12 Jun 2018
Biodiversity and vector-borne diseases: effects of landscape, mosquito and vertebrate communities on the transmission of West Nile Virus and avian malaria parasites

BRANTA — Martina Ferraguti

Biodiversity and vector-borne diseases: effects of landscape, mosquito and vertebrate communities on the transmission of West Nile Virus and avian malaria parasites

Institution: Universidad Pablo de Olavide

Supervisors: Jordi Figuerola, Josué Martínez de la Puente

Details: PhD, 2017

Martina Ferraguti. Departamento de Ecología de Humedales, Estación Biológica de Doñana (EBD-CSIC), Avda. Américo Vespucio 26, E-41092, Seville, Spain.

Subject Keywords:Vector-borne diseases, Avian malaria parasites, WNV
Species Keywords: House sparrows, Passer domesticus


Emerging vector-borne diseases are an important issue in public health, and both the number and distribution of many have increased in recent decades. Global change has contributed to the increase in emerging infectious diseases due to factors such as habitat alteration, the introduction of alien species and climate change. All of these factors can directly or indirectly affect the transmission ecology of vector-borne pathogens, thereby altering the relationships between pathogens, vectors and host populations. In particular, the anthropogenic alteration of landscapes often leads to an increase in the abundance of just a few animal species and an overall loss of biodiversity, which upsets the composition of both vector and host communities. Thus, habitat characteristics may be a key element affecting the transmission dynamics of mosquito-borne pathogens.

Here, I use a multidisciplinary approach to identify the factors affecting the transmission of two mosquito-borne pathogens – avian malaria parasites (mainly avian Plasmodium) and West Nile virus (WNV) – that circulate naturally in birds in southern Spain. In particular, this thesis explores how the vector (mosquitoes) and vertebrate (birds and mammals) communities and the environment affect pathogen prevalence, richness and/or diversity in wild bird populations living in 15 natural, 15 rural and 15 urban areas. Extensive monitoring of the natural populations of insects and birds was combined with molecular and serological analyses and remote sensing in order to gain better knowledge of pathogen dynamics. Using house sparrows Passer domesticus as the main host study model, the foremost aim was to assess how landscape and biodiversity affect the transmission of two mosquito-borne pathogens infecting wild birds. In the seven chapters, (1) the interaction between potential insect vectors and pathogens, (2) the interactions between vertebrate hosts and pathogens and (3) how biodiversity affects the transmission of vector-borne pathogens under natural conditions, were explored.

To identify the factors affecting the interactions between potential insect vectors and bird pathogens, I first identified the impact that urbanization and landscape characteristics (e.g. land use, distance to water sources and a vegetation index) have on mosquito communities in southern Spain. Human activities were largely responsible for determining the composition of mosquito communities in the area and may increase the likelihood of humans coming into contact with the pathogens that mosquitoes transmit. In addition, avian malaria parasites were found to be harboured by different species of mosquitoes, revealing general associations between insect species and parasite lineages, thereby providing evidence for the low transmission specificity of avian Plasmodium parasites. The results of this study highlight how mosquito feeding patterns influence parasite transmission, and ornithophilic mosquito species (feeding mainly on birds) were found to have greater parasite prevalence than those that feed mainly on mammals. In addition, parasite prevalence in mosquitoes varied seasonally, with the highest prevalence recorded in autumn. The diversity of blood parasites in Culicoides circumscriptus was investigated to identify potential nodes of the wild parasite-vector-host transmission network. Overall, these studies allowed me to identify the potential insect vectors of avian pathogens and the biotic and environmental factors that potentially affect their prevalence.

By analysing the prevalence of antibodies in resident birds, I also confirmed the local circulation of WNV in 2013, which underlines the usefulness of active surveillance programs in wild birds in areas with no disease-associated mortalities. The influence of vectors and vertebrate communities and environmental characteristics on the prevalence, richness and diversity of the avian malaria parasites infecting house sparrows was investigated in the 45 localities. Factors linked to the host community were the most relevant for explaining variations in Plasmodium lineage richness and diversity, while the vector community was most important for determining the prevalence of parasites in birds.

Finally, the relationship between pathogens and vector community abundance and composition was tested. Mosquito community composition was identified as a key factor that was related to the seroprevalence of WNV in these sparrow populations. The abundance of the ornithophilic mosquito Culex perexiguus was positively related to WNV seroprevalence. In addition, seropositive birds were only found in natural and rural habitats, which may explain why historically the incidence of WNV in humans in southern Spain – despite local circulation of this virus in wild birds – is currently low. Finally, with the information collected in this thesis, I tested the hypothesis that biodiversity ‘dilutes’ pathogen transmission. The dilution effect hypothesis proposes that greater biodiversity reduces the possibility of transmission of pathogens to humans and/or other species. This hypothesis was tested for the seroprevalence of WNV and the prevalence of Plasmodium, Haemoproteus and Leucocytozoon parasites in birds. Overall, no negative relationship between variables related to biodiversity (diversity index or species richness) and pathogen prevalence was found, which contradicts the predictions of the dilution effect hypothesis.

This thesis identifies key variables affecting the transmission dynamics of avian vector-borne pathogens based on the description of the factors that mark the vector community and its interaction with different groups of pathogens. It also includes the study of the biotic and abiotic factors that determine the infection of wild birds and, finally, analyses how biodiversity determines the prevalence of vector-borne pathogens in wild birds. These results allowed me to identify the complex transmission networks of vector-borne pathogens, including those that potentially spread emerging zoonotic diseases and could have an impact on human and animal health.

Published Papers

Ferraguti M., Martínez-de la Puente J., Roiz D., Ruiz S., Soriguer R., Figuerola J. (2016) Effects of landscape anthropization on mosquito community composition and abundance. Scientific Reports, 6: 29002.

Ferraguti M., Martínez-de la Puente J., Muñoz J., Roiz D., Ruiz S., Soriguer R., Figuerola J. (2013) Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PloS one, 8: e66237.

Ferraguti M., Martínez-de la Puente J., Ruiz S., Soriguer R., Figuerola J. (2013) On the study of the transmission networks of blood parasites from SW Spain: diversity of avian haemosporidians in the biting midge Culicoides circumscriptus and wild birds. Parasites & Vectors, 6: 208.

Ferraguti M., Martínez-de la Puente J., Soriguer R., Llorente F., Jiménez-Clavero M.Á., Figuerola J. (2016) West Nile virus-neutralizing antibodies in wild birds from southern Spain. Epidemiology and Infection, 144: 1907 – 1911.

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