Multihost/Multivector Community Network: Disentangling Sandfly Species and Host Interactions in Avian Habitats

Abstract

Ascertaining the feeding behavior of vectors is a key for understanding epidemiology of the infections they transmit. For some host-vector-parasite systems, this information is biased towards human and peridomestic habitats, frequently underestimating the likely role of wildlife. In addition, studies on vector interactions often focus on a one-to-one host-vector relationship, even though it is crucial to analyze how multiple vector species interact with multiple hosts. These biases particularly affect our knowledge of sandflies, the main vector of Leishmania spp. and various phleboviruses, that are rarely explored in non-peridomestic habitats and in the context of multiple interactions with various hosts. To reveal the multihost/multivector network involving phlebotomine sandflies in a semiarid and poorly populated area of Spain, we sampled the sandfly community close to avian nests by means of two trapping methods (Centers for Disease Control (CDC) and sticky traps) during 3 years and identified the blood-meal source of all engorged sandflies. We detected six phlebotomine species with Phlebotomus perniciosus, P. papatasi, and Sergentomyia minuta being the most abundant ones. We identified 13 blood source species, with humans being the most common one, followed by Coracias garrulus (European roller) and Sus scrofa (likely wild boar). Five of the six sandfly species fed largely on wild mammals, although, three also fed on wild birds. Phlebotomus sergenti only fed on birds based on this analysis. Phlebotomus papatasi and P. sergenti were common visitors of bird nests suggesting an endophagic behavior. A network analysis showed a highly-connected and poorly-specialized network wherein sandflies shared most of the blood source and showed an opportunistic feeding behavior with marked anthropophilia. Our results obtained close to avian nests show that sandfly populations are maintained by various wild animals, which will greatly complicate the management and control of the pathogens they transmit to humans and domestic animals.

Keywords: anthropophilia; arid areas; blood meal; endophagy; phlebotomine; vector-borne.

Figure 1

Study area: Almería province in Spain (A); studied municipalities in Almería province (B); localities where sandflies were collected during the study period, including CDC and sticky traps (C); localities where sandflies were sampled in 2018 using CDC traps (D). In the graphs, some nearby localities overlap. CDC, Centers for Disease Control.

Figure 2

Habitat types sampled with CDC and sticky traps: bridges over ramblas (A); sandstone cliffs (B); isolated group of trees (C). CDC, Centers for Disease Control.

Figure 3

Network of hosts and sandflies from identified blood meals of individuals captured in 2018 by CDC traps. (A) Quantitative bipartite interaction network between the vertebrate hosts and the phlebotomine parasites. (B) The adjacency matrix of blood meals network, organized into three modules. Colored cells represent the gradient of interactions: from white (lower number of interactions) to deep blue (higher number of interactions). (C) Unipartited network, which links mean shared sandfly species (green dots) among host species (yellow dots). CDC, Centers for Disease Control.