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 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.

Figure 1

Distribution of antibody levels against (a) avian influenza virus (AIV), (b) Toxoplasma gondii (TOX), and (c) infectious bronchitis virus (IBV) in yellow-legged gulls adults (n = 90), eggs (n = 108), nestlings (≤ 7 days old; n = 28) and chicks (> 7 days old; n = 114) on Frioul, 2021–2022. Note: we did not test for TOX and IBV antibodies in nestlings, or for IBV antibodies in eggs.

Figure 2

Changes in antibody concentrations from hatching (Day 0, egg stage) through fledging (Day 40) in yellow-legged gull chicks (n = 142) on Frioul, 2021–2022: (a) avian influenza virus (AIV), (b) Toxoplasma gondii (TOX), and (c) infectious bronchitis virus (IBV). Figure includes individual trajectories in antibody concentrations (light lines), fitted values derived from the best-fitting non-linear model combining exponential decrease in maternal antibodies and linear increase in antibody generation (heavy lines), and zero values (dashed lines).

Figure 3

Inter-pair differences in antibodies against (a) avian influenza virus (AIV) and (b) Toxoplasma gondii (TOX) between sets of biological siblings (blue) and foster siblings (pink) for yellow-legged gull chicks (n = 670 samples) from Day 0 (hatch) to Day 40 on Frioul, 2021. Dots show daily differences between siblings, and lines show mean differences across the population with 95% confidence intervals (shaded).

Figure 4

Generalized additive model fits of the relationship between sibling titre and predicted titre for a) avian influenza virus (AIV) and b) Toxoplasma gondii (TOX) at 5-day intervals for yellow-legged gulls on Frioul, 2021. Relationships are shown for biological siblings (solid red line) and foster siblings (dotted blue line) with shaded areas indicating 95% confidence intervals. Labels indicate chick age in days from 0 to 40.