups of An. stephensi were infected with one of three entomopathogenic fungi, and/or P. yoelii. Infected and uninfected mosquitoes were released on to a thermal gradient (14 - 38 degrees C) for "snapshot" assessments of thermal preference during the first five days post-infection. Mosquito survival was monitored for eight days and, where appropriate, oocyst prevalence and intensity was assessed.

Results and conclusion: Both infected and uninfected An. stephensi showed a non-random distribution on the gradient, indicating some capacity to behaviourally thermoregulate. However, chosen resting temperatures were not altered by any of the infections. There is thus no evidence that thermally-mediated behaviours play a role in determining malaria prevalence or that they will influence the performance of fungal biopesticides against adult Anopheles.

Figure 1

Frequency distribution of fungi infected An. stephensi on a thermal gradient. Percent frequency distribution of the pooled perching temperatures recorded from the thermal gradient for experiment 1. Anopheles stephensi were exposed to one of three fungal isolates or left untreated as a control. Dashed line shows the distribution of available temperatures in the gradient.

Figure 2

Frequency distribution of fungus- and malaria-infected An. stephensi on a thermal gradient. Percent frequency distribution of the pooled perching temperatures recorded from experiment 2. Anopheles stephensi were infected with the rodent malaria P. yoelii, the fungal isolate F52, a combination of the two or left untreated as a control. Dashed line shows the distribution of available temperatures in the gradient.

Figure 3

Mean resting position of An. stephensi following infection with fungal pathogens. Pooled daily mean perching temperature of Anopheles stephensi on a thermal gradient from experiment 1. Mosquitoes were treated with one of three entomopathogenic fungi (Beauveria bassiana isolate IMI391510, Metarhizium anisopliae var anisopliae isolate F52, or M. anisopliae var acridum isolate IMI330189) or left untreated as control

Figure 4

Daily mean perching temperature of Anopheles stephensi infected with P. yoelii. Pooled daily mean perching temperature of Anopheles stephensi on a thermal gradient from experiment 2. Mosquitoes were infected with either the rodent malaria P. yoelii only, the Metarhizium anisopliae var anisopliae isolate F52 only, a combination of the two or left untreated as a control.

Figure 5

Prevalence and mean intensity of P. yoelii infection in An. stephensi. Infection status of dissected An. stephensi on day 8 following blood meal. Dark grey bars indicated the percent of mosquitoes that had oocysts present on the midgut and light grey bars indicate the mean (± SEM) number of oocysts present. "Constant temperature" were those mosquitoes kept in the insectary at 26°C for the duration of the study and "Exposed to gradient" were those mosquitoes that had a daily 30 minute exposure to the gradient before being returned to the constant temperature environment.