Prevalence of Influenza A Antibodies in Yellow-Legged Gull (Larus michahellis) Eggs and Adults in Southern Tunisia

Abstract

Investigating the prevalence of anti-influenza A viruses (AIV) antibodies in wild birds can provide important information for the understanding of bird exposure to AIV, as well as for prevention purposes. We investigated AIV exposure in nature by measuring the prevalence of anti-AIV antibodies in the nests and adults of an abundant and anthropophilic waterbird species common around the Mediterranean sea, the yellow-legged gull (Larus michahellis). Sampling took place in two colonies located in the gulf of Gabès in southern Tunisia: Sfax and Djerba. Antibodies were detected in the two sites, with higher prevalence in adults, eggs, and nests at Sfax than Djerba. Across both colonies, clutches that were laid later in the season, and, thus, more likely by younger parents, showed lower prevalence. Using patch occupancy modeling applied to egg clutches, we found that it is unnecessary to sample all the eggs in a given nest; nest status (antibody positive or negative) can be reliably estimated from a single egg. Differences in the density of birds, notably Larids, between the two sites may explain the observed differences in prevalence. The higher concentration of Larids in the Sfax colony could favor the transmission of AIV to yellow-legged gulls. This study highlights the importance of further developing ecological-based approaches to the factors determining the circulation of infectious agents in species such as the yellow-legged gull, which exist at the interface between diverse biological communities and human activities.

Circulation of a Meaban-Like Virus in Yellow-Legged Gulls and Seabird Ticks in the Western Mediterranean Basin

“…In birds, adult females that have been exposed to infectious agents can develop humoral immune responses and transfer some of the antibodies produced to the yolk of their eggs [50], [51]. There is a positive correlation between the amount of antibodies in the egg yolk and the amount of antibodies in the plasma of breeding females at the time of laying [52], [53]; therefore, egg yolk antibodies can reflect a female's prior exposure to infectious agents. This indirect method can be useful if the host immune response is detectable for a relatively long time period [53], [54], which has been shown to be the case for WNV in other avian species [55], [56].…”

“…There is a positive correlation between the amount of antibodies in the egg yolk and the amount of antibodies in the plasma of breeding females at the time of laying [52], [53]; therefore, egg yolk antibodies can reflect a female's prior exposure to infectious agents. This indirect method can be useful if the host immune response is detectable for a relatively long time period [53], [54], which has been shown to be the case for WNV in other avian species [55], [56]. Partial clutches can be sampled over a large area that encompasses several host populations, and there is no need to capture breeding adults.…”

“…Partial clutches can be sampled over a large area that encompasses several host populations, and there is no need to capture breeding adults. Subsequently, the estimates of antibody prevalence obtained with the eggs can establish target locations that should be specifically surveyed in order to characterize the detected infectious agents [53], [54]. The yellow-legged gull offers several advantages in this regard.…”

“…Because of this behavior and the negative effect that these gulls have on other bird species, population control efforts, including egg sterilization campaigns, have been implemented around the Mediterranean Basin [32]. As a result, there are no conservation concerns when sampling yellow-legged gull eggs for eco-epidemiological purposes [53], [54].…”

Transfer of Maternal Antibodies against Avian Influenza Virus in Mallards (Anas platyrhynchos)

“…Circulating antibodies to H13 AIV in adult ring-billed gulls ( Larus delawarensis ) ranged between 82 and 92%, with antibody prevalence in 3-wk-old chicks ranging between 5 and 30% [10]. In yellow-legged gulls ( Larus michahellis ), 81% of females had circulating AIV antibodies and 51% of their eggs received these antibodies maternally [11]. In this species it was shown that maternal AIV antibodies in eggs reflected the circulating AIV antibodies of the laying females, and that the first-laid eggs received highest levels of maternal antibodies [12].…”