Exposure of yellow-legged gulls to Toxoplasma gondii along the Western Mediterranean coasts: Tales from a sentinel

Abstract

Efficiently tracking and anticipating the dynamics of infectious agents in wild populations requires the gathering of large numbers of samples, if possible at several locations and points in time, which can be a challenge for some species. Testing for the presence of specific maternal antibodies in egg yolks sampled on the colonies could represent an efficient way to quantify the exposure of breeding females to infectious agents, particularly when using an abundant and widespread species, such as the yellow-legged gull (Larus michahellis). We used such an approach to explore spatio-temporal patterns of exposure to Toxoplasma gondii, a pathogenic protozoan responsible of toxoplasmosis in humans and other warm-blooded vertebrates. First, we tested the validity of this approach by exploring the repeatability of the detection of specific antibodies at the egg level using two different immunoassays and at the clutch level using an occupancy model. Then, samples gathered in 15 colonies from France, Spain and Tunisia were analysed using an immunoassay detecting antibodies specifically directed against T. gondii. Prevalence of specific antibodies in eggs was overall high while varying significantly among colonies. These results revealed that T. gondii circulated at a large spatial scale in the western Mediterranean yellow-legged gull population, highlighting its potential role in the maintenance community of this parasite. Additionally, this study illustrates how species commensal to human populations like large gulls can be used as wildlife sentinels for the tracking of infectious agents at the human-wildlife interface, notably by sampling eggs.

Keywords: Eco-epidemiology; Immunoassay; Mediterranean region; Sampling strategy; Stable isotope analysis; Toxoplasma gondii.

Graphical abstract

Fig. 1

Map of prevalences of anti-T. gondii antibodies in yellow-legged gull egg yolk samples in 2009 (a) and 2016 (b) illustrating the spatial variability. RIO: Riou; FRI: Frioul; CAR: Carteau; VIC: Vic-la-Gardiole; GRU: Gruissan; HOT: Hortel; SID: Sidrière; COR: Corrège; MED: Medes; BCN: Barcelona; EBR: Ebro Delta; DRA: Dragonera; AIR: Illa de l’Aire; SSF: Sfax; HDJ: Djerba. Coloured circles highlight the colonies in which temporal variations were explored (Fig. 2).Sample sizes and confidence intervals are given in Appendix A, Table S1.1. Base map: esri^©. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2

Limited temporal variations of the prevalence of anti-T. gondii antibody in yellow-legged gull egg yolk samples between 2009 and 2016 in three colonies: Frioul, Gruissan and Medes Islands. Curves correspond to cubic splined fitted to the yearly prevalences for visualisation purposes only. Bars indicate 95% Clopper-Pearson confidence intervals. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3

Location and status of yellow-legged gull nests sampled in 2016 and screened for anti-T.gondii antibodies. Base map: Google^©. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4

Biplots of δ¹³C and δ¹⁵N (a) and δ³⁴S and δ¹⁵N (b) representing the isotopic variability of yellow-legged gull albumen samples as a response of their immunological status against T. gondii. Isotopic signatures (as a proxy of females' diet) and egg/nest immunological status (as a proxy of females' exposure to the parasite) does not appear to be related. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)