Parasites in space and time: a case study of haemosporidian spatiotemporal prevalence in urban birds.

Prevalence responses to anthropic factors differ across hosts and parasite species. We here analyzed the spatiotemporal variation of avian haemosporidian prevalence in bird assemblages of the Mooswald forest (i.e., urban greenspace; Freiburg, Germany), in response to local environmental features (e.g., water sources, human presence (visited)/absence (unvisited)) and bird-level traits (e.g., body condition, age, sex) in 2 years. We used a nested PCR protocol (mitochondrial (mt)DNA cytochrome b (cyt b) gene) and microscopy to determine haemosporidian infections. Prevalence was analyzed using a general linear multi-model (glmulti) approach with Akaike information criterion corrected for small samples (AICc), with subsequent model inferences using a GLMM on the best selected model, considering bird species as a random factor. Analyses were conducted for the main understory bird species (Blackcap - Sylvia atricapilla, Chaffinch - Coereba flaveola, Great Tit - Parus major, Blue Tit - Cyanistes caeruleus, European Robin - Erithacus rubecula, Blackbird - Turdus merula, Song Thrush - Turdus philomelos). We further conducted spatial autocorrelation analyses for all haemosporidian infections, and classification and regression trees (CARTs) for focal species. We analyzed a total of 544 samples of seven bird species. In 2011 prevalence for Haemoproteus/Plasmodium was 25.8% and 11.7% for Leucocytozoon. In 2013 prevalence for Haemoproteus/Plasmodium was 26.5% and 35.5% for Leucocytozoon. Haemosporidian prevalence was significantly different between some focal species. There was a negative association between distance to the nearest water source and prevalence in the year 2011, and the opposite pattern for the year 2013. However, when analyzed for the six focal species separately, such a relationship could change from a negative to a positive one, or there could be no relationship at all. For Leucocytozoon there was higher prevalence in the section of the forest visited by humans. We did not find spatial autocorrelation for prevalence across the study site, but there were statistically significant local spatial clusters in the visited section. Although there were similar responses of prevalence to some factors, infection patterns were generally bird species-specific. Thus, prevalence is a labile epidemiological parameter, varying spatiotemporally in an idiosyncratic way.

Forests of opportunities and mischief: disentangling the interactions between forests, parasites and immune responses.

Habitat characteristics determine the presence of individuals through resource availability, but at the same time, such features also influence the occurrence of parasites. We analyzed how birds respond to changes in interior forest structures, to forest management regimes, and to the risk of haemosporidian infections. We captured and took blood samples from blackcaps (Sylvia atricapilla) and chaffinches (Fringilla coelebs) in three different forest types (beech, mixed deciduous, spruce). We measured birds' body asymmetries, detected avian haemosporidians, and counted white blood cells as an immune measure of each individual per forest type. We used, to our knowledge for the first time, continuous forest structural parameters to quantify habitat structure, and found significant effects of habitat structure on parasite prevalence that previously have been undetected. We found three times higher prevalence for blackcaps compared with chaffinches. Parasite intensity varied significantly within host species depending on forest type, being lowest in beech forests for both host species. Structurally complex habitats with a high degree of entropy had a positive effect on the likelihood of acquiring an infection, but the effect on prevalence was negative for forest sections with a south facing aspect. For blackcaps, forest gaps also had a positive effect on prevalence, but canopy height had a negative one. Our results suggest that forest types and variations in forest structure influence the likelihood of acquiring an infection, which subsequently has an influence on host health status and body condition; however, responses to some environmental factors are host-specific.

Associations of forest type, parasitism and body condition of two European passerines, Fringilla coelebs and Sylvia atricapilla.

Human-induced forest modification can alter parasite-host interactions and might change the persistence of host populations. We captured individuals of two widespread European passerines (Fringilla coelebs and Sylvia atricapilla) in southwestern Germany to disentangle the associations of forest types and parasitism by haemosporidian parasites on the body condition of birds. We compared parasite prevalence and parasite intensity, fluctuating asymmetries, leukocyte numbers, and the heterophil to lymphocyte ratio (H/L-ratio) among individuals from beech, mixed-deciduous and spruce forest stands. Based on the biology of bird species, we expected to find fewer infected individuals in beech or mixed-deciduous than in spruce forest stands. We found the highest parasite prevalence and intensity in beech forests for F. coelebs. Although, we found the highest prevalence in spruce forests for S. atricapilla, the highest intensity was detected in beech forests, partially supporting our hypothesis. Other body condition or health status metrics, such as the heterophil to lymphocyte ratio (H/L-ratio), revealed only slight differences between bird populations inhabiting the three different forest types, with the highest values in spruce for F. coelebs and in mixed-deciduous forests for S. atricapilla. A comparison of parasitized versus non-parasitized individuals suggests that parasite infection increased the immune response of a bird, which was detectable as high H/L-ratio. Higher infections with blood parasites for S. atricapilla in spruce forest indicate that this forest type might be a less suitable habitat than beech and mixed-deciduous forests, whereas beech forests seem to be a suboptimal habitat regarding parasitism for F. coelebs.