Disease Ecology in a modified world: Linking combined environmental stressors, population dynamics and movement ecology to understand the circulation of infectious agents – EcoDIS

EcoDis combines a field-based approach with laboratory analysis to address the project's central objective via three steps: 1) Mapping the spatial variability of gull exposure to pollutants and parasites/pathogens arpund the western Mediterranean. This involves sampling birds (adult and juvenile) in representative colonies across the region and analysing these samples using eco-toxicological, molecular and chemical methods to assess exposure to pollutants and parasites/pathogens. 2) To assess the cumulative effects of these stressors on gull demography (reproductive success, survival and return rates) through the monitoring of five focal colonies and from information obtained from bio-logging of individual birds. These observations will be complemented by toxicological tests in the laboratory to examine the interaction between different types of stresses (e.g.,effect of heavy metals on nest parasites). 3) Based on the monitoring data, genetic analyses and experimental results, link gull movements at different spatial scales, and between urban/non-urban areas, with the distribution of infectious agents and the potential risk for humans. The integration of these data with information on gull diets will allow an assessment of the extent to which the health status and reproductive success of the birds are related to anthropogenic resource use.

During our screen of parasites and pathogens, a new blood parasite from the Babesia Peircei group was discovered in gulls. It shows an extremely high prevalence in a French colony, particularly among young birds, but appears to be largely absent in other colonies, despite the presence of the tick vector. This calls into question the connectivity between colonies and the possible role of environmental factors in the establishment of the parasite within colonies. We found that this parasite can have a significant impact on the fitness of the birds and may thus represent an important stress factor for these populations. The additional presence of other types of infectious agents in these birds is currently being investigated.

Furthermore, analyses of historical banding data demonstrate that gull populations move differently depending on the colony’s location and their age. Based on these behaviors, we can predict the direction of pathogen circulation. Contemporary data from the project will allow us to test whether movement patterns have changed over the past decade, particularly with the closure of public landfills used by these birds for feeding.

Finally, among the various pollutants studied, a study on plastics found in bird regurgitations suggests that parents adapt their diet in response to the presence of chicks. Indeed, the number of plastic particles in regurgitated pellets decreases around the time of chick hatching, a period when young birds can be especially sensitive to poor-quality food. Consequently, although gulls frequently feed on anthropogenic food sources, they seem capable of adjusting their foraging to ensure the survival of their young. More generally, the use of food resources containing plastics varies greatly between colonies within the western Mediterranean.

By linking information on environmental stressors to gull demography and observed movements, we can better understand the role of bird health and reproductive success in their movements. Interestingly, such movements will subsequently have a feedback effect, altering both the presence of contaminants and pathogens at different spatial scales and the potential risks to human and animal health. These results will be useful from a fundamental point of view to better understand the ecology of an anthropophilic bird, but will also provide essential information to wildlife managers and public health officials.

To date, the results of the project have resulted in 1 paper published in an international journal (Ticks & Tick-borne Diseases), with two other manuscripts in the submission process. We have also presented elements of the project at 3 international and 4 national conferences. In terms of outreach activities, the project was presented in 1 article for wildlife managers (https://pole-lagunes.org/etudier-limpact-des-polluants-sur-les-goelands-leurs-mouvements-et-leurs-parasites-lancement-du-projet-ecodis/) and in the CNRS blog on oceans (https://lejournal.cnrs.fr/nos-blogs/un-ocean-de-decouvertes/la-surveillance-des-oiseaux-marins-de-nouveaux-enjeux-sanitaires). We also presented part of the project to the general public via the conference ARBE - Provence Alpes-Côte d'Azur «Fighting plastic pollution in natural environments« (https://youtu.be/EB-SzAgcoxQ)

Environmental pollutants and pathogens are known to negatively impact wildlife health and alter population dynamics. While these effects are often sub-lethal or weak individually, we have little information about their cumulative and interactive effects when experienced together. EcoDIS will address this issue via an interdisciplinary approach that combines demographic monitoring, ecotoxicology, population genetics, epidemiology, and movement ecology. We will examine these facets in a common and abundant Mediterranean species, the Yellow-legged gull (Larus michahellis), a colonial breeding seabird that lives in close proximity to humans.

The project includes three principal objectives and five scientific workpackages (WP). The first objective is to map spatial variability in gull exposure to pollutants and parasite/pathogens across the western Mediterranean Sea (WP1). This will involve assessing pollutant levels (metallic trace elements, macroplastics, microplastics and plastic additives), and exposure to parasites and pathogens (ectoparasites, helminths, bacteria and viruses) in birds from a series of 15 colony locations. Given previous results, we expect these factors to vary strongly at this spatial scale. The second objective is to evaluate the combined effects of these potential stressors on gull demographics (reproductive success, survival and return rates) via monitoring in select focal colonies (WP2). We expect that stressors will have cumulative effects in some cases, but may be interactive in others. Indeed, a particularly novel aspect to be experimentally tested in the project is the potential for parasites and contaminants to interact antagonistically (WP3). If parasites act as pollution sinks, absorbing pollutants faster than their hosts, they may confer a benefit to hosts in highly polluted locations. In contrast, if a contaminant lowers parasite fitness, hosts may prefer to use contaminated sites to escape deleterious parasites. Finally, the last project objective will be to link observational and experimental data to gull movements among colonies and between urban / non-urban areas to examine disease circulation and human risk. Movement will be inferred via direct studies on the gulls - population genetic analyses, CMR modelling of ringing data, and biologging (WP4). It will also be determined indirectly by examining structure in three types of common parasites - a tick nest ectoparasite (Ornithodoros maritimus), a tick-borne blood parasite (Babesia sp.), and a directly transmitted microbe such as avian influenza virus (WP5). We will then assess if combined stressors alter movement and if movement can, in turn, explain the structure of infectious agents at different spatial scales. In addition, the integration of this data with information on feeding regimes (from regurgitates and stable isotope analyses) will enable us to evaluate the degree to which health status and reproductive success are linked to the use of anthropogenic resources.

A consortium of seven national and international partners with complementary skills and strong experience in marine systems will ensure project success. By using a widespread wildlife species frequently found in urban areas, the results of the EcoDIS project will be of both significant fundamental (i.e., effects of combined environmental stressors on wildlife population dynamics) and applied interest (i.e., pathogen circulation by wildlife and human exposure risk). Results may also enable us to use common species like YLGs, or their even their parasites, as indicator species of environmental quality. Finally, technical advances in quantifying microplastics in animal tissues are expected and will represent a major contribution toward characterizing the impact of this important environmental pollutant on animal populations.