Periodic Reporting for period 1 - SENTIMOUV (Spatial and demographic dynamics of disease transfer at the wildlife-human interface)
Période du rapport: 2020-01-01 au 2021-12-31
Infectious diseases are a significant threat to public health, livestock production, and biodiversity conservation. Increasing human population densities, land use change, biodiversity loss, and climate change have accelerated the emergence and spread of new and existing diseases. Free-ranging wildlife populations, particuarly cosmopolitan wildlife species living in human-dominated habitats, act as reservoirs for the spread of disease and are key for predicting current and future disease dynamics. At the same time, wildlife populations in urban areas are often the targets of management actions due to perceived threats to human health, safety, and livelihoods. Since management can alter individual movements, energetic expenditure, and behavior, with effects on wildlife-pathogen interactions, a comprehensive understanding of wildlife-pathogen systems is key to selecting appropriate management actions.
Due to their global distribution and wide-ranging movements, seabirds are important vectors for the spread of pathogens across continents and oceans. Generalist coastal seabirds, which exploit anthropogenic food sources, are particularly likely to interact with zoonotic pathogens, making them useful for monitoring disease prevalence. However, many factors mediating interactions between seabirds and pathogens remain unknown or poorly understood. The effects and duration of early-life exposure may play a key role in later disease states, but the dynamics of developmental exposure are complex. Subsequently, large-scale movement patterns, including migration, dispersal, and foraging, mediate exposure to infectious agents and may vary widely between individuals. Improved understanding of disease exposure across life stages and heterogeneous environments is required to understand disease dynamics in wide-ranging seabirds.
Our study combined field study, laboratory analysis, and modeling to explore prevalence and transmission of zoonotic pathogens by brown skuas (Stercorarius antarcticus) and yellow-legged gulls (Larus michahellis), two scavenging and predatory seabirds that forage in marine and terrestrial environments and nest among other marine birds, making them key reservoirs for diease transmission and spread to avian and human populations. These complementary studies allowed us to describe exposure pathways and probabilities across individuals and life stages, evaluate spatial dynamics of adults, assess potential effects of management on local disease circulation, and develop guidelines for management and monitoring.
Due to their global distribution and wide-ranging movements, seabirds are important vectors for the spread of pathogens across continents and oceans. Generalist coastal seabirds, which exploit anthropogenic food sources, are particularly likely to interact with zoonotic pathogens, making them useful for monitoring disease prevalence. However, many factors mediating interactions between seabirds and pathogens remain unknown or poorly understood. The effects and duration of early-life exposure may play a key role in later disease states, but the dynamics of developmental exposure are complex. Subsequently, large-scale movement patterns, including migration, dispersal, and foraging, mediate exposure to infectious agents and may vary widely between individuals. Improved understanding of disease exposure across life stages and heterogeneous environments is required to understand disease dynamics in wide-ranging seabirds.
Our study combined field study, laboratory analysis, and modeling to explore prevalence and transmission of zoonotic pathogens by brown skuas (Stercorarius antarcticus) and yellow-legged gulls (Larus michahellis), two scavenging and predatory seabirds that forage in marine and terrestrial environments and nest among other marine birds, making them key reservoirs for diease transmission and spread to avian and human populations. These complementary studies allowed us to describe exposure pathways and probabilities across individuals and life stages, evaluate spatial dynamics of adults, assess potential effects of management on local disease circulation, and develop guidelines for management and monitoring.
The onset of the COVID-19 epidemic in 2020 forced the cancellation of the first year of fieldwork on yellow-legged gulls. Instead, we synthesized and published a related dataset on epidemiology and movements of brown skuas in the southern Indian Ocean (Amsterdam Island). This work, currently in revision with the journal Functional Ecology, showed that non-breeding skuas move greater distances than breeders, making them important vectors for the spread of avian cholera. Both breeders and non-breeders were exposed to avian cholera at similar rates; however, as non-breeders ranged more widely and were more active, they interacted more with breeding seabirds and marine mammals of conservation concern. ("Skuas Infographic")
During the second year of the project, we collected data on the archipelago of Frioul, Marseille, France. For Part 1 of our study, we deployed 30 lGPS loggers (UvA-BITS, Amsterdam, Netherlands) on breeding adult yellow-legged gulls to explore their year-round movements ("Movement Infographic"). In order to explore the effect of a common management practice on the movement of individuals, we induced reproductive failure for 15 of the captured gulls, while the other 15 completed breeding normally. The two groups used similar habitats; however, the non-oiled group departed the colony earlier than the oiled group, suggesting that nest control increases the time that individuals remain near the colony site. In Part 2, we experimentally swapped one of two eggs per nest at 40 pairs of nests. We then collected blood samples from nestlings every five days through ~40 days of age, and tested the samples for antibodies against avian influenza virus (AIV), infectious bronchitis virus (IBV), and Toxoplasma gondii (toxoplasmosis). We found that AIV circulates widely and is present at high levels in nestlings, while toxoplasmosis is infrequent and IBV absent. Antibody levels depended on maternal transfer through early development and declined through Day 15 for toxoplasmosis and Day 25 for AIV. At this point, foster siblings became more similar than biological siblings, and antibody levels began to rise in response to external exposure. However, after the initial period of antibody decline, differences between foster and biological siblings were non-significant, suggesting that exposure to external sources does not vary substantially among nests ("Antibody Infographic"). Results are currently in preparation for submission to Journal of Experimental Biology (Part 1) and Proceedings of the Royal Society B (Part 2).
