Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls
Abstract Monitoring pathogen circulation in wildlife sentinel populations can help to understand and predict the spread of disease at the wildlife-livestock-human interface. Immobile young provide a useful target population for disease surveillance, since they can be easily captured for sampling and...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-02-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-024-54796-1 |
| _version_ | 1797275214173700096 |
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| author | Juliet S. Lamb Jérémy Tornos Mathilde Lejeune Thierry Boulinier |
| author_facet | Juliet S. Lamb Jérémy Tornos Mathilde Lejeune Thierry Boulinier |
| author_sort | Juliet S. Lamb |
| collection | DOAJ |
| description | Abstract Monitoring pathogen circulation in wildlife sentinel populations can help to understand and predict the spread of disease at the wildlife-livestock-human interface. Immobile young provide a useful target population for disease surveillance, since they can be easily captured for sampling and their levels of antibodies against infectious agents can provide an index of localized circulation. However, early-life immune responses include both maternally-derived antibodies and antibodies resulting from exposure to pathogens, and disentangling these two processes requires understanding their individual dynamics. We conducted an egg-swapping experiment in an urban-nesting sentinel seabird, the yellow-legged gull, and measured antibody levels against three pathogens of interest (avian influenza virus AIV, Toxoplasma gondii TOX, and infectious bronchitis virus IBV) across various life stages, throughout chick growth, and between nestlings raised by biological or non-biological parents. We found that levels of background circulation differed among pathogens, with AIV antibodies widely present across all life stages, TOX antibodies rarer, and IBV antibodies absent. Antibody titers declined steadily from adult through egg, nestling, and chick stages. For the two circulating pathogens, maternal antibodies declined exponentially after hatching at similar rates, but the rate of linear increase due to environmental exposure was significantly higher in the more prevalent pathogen (AIV). Differences in nestling antibody levels due to parental effects also persisted longer for AIV (25 days, vs. 14 days for TOX). Our results suggest that yellow-legged gulls can be a useful sentinel population of locally transmitted infectious agents, provided that chicks are sampled at ages when environmental exposure outweighs maternal effects. |
| first_indexed | 2024-03-07T15:11:07Z |
| format | Article |
| id | doaj.art-783b5b8309144531aa9aa60235e40388 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-07T15:11:07Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-783b5b8309144531aa9aa60235e403882024-03-05T18:38:57ZengNature PortfolioScientific Reports2045-23222024-02-0114111110.1038/s41598-024-54796-1Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gullsJuliet S. Lamb0Jérémy Tornos1Mathilde Lejeune2Thierry Boulinier3Centre d’Écologie Fonctionnelle et Évolutive (CEFE), UMR CNRS 5175, University of Montpellier, EPHE, University Paul Valéry Montpellier 3, IRDCentre d’Écologie Fonctionnelle et Évolutive (CEFE), UMR CNRS 5175, University of Montpellier, EPHE, University Paul Valéry Montpellier 3, IRDCentre d’Écologie Fonctionnelle et Évolutive (CEFE), UMR CNRS 5175, University of Montpellier, EPHE, University Paul Valéry Montpellier 3, IRDCentre d’Écologie Fonctionnelle et Évolutive (CEFE), UMR CNRS 5175, University of Montpellier, EPHE, University Paul Valéry Montpellier 3, IRDAbstract Monitoring pathogen circulation in wildlife sentinel populations can help to understand and predict the spread of disease at the wildlife-livestock-human interface. Immobile young provide a useful target population for disease surveillance, since they can be easily captured for sampling and their levels of antibodies against infectious agents can provide an index of localized circulation. However, early-life immune responses include both maternally-derived antibodies and antibodies resulting from exposure to pathogens, and disentangling these two processes requires understanding their individual dynamics. We conducted an egg-swapping experiment in an urban-nesting sentinel seabird, the yellow-legged gull, and measured antibody levels against three pathogens of interest (avian influenza virus AIV, Toxoplasma gondii TOX, and infectious bronchitis virus IBV) across various life stages, throughout chick growth, and between nestlings raised by biological or non-biological parents. We found that levels of background circulation differed among pathogens, with AIV antibodies widely present across all life stages, TOX antibodies rarer, and IBV antibodies absent. Antibody titers declined steadily from adult through egg, nestling, and chick stages. For the two circulating pathogens, maternal antibodies declined exponentially after hatching at similar rates, but the rate of linear increase due to environmental exposure was significantly higher in the more prevalent pathogen (AIV). Differences in nestling antibody levels due to parental effects also persisted longer for AIV (25 days, vs. 14 days for TOX). Our results suggest that yellow-legged gulls can be a useful sentinel population of locally transmitted infectious agents, provided that chicks are sampled at ages when environmental exposure outweighs maternal effects.https://doi.org/10.1038/s41598-024-54796-1 |
| spellingShingle | Juliet S. Lamb Jérémy Tornos Mathilde Lejeune Thierry Boulinier Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls Scientific Reports |
| title | Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| title_full | Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| title_fullStr | Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| title_full_unstemmed | Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| title_short | Rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| title_sort | rapid loss of maternal immunity and increase in environmentally mediated antibody generation in urban gulls |
| url | https://doi.org/10.1038/s41598-024-54796-1 |
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