Host immune responses to experimental infection of Plasmodium relictum (lineage SGS1) in domestic canaries (Serinus canaria)

Abstract

Understanding the complexity of host immune responses to parasite infection requires controlled experiments that can inform observational field studies. Birds and their malaria parasites provide a useful model for understanding host-parasite relationships, but this model lacks a well-described experimental context for how hosts respond immunologically to infection. Here, ten canaries (Serinus canaria) were infected with the avian malaria parasite Plasmodium relictum (lineage SGS1) in a controlled laboratory setting with ten uninfected (control) birds. A suite of immunological blood parameters, including the concentration of four white blood cell types, the concentration of the acute phase protein haptoglobin, and the bacteria-killing ability of blood plasma, were repeatedly measured over a 25-day period covering the acute phase of a primary infection by P. relictum. Three infected and one control bird died during the course of the experiment. A multivariate statistical analysis of the immune indices revealed significant differences between infected and uninfected individuals between 5 and 14 days postinfection (dpi). Group differences corresponded to reduced concentrations of lymphocytes (5 dpi), heterophils (8 dpi), and monocytes (11 and 14 dpi), and an increase in haptoglobin (14 dpi), in infected birds relative to uninfected controls, and no change in bacteria-killing. Upon re-running the analysis with only the surviving birds, immunological differences between infected and control birds shifted to between 11 and 18 dpi. However, there were no clear correlates relating immune parameters to the likelihood of surviving the infection. The results presented here demonstrate the dynamic and complex nature of avian immune function during the acute phase of malaria infection and provide a context for studies investigating immune function in wild birds.

An experimental test of the physiological consequences of avian malaria infection

“…Acute infections can cause mortality, particularly in species that have been recently introduced to the parasites (Atkinson, Woods, Dusek, Sileo, & Iko, ). During the acute phase, birds can reduce activity levels and food intake, lose body mass and experience severe declines in both haematocrit and haemoglobin (Atkinson et al., ; Ellis et al., ; Krams et al., ; Mukhin, Palinauskas, Platonova, & Kobylkov, ; Palinauskas, Valkiūnas, Bolshakov, & Bensch, ). Observational field studies, which primarily focus on chronic infection, have found positive (e.g.…”

Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria

“…Controlled experimental studies with P. relictum are relatively easy to design due to availability of laboratory-friendly experimental vertebrate hosts (canaries and some species of other common birds), laboratory-colonized susceptible mosquitoes (species of the Culex pipiens complex) and worldwide high prevalence in many wild bird species (donors of natural infections). This makes P. relictum a convenient and even unique model organism to approach numerous questions about mechanisms of host-parasite interactions, including the immunological aspects during malaria infections [ 56 – 58 ], the ecology and evolution of host-parasite associations [ 25 , 59 – 63 ], the host adaptations to tolerate malaria infections [ 10 , 31 , 47 , 64 , 65 ], patterns of mosquito transmission [ 32 , 46 , 53 , 66 – 68 ] and many other questions.…”

Overlap in the Seasonal Infection Patterns of Avian Malaria Parasites and West Nile Virus in Vectors and Hosts

“…8 Indeed, parasites with similar infection dynamics in Culex vectors (CHI02PL, CHI04PL, and CHI07PL) were apparently specialized American robins 43,44 and had MIRs that generally peaked in late July or early August. In addition, juvenile robins accumulated infections of these parasites contemporaneously, with the most rapid increase in infections occurring in July and August (weeks [25][26][27][28][29][30][31][32][33][34][35].…”

“…26 If the host survives the acute infection, parasitemia in the blood often declines to lower levels. Low parasitemia in the blood generally persists through this chronic stage of infection, 27 and parasites may disappear from the blood stream, lying dormant in tissues. Relapses and recrudescence of low-level or dormant malaria infection may occur, especially during periods of host stress.…”