Although in-person dissemination was limited due to COVID-19, we partnered with a local high school in Marseille (lycée Jean Perrin) to present information on theory, implementation, and applications of mark-recapture studies in the classroom and in the field.
During the second year of the project, we collected data on the archipelago of Frioul, Marseille, France. For Part 1 of our study, we deployed 30 lGPS loggers (UvA-BITS, Amsterdam, Netherlands) on breeding adult yellow-legged gulls to explore their year-round movements ("Movement Infographic"). In order to explore the effect of a common management practice on the movement of individuals, we induced reproductive failure for 15 of the captured gulls, while the other 15 completed breeding normally. The two groups used similar habitats; however, the non-oiled group departed the colony earlier than the oiled group, suggesting that nest control increases the time that individuals remain near the colony site. In Part 2, we experimentally swapped one of two eggs per nest at 40 pairs of nests. We then collected blood samples from nestlings every five days through ~40 days of age, and tested the samples for antibodies against avian influenza virus (AIV), infectious bronchitis virus (IBV), and Toxoplasma gondii (toxoplasmosis). We found that AIV circulates widely and is present at high levels in nestlings, while toxoplasmosis is infrequent and IBV absent. Antibody levels depended on maternal transfer through early development and declined through Day 15 for toxoplasmosis and Day 25 for AIV. At this point, foster siblings became more similar than biological siblings, and antibody levels began to rise in response to external exposure. However, after the initial period of antibody decline, differences between foster and biological siblings were non-significant, suggesting that exposure to external sources does not vary substantially among nests ("Antibody Infographic"). Results are currently in preparation for submission to Journal of Experimental Biology (Part 1) and Proceedings of the Royal Society B (Part 2).
Although in-person dissemination was limited due to COVID-19, we partnered with a local high school in Marseille (lycée Jean Perrin) to present information on theory, implementation, and applications of mark-recapture studies in the classroom and in the field.
Our results from Amsterdam Island have important management and monitoring implications, as avian cholera is a serious risk for the endangered, endemic Amsterdam albatross (Diomedia amsterdamensis). We recorded non-breeding skuas with active avian cholera infections traveling or foraging in Amsterdam albatross breeding areas, while no breeders did so. Our work highlights the importance of tracking movements of non-breeders as well as breeders in order to fully measure the effects of rodent eradication on disease dynamics in this system and assess how rodent eradication might affect transmission risk to Amsterdam albatross.
Our results from Frioul provide important insights for management of yellow-legged gulls and their use as sentinels for pathogen circulation. We show that egg oiling, which is commonly used to control populations in this species, could lead to longer residence times of gulls in breeding areas. We also document long-distance overland migration by this population to urban centers and agricultural areas, which could result in transfer of persistent and emerging pathogens between otherwise distinct habitats. Finally, we show that antibody levels in chicks are a useful index of localized pathogen circulation around the breeding colony provided that maternal effects are controlled for by sampling during later stages of chick growth (i.e. closer to fledging). Monitoring antibody levels in chicks could be a useful tool for identifying emerging pathogens or detecting changes in the circulation of known zoonotic agents in coastal urban centers.
We also developed and tested a new technique for following nestlings using modified Chipolo ONE loggers (Chipolo d.o.o. Gabrsko, Slovenia), which are designed to locate lost objects via Bluetooth connections. By repackaging loggers in waterproof plastic casing, we could attach them to gull nestlings and use them to relocate chicks once they began to move away from their nests at about two weeks of age. We plan to write a technical note describing this methodology for an ornithological journal.
Our results from Frioul provide important insights for management of yellow-legged gulls and their use as sentinels for pathogen circulation. We show that egg oiling, which is commonly used to control populations in this species, could lead to longer residence times of gulls in breeding areas. We also document long-distance overland migration by this population to urban centers and agricultural areas, which could result in transfer of persistent and emerging pathogens between otherwise distinct habitats. Finally, we show that antibody levels in chicks are a useful index of localized pathogen circulation around the breeding colony provided that maternal effects are controlled for by sampling during later stages of chick growth (i.e. closer to fledging). Monitoring antibody levels in chicks could be a useful tool for identifying emerging pathogens or detecting changes in the circulation of known zoonotic agents in coastal urban centers.
We also developed and tested a new technique for following nestlings using modified Chipolo ONE loggers (Chipolo d.o.o. Gabrsko, Slovenia), which are designed to locate lost objects via Bluetooth connections. By repackaging loggers in waterproof plastic casing, we could attach them to gull nestlings and use them to relocate chicks once they began to move away from their nests at about two weeks of age. We plan to write a technical note describing this methodology for an ornithological journal.