The role of uropygial secretion and birds body odour on their interaction with mosquitoes and parasites

Resumen

Chemical signals are implied in vital proceses such as food acquisition, reproduction, predation avoidance and interspecific interactions. In blood sucking insects such as mosquitoes, chemical signals play a key role by allowing the detection of their vertebrate hosts. Besides interspecific differences, vertebrate host characteristics such as age, sex, size and infection by blood parasites, may affect the chemical signals emitted by hosts, which may in turn affect vector-host interactions and ultimately, the transmission dynamics of vector-borne diseases. Mosquitoes transmit parasites and other pathogens causing important diseases that affect humans, wildlife, and domestic animals. This is the case of malaria parasites, which may largely affect host population dynamics. However, the mechanisms affecting the interactions between mosquitoes, parasites, and vertebrate hosts are not fully understood, especially in the case of wild nonmodel species. The aim of this thesis is to assess the role of different bird chemical cues (uropygial gland secretions and body odour) in mosquito attraction and the effect of host infection by avian malaria parasites on these interactions. To deal with this important question, I used a multidisciplinary approach that combines techniques from different research areas (e.g. molecular parasitology, entomology, and ornithology), and data from field and laboratory experiments under controlled conditions. As study system, I used i) two wild passerines as vertebrate hosts, the common blackbird (Turdus merula) and the house sparrow (Passer domesticus), ii) two species of mosquitoes, namely the common house mosquito (Culex pipiens) and the marshland mosquito (Aedes caspius), and iii) avian haemospodians, including mosquito-borne parasites of the genus Plasmodium. In order to better understand the dynamics of host-vector-pathogen interactions, I tested the host manipulation hypothesis, which argues that parasites may modify certain characteristics of their hosts to increase their transmission success. Thus, malaria infected birds would be more attractive to mosquitoes than uninfected ones, thereby enhancing the contact rates between parasites and insect vectors. However, the mechanisms underlying this differential attraction are still unknown. I studied the potential effect of parasite infections on the odours emitted by birds and how this may in turn affect the interactions with mosquitoes. Secretions of the uropygial gland are considered as one of the main sources of bird odour, so the effects of parasites on bird-vector interactions could be driven by their effects on the composition of these secretions. I performed different studies to determine the potential factors affecting the composition of birds’ uropygial secretions, including parasite infections, and subsequently, I tested the role of secretions and body odour in mosquito attraction. The overall composition of uropygial secretions of wild birds differed between sexes and age classes, while this was not the case for the infection by avian haemosporidian parasites neither the habitat type (forest vs urban areas). Further analyses revealed the presence of the pollutant DDE in uropygial secretions. DDE is mainly derived from the DDT used decades ago. The relative proportion of DDE was higher in older and forest-dwelling birds, and increased with bird´s body mass. Overall these results support the role of both intrinsic and extrinsic factors in between-individuals variation in the composition of uropygial gland secretions. However, these results do not provide support for the potential effect of parasite infections on the composition of bird uropygial secretions.On the basis of the importance of the uropygial gland secretion as a source of bird odour, I evaluated the role of this secretion in the attraction of two species of mosquitoes with differential feeding patterns, namely the ornithophilic Cx. pipiens and the mammophilic Ae. capius. Both species of mosquitoes were similarly attracted to this stimulus (uropygial gland secretions + CO2) than to the control (only CO2) in a dual choice olfactometer, suggesting that the attraction of mosquitoes to avian hosts is not mediated by this chemical cue. Subsequently, I tested the role of Plasmodium infection in the attraction of Cx. pipiens mosquitoes towards both uropygial secretions and bird´s body odours (headspace). Culex pipiens were more attracted towards the headspace of Plasmodium infected than uninfected birds, while no differences were found in the attraction of mosquitoes when the stimulus tested was the uropygial gland secretion. These results suggest that Plasmodium parasite modify bird body odour increasing the attraction of mosquitoes and therefore, increasing its capacity of transmission to new vertebrate hosts. However, these effects are not driven by changes in the volatile fraction of the uropygial gland secretion. In sum, this thesis provides novel evidence into the complex mechanisms that drive the interactions between parasites, vectors, and vertebrates, and highlights the role of chemical cues such as the odour of birds in the attraction of mosquitoes to individuals infected by haemosporidians. These results may have important implications for the epidemiology of Plasmodium parasites in natural environments and open new questions for future studies on the identification of key components of bird´s odours determining mosquito attraction.