The Strategy to Survive Primary Malaria Infection: An Experimental Study on Behavioural Changes in Parasitized Birds

Abstract

Avian malaria parasites (Haemosporida, Plasmodium) are of cosmopolitan distribution, and they have a significant impact on vertebrate host fitness. Experimental studies show that high parasitemia often develops during primary malaria infections. However, field studies only occasionally reveal high parasitemia in free-living birds sampled using the traditional methods of mist-netting or trapping, and light chronic infections predominate. The reason for this discrepancy between field observation and experimental data remains insufficiently understood. Since mist-netting is a passive capture method, two main parameters determine its success in sampling infected birds in wildlife, i. e. the presence of parasitized birds at a study site and their mobility. In other words, the trapping probability depends on the survival rate of birds and their locomotor activity during infection. Here we test (1) the mortality rate of wild birds infected with Plasmodium relictum (the lineage pSGS1), (2) the changes in their behaviour during presence of an aerial predator, and (3) the changes in their locomotor activity at the stage of high primary parasitemia.We show that some behavioural features which might affect a bird's survival during a predator attack (time of reaction, speed of flush flight and take off angle) did not change significantly during primary infection. However, the locomotor activity of infected birds was almost halved compared to control (non-infected) birds during the peak of parasitemia. We report (1) the markedly reduced mobility and (2) the 20% mortality rate caused by P. relictum and conclude that these factors are responsible for the underrepresentation of birds in mist nets and traps during the stage of high primary parasitemia in wildlife. This study indicates that the widespread parasite, P. relictum (pSGS1) influences the behaviour of birds during primary parasitemia. Experimental studies combined with field observations are needed to better understand the mechanisms of pathogenicity of avian malaria parasites and their influence on bird populations.

Fig 1. Behavioural setup.

Behavioural setup with a predator dummy (A, Falco columbarius) speeding down along a fishing line (B). Two video cameras (C1 and C2) film the appearence of the predator dummy behind a shield (D) and the resulting take-off of an attacked experimental bird (E).

Fig 2. Dynamics of parasitemia.

Dynamics of parasitemia of Plasmodium relictum (lineage pSGS1) in different individuals of experimentally infected siskins. Symbols represent different individuals; arrows mark birds dead on 8 and 17 dpi.

Fig 3. Changes in behavioural characteristics.

Changes of time reaction, angle of take-off, and speed of flight in control (non-infected) and Plasmodium relictum (lineage pSGS1) infected birds. Boxes and whiskers represent the upper/lower qartiles ± maximum/minimum values of distribution: grey boxes—first test before experiment, white boxes–second test after exposure. Points indicate outliers, solid horizontal lines show medians.

Fig 4. Changes in locomotor activity.

Locomotor activity as a mean number of jumps per day (±SEM) of experimentally infected with Plasmodium relictum (lineage pSGS1) (solid line) and non-infected (control, dashed line) groups of siskins. Arrow shows the day of exposure. Vertical dash-dot lines set bounds to the most severe stage of parasitemia.