Abstract
Toxoplasma gondii is a protozoan parasite that uses felids as definitive hosts and warm-blooded animals as intermediate hosts. While the dispersal of T. gondii infectious oocysts from land to coastal waters has been well documented, transmission routes to pelagic species remain puzzling. We used the modified agglutination test (MAT titre ≥ 10) to detect antibodies against T. gondii in sera collected from 1014 pelagic seabirds belonging to 10 species. Sampling was carried out on eight islands of the Western Indian Ocean: Reunion and Juan de Nova (colonized by cats), Cousin, Cousine, Aride, Bird, Europa and Tromelin islands (cat-free). Antibodies against T. gondii were found in all islands and all species but the great frigatebird. The overall seroprevalence was 16.8% [95% CI: 14.5%-19.1%] but significantly varied according to species, islands and age-classes. The low antibody levels (MAT titres = 10 or 25) detected in one shearwater and three red-footed booby chicks most likely resulted from maternal antibody transfer. In adults, exposure to soils contaminated by locally deposited oocysts may explain the detection of antibodies in both wedge-tailed shearwaters on Reunion Island and sooty terns on Juan de Nova. However, 144 adults breeding on cat-free islands also tested positive. In the Seychelles, there was a significant decrease in T. gondii prevalence associated with greater distances to cat populations for species that sometimes rest on the shore, i.e. terns and noddies. This suggests that oocysts carried by marine currents could be deposited on shore tens of kilometres from their initial deposition point and that the number of deposited oocysts decreases with distance from the nearest cat population. The consumption of fishes from the families Mullidae, Carangidae, Clupeidae and Engraulidae, previously described as T. gondii oocyst-carriers (i.e. paratenic hosts), could also explain the exposure of terns, noddies, boobies and tropicbirds to T. gondii. Our detection of antibodies against T. gondii in seabirds that fish in the high sea, have no contact with locally contaminated soils but frequent the shores and/or consume paratenic hosts supports the hypothesis of an open-sea dispersal of T. gondii oocysts by oceanic currents and/or fish.
Highlights
The land-to-sea transport of the free infective forms of zoonotic protozoa, dispersed with the faeces of humans, pets and farm animals has a growing negative impact on public health and marine life [1, 2]
Based on the analysis of 1014 seabirds belonging to ten species sampled in the Western Indian Ocean, we found an overall prevalence of 16.8% of seabirds carrying antibodies against T. gondii
If we had considered only Modified agglutination test (MAT) titres 25, T. gondii prevalence would have been of 9.17% (93/1014), higher than prevalence reported for other seabird species such as the Galapagos penguin (Spheniscus mendiculus) and the flightless cormorant (Phalacrocorax harrisi), both sampled in the Galapagos Archipelago (Ecuador) in the Pacific Ocean (2.3% at MAT titre 25) [54]
Summary
The land-to-sea transport of the free infective forms of zoonotic protozoa (oocysts or cyst), dispersed with the faeces of humans, pets and farm animals has a growing negative impact on public health and marine life [1, 2]. Antibodies against T. gondii have been detected far away from potential contamination sources by cats as in Weddell seals, Leptonychotes weddellii, and elephant seals, Mirounga leonina, sampled in the Antarctic Peninsula [50, 51], or in pelagic dolphins [14, 46], as well as in pelagic seabirds breeding on felid-free islands [52,53,54] In all these cases, the transport of infectious oocysts by marine currents or by fish have been mentioned as the two likely routes of transmission of T. gondii to pelagic species but without evidence of the involvement of one and/or the other in the exposure of the species studied. Based on the literature on seabird diet, we discussed the relationship between the prevalence of T. gondii in seabirds and their consumption of paratenic-host fish
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