The prevalence of avian haemosporidian parasites in an invasive bird is lower in urban than in non‐urban environments

Abstract

Urbanization affects the ecology of wildlife diseases and although it has been suggested that there are lower risks of infection in urban areas, there have been no experiments to support this conclusion. We assessed haemosporidian prevalence and intensity in House Sparrows Passer domesticus using field and experimental data under contrasting conditions (i.e. urban vs. non‐urban). For experimental data, we kept 32 male House Sparrows in captivity as a proxy of stress, and for field data we sampled 49 House Sparrows (17 females). We made use of microscopy to determine the relative intensity and used the polymerase chain reaction to estimate infection prevalence. We obtained total leucocyte counts, leucocyte differentials, heterophil/lymphocyte ratio (H/L) as a measure of stress, and the Polychromatic Index as a measure of physiological condition (erythropoiesis). We identified a total of 10 haemosporidian lineages. For field samples (both males and females), we found a significantly higher prevalence of infection in non‐urban House Sparrows than in urban ones. Under experimental conditions, non‐urban House Sparrows showed a higher prevalence than urban ones both before and after captivity, with a significant increase in parasite intensity. The number of infected birds increased after captivity for both urban (~ 32%) and non‐urban House Sparrows (~ 19%), indicating either a recrudescence of chronic and relapses of latent infections or the appearance of infections that had been acquired earlier. The H/L ratio was significantly higher for non‐urban than for urban male House Sparrows before captivity. No difference in H/L was found for urban House Sparrows before and after captivity, indicating tolerance to city stressors. Our results showed a significant decrease in H/L for non‐urban birds after captivity, suggesting higher stress in the non‐urban agricultural environment. Haemosporidian infections were not associated with the H/L ratio. Our study provides evidence that highly urbanized areas within cities represent lower haemosporidian infection risks than do non‐urban areas for House Sparrows.

Do Invasive Mosquito and Bird Species Alter Avian Malaria Parasite Transmission?

“…Culicoides and louse flies are the main vectors of Haemoproteus of the subgenera Parahaemoproteus and Haemoproteus, respectively, while Leucocytozoon are transmitted by blackflies [6]. Avian haemosporidians have been used as study models to assess the role of parasites on the invasive success of different alien species including house sparrows (Passer domesticus) [7,8] and mynas (Acridotheres tristis) [9]. However, the role of insect vectors to explain the epidemiology of these pathogens affecting invasive avian species has traditionally been neglected.…”

Effects of forest structure on the interaction between avian hosts, dipteran vectors and haemosporidian parasites

“…Host physiological changes due to an infection can potentially change host behavior [ 3 ], fitness, reproductive success, or survival [ 4 ]. Chronic infections produce recurring disease symptoms that may adversely affect hosts throughout their life [ 5 ], regulating host populations and modifying interactions within communities [ 6 ]. Bottom-up and top-down processes are likely in host-parasite systems, specifically when the environment either influences first the parasites (top-down regulation) or the host physical condition (bottom-up regulation) [ 7 ].…”

“…Outcomes of this trade-off can be observed in bilateral asymmetries, such as that of tarsus growth, which reflect early developmental challenges that depend on available resources of the place the young birds inhabit [17]. The life history and habitat preferences of the avian hosts play an essential role in determining the likelihood of an infection [6,18]. Hence, habitat change alters ecosystem processes and species interactions, leading for example to higher infection rates in more intensively used habitats [19,20].…”

Physiological and morphological correlates of blood parasite infection in urban and non-urban house sparrow populations

“…Similarly, other previous studies did not find differences in prevalence between urban and rural habitats [ 38 ], even in the same biological model [ 7 ]. However, other contrasting results prevent us from suggesting a conclusive pattern, especially because previous studies found that avian malaria prevalence can differ between habitats and can be related to the degree of urbanisation [ 35 – 37 , 39 – 42 ]. Changes in climatic conditions (mainly temperature and precipitation) and habitat characteristics can affect both vector-borne parasites and their insect vectors (e.g.…”

“…While some studies found a higher prevalence in urban habitats [ 35 – 37 ], others found no difference [ 38 ] or even a lower prevalence [ 39 – 41 ]. Regarding house sparrows, one study found no difference in prevalence between urban and rural areas [ 7 ], while another study found a higher prevalence in non-urban birds, using both field and experimental data [ 42 ]. Nevertheless, the detrimental effect of malaria on survival and reproduction could be exacerbated in cities because of additional urban environmental constraints.…”