Dynamics of host-parasite interactions in spatially structured systems: dispersal and local interactions in seabirds
This research program has been developing as part of IPEV n°333 Program ‘PARASITO ARCTIQUE’ (set up and led since 1998 by Thierry BOULINIER, in collaboration with Karen McCOY of MIVEGEC) and is now also developping as part of IPEV n°1151 Program ‘ECOPATH’ (started in 2015), which focuses on the eco-epidémiology of directly transmitted and tick-borne infectious agents of colonial marine vertebrates in the sub-antarctic and antarctic.
Some key findings:
Black-legged kittiwakes put in their eggs maternal antibodies against Lyme disease Borrelia, a tick-borne infectious agent to which their nestlings are likely to be exposed to (Gasparini et al. 2001 Proc Roy Soc B, 2002 Ecology Letters)
Following key earlier theoretical and observatiobal studies on the use of public information in breeding habitat selection (Boulinier & Danchin 1997 Evol Ecol, Danchin et al. 1998 Ecology), we experimentally showed that the dispersal propensity of breeding black-legged kittiwakes that lost their eggs is affected by the breeding performance of their neighbours: if their neighbours were successful, they are much more likely to attend their nest until the end of the season and to be faithful to their breeding cliff than if their neighbours failed (Boulinier et al. 2008 Biology Letters).
The populations of the widely distributed seabird tick Ixodes uriae are structured among host populations (McCoy et al. 2001 JeB, 2005, Dietrich et al. 2012, J Biogeogr, 2014 Mol Ecol), which can have cascading effects on the circulation of tick-borne infectious agents such as Borrelia burdgoferi sensu lato and viruses.
In a study using multi-event capture-mark-recapture modelling to account for potential differences in recapture and resighting probabilities among categories of individuals, we showed that annual survival of breeding kittiwakes does not differ between individuals that are seropositive and seronegative against Lyme disease Borrelia (Chambert et al. 2012 Journal of Animal Ecology).
Prospecting by potential local recruits is likely a key behavioural aspect of breeding habitat selection, which can thus have important consequences for the ecology and evolution of dispersal and the role of behaviour in the response of populations to environmlental changes at different spatial scales (Boulinier et al. 1996 J Avian Biol, Boulinier & Danchin 1997 Evol Ecol, Reed et al. 1999 Current Ornithology). We recently highlithed the possible use of modern tracking devices to further explore these aspects, notably via the use of GPS to precisely track prospecting movements by failed breeders (Ponchon et al. 2013 MEE).
Using a matrix modelling approach, we showed that informed dispersal, such as breeding habitat selection strategies based on public information, can lead to faster population responses when abrupt environmental changes occur, which can reduce their risks of local extinctions and may be important to consider when attempting to project changes in species distribution (Ponchon et al. 2014 Diversity & Distribution).
In a review paper, we stress that not only migrating and foraging movements can be important for spreading parasites and pathogens, but also propecting movements (Boulinier et al. 2016 Integrative Comparative Biology): this is a key issue because little is known about such movements which can link, within a breeding season, sub-populations of hosts situated at a broad range of distances.
In the context of epizooties of avian cholera threatening albatros species on Amsterdam Island, we are exploring the potential usefulness of vaccination as a conservation tool. The first results on nestlings of yellow-nosed albatrosses are promising, with much higher survival of chicks from the vaccinated a year of outbreak compared to other chick groups (Bourret et al. 2018, Conservation Letters). This opens important perspectives, although a key issue is whether vaccination of breeding females could protect nestlings over several breeding attemps via the transfer of maternal antibodies; work is on-going on this aspect as part of ECOPATH 1151 IPEV program.
Evolutionary ecology of the maternal transfer of antibodies
This research program is developed as part of ANR Blanche EVEMATA grant (2012-2015), lead by Thierry BOULINIER, with 3 partner teams: Elsa JOURDAIN of INRA-Theix, Bertrand BED’HOMM of INRA Jouy-en-josas, and Karen McCOY of MIVEGEC Montpellier). It is also involving field work carried out as part of IPEV programmes ‘PARASITO-ARCTIQUE’ n°333 and ‘ECOPATH’ n°1151 (see above).
Maternal antibodies can persist in nestlings of the Cory’shearwater, a Procellariiform, much longer than what was previously known for birds. Such a long persistence can be expected given the extreme life history of Procellariiforms (the taxonomic group includes also albatrosses and petrels), notably their long growth period on the colony (Garnier et al. 2012 Proc Roy Soc B).
Maternal antibodies can be transmitted via allosuckling in mammals species, which may be important when considering the evolution of of allosucking. It also suggests a potential tool to explore further interactions between lactating females and offspring (Garnier et al. 2013 Mammalian Biology).
Tracking maternal antibodies against species infectious agents in the egg yolks of an abundant and widespread species like the Yellow-legged gull can allow tracking efficiently the presence and circulation of infectious agents. Such an approach allowed us to detect the presence of a Meaban-like flavivirus in a catalan colony, but also to show that its spatial circulation is currently very restricted (Arnal et al. 2014 PLoS One).
Our earlier finding that maternal antibodies in Cory’s shearwater can persist a long time in nestlings lead us to suggest that vaccination could be used an efficient conservation tool in species exposed to infectious disease killing nestlings and against which a vaccine can be made available (Garnier et al. 2012 PRSB). The efficiency of such an approach would nevertheless rests on the ability for a vaccinated female to transmit persisting antibodies several years in a row; this is what we showed in a study involving vaccination against NDV and the tracking of decay of antibodies in nestlings over several years (Ramos et al. 2014 American Naturalist)
Animal community dynamics in a spatial context
Taking into account heterogeneity in species detectability can be important in studies aiming at investigating factors affecting the dynamics of communities (Boulinier et al. 1998 Ecology). We proposed methods to do so (Nicols et al. 1998 Ecol Appl) and applied them to address key questions about landscape fragmentation and local extinction and turnover rates (Boulinier et al. 1998 PNAS), and the effects of species characteristics on their local dynamics of extinction/colonization (Doherty et al. 2003 PNAS).
Oasis bird communities represent an excellent system for addressing basic questions related to the dynamics of metapopulation and metacommunities (Selmi et al. 2004 Oecologia), but also for investigating the effects of human activities on local biodiversity: traditional oases host much richer bird communities than modern ones (Selmi et al. 2003 Biological Conservation).