Blood parasites in vectors reveal a united blackfly community in the upper canopy

Abstract

Background: The behaviour of blood-sucking arthropods is a crucial determinant of blood protozoan distribution and hence of host-parasite coevolution, but it is very challenging to study in the wild. The molecular identification of parasite lineages in vectors can be a useful key to understand the behaviour and transmission patterns realised by these vectors. Methods: In this study, we collected blackflies around nests of three raptor species in the upper forest canopy in central Europe and examined the presence of vertebrate DNA and haemosporidian parasites in them. We molecularly analysed 156 blackfly individuals, their vertebrate blood meals, and the haemosporidian parasite lineages they carried. Results: We identified nine species of Simulium blackflies, largely belonging to the subgenera Nevermannia and Eusimulium. Only 1% of the collected specimens was visibly engorged, and only 4% contained remains of host DNA. However, in 29% of the blackflies Leucocytozoon lineages were identified, which is evidence of a previous blood meal on an avian host. Based on the known vertebrate hosts of the recorded Leucocytozoon lineages, we can infer that large and/or abundant birds, such as thrushes, crows, pigeons, birds of prey, owls and tits are the main targets of ornithophilic blackflies in the canopy. Blackfly species contained similar proportions of host group-specific parasite lineages and thus do not appear to be associated with particular host groups. Conclusions: The Leucocytozoon clade infecting thrushes, crows, and pigeons present in most represented blackfly species suggests a lack of association between hosts and blackflies, which can increase the probability of host switches of blood parasites. However, the composition of the simuliid species differed between nests of common buzzards, goshawks and red kites. This segregation can be explained by coinciding habitat preferences between host and vector, and may lead to the fast speciation of Leucocytozoon parasites. Thus, subtle ecological preferences and lack of host preference of vectors in the canopy may enable both parasite diversification and host switches, and enforce a habitat-dependent evolution of avian malaria parasites and related haemosporidia.

Blood Parasites in Sympatric Vultures: Role of Nesting Habits and Effects on Body Condition

“…Our current results do not confirm if the adaptations connected with carrion-feeding lifestyle and gut microbiome suppress transmission, or otherwise affect the blood parasite fauna. In conjunction with the patterns found in previous studies on raptor and non-raptor scavengers, it appears probable that habitat features play an important role in the transmission of blood parasites [26,62]. An additional role in the specific features of the host immunity needs to be further explored.…”

“…However, vectors mostly seek hosts close to their emergence and oviposition sites, which for blackflies are flowing water bodies [ 44 , 45 ]. Additionally, some vector species appear to have quite specific habitat and less specific host preferences, e.g., using cavities or keeping close to shade and intact foliage, and even preferring specific heights in the trees [ 26 , 46 ]. At the same time, flying in hot and open areas may strongly increase the danger of desiccation without compensating with secure encounters with hosts.…”

“…These social and nesting habits, as well as the general environmental conditions of the breeding areas, have been highlighted as influencing factors on the occurrence of blood parasites in vultures and other species [ 17 , 18 , 23 , 24 ]. Therefore, spatial and temporal variations in prevalence due to inter-annually changing climatic conditions and nest habitats, and their effects on vectors can be expected [ 25 , 26 ]. The nesting habitat can influence the body condition of hosts through the direct impact of harsh environmental conditions in montane vs. lowland areas, and due to expenditure for food resource exploitation, and their effects on nestling condition, thereby indirectly affecting their parasite loads [ 27 , 28 ].…”

Prevalence and genetic diversity of avian haemosporidian parasites in wild bird species of the order Columbiformes

“…Hence, it is likely that feral pigeons could have acted as a reservoir and blackflies transmitted the lineages from feral pigeons to woodpigeons and vice versa. While Scaglione et al ( 2015 ) states that Leucocytozoon parasites are not routinely found in pigeons, a study sampling blackflies in Central Europe showed pigeons to be one of the main targets of ornithophilic blackflies (Chakarov et al 2020 ). High rates of Leucocytozoon in the sampled woodpigeons may have been favoured by the opportunities for transmission that the woodpigeons offered (e.g.…”

“…However, only few studies have presented data on the prevalence and diversity of haemosporidian parasites in closely related bird species. Differences in prevalence between species are associated with several factors and the interactions between those, including life-history traits and ecology of the hosts and vectors, parasite characteristics and environmental conditions, that may affect the activity of vectors and the development of parasites (Sol et al 2000 ; Gupta et al 2011 ; Quillfeldt et al 2011 ; Hellard et al 2016 ; Chakarov et al 2020 ; Ciloglu et al 2020b ; Ellis et al 2020 ). Also different behavioural characteristics (e.g.…”