The consequences of reservoir host eradication on disease epidemiology in animal communities

Abstract

Non-native species have often been linked with introduction of novel pathogens that spill over into native communities, and the amplification of the prevalence of native parasites. In the case of introduced generalist pathogens, their disease epidemiology in the extant communities remains poorly understood. Here, Sphaerothecum destruens, a generalist fungal-like fish pathogen with bi-modal transmission (direct and environmental) was used to characterise the biological drivers responsible for disease emergence in temperate fish communities. A range of biotic factors relating to both the pathogen and the surrounding host communities were used in a novel susceptible-exposed-infectious-recovered (SEIR) model to test how these factors affected disease epidemiology. These included: (i) pathogen prevalence in an introduced reservoir host (Pseudorasbora parva); (ii) the impact of reservoir host eradication and its timing and (iii) the density of potential hosts in surrounding communities and their connectedness. These were modelled across 23 combinations and indicated that the spill-over of pathogen propagules via environmental transmission resulted in rapid establishment in adjacent fish communities (<1 year). Although disease dynamics were initially driven by environmental transmission in these communities, once sufficient numbers of native hosts were infected, the disease dynamics were driven by intra-species transmission. Subsequent eradication of the introduced host, irrespective of its timing (after one, two or three years), had limited impact on the long-term disease dynamics among local fish communities. These outputs reinforced the importance of rapid detection and eradication of non-native species, in particular when such species are identified as healthy reservoirs of a generalist pathogen.

The rise of the rosette agent in Europe: An epidemiological enigma

“…The bimodal transmission of S. destruens (i.e. environmental/direct) has been shown using a Susceptible‐exposed‐infectious‐recovered model (SEIR) to increase its risk of emergence and persistence (Al‐Shorbaji, Gozlan, Roche, Britton, & Andreou, ; Al‐Shorbaji et al., , ). After the introduction of S. destruens in the wild, the predicted pattern of mortality suggests an initial rapid decline in local fish communities as empirically observed at site level by Gozlan et al.…”

“…The high number of infections predicted in high‐density populations suggests that fish farms would suffer severe consequences, as already shown in California (Harrell et al., ). In addition, the limited species diversity in fish farms with in some cases a monospecies production, would exacerbate further S. destruens emergence (Al‐Shorbaji et al., ). In natural communities, it is expected that shoaling species (e.g., sunbleak Leucaspius delineatus ) would experience higher levels of mortality compared to solitary species (e.g., carp Cyprinus carpio ), as hosts would be closely grouped in large numbers, allowing both direct and environmental transmission to take place.…”

“…This type of generalist parasite can infect a wide range of hosts with varying severity. Depending on the level of virulence and transmissibility in each fish host, the introduction of a second host with a different susceptibility can lead to a change in virulence in the pathogen and thus alter its potential transmissibility to the first host and the outcome of infection (Woolhouse, Taylor, & Haydon, ; Al‐Shorbaji, Roche, Gozlan, Britton, & Andreou, ; Al‐Shorbaji, Roche, Britton, Andreou, & Gozlan, ). For example, Al‐Shorbaji et al.…”

“…For example, Al‐Shorbaji et al. () epidemiological models show that within a fish community, despite S. destruens dynamics being initially driven by environmental transmission, once sufficient numbers of susceptible hosts are infected, the disease dynamics are then driven by intraspecies transmission. Whilst the introduction of the rosette agent S. destruens in Europe went unnoticed for over 45 years, recent findings have shed light on what remained to date an epidemiological enigma.…”

Individual behavioral differences and health of golden‐headed lion tamarins (Leontopithecus chrysomelas)

“…Our hypothesis that tamarins living in DFAM have health concerns was supported by our finding that they were infected with endoparasites while those living in cabruca had no endoparasites in collected feces. A human‐disturbed environment tends to have lower biodiversity (Al‐Shorbaji, Roche, Gozlan, Britton, & Andreou, 2016) and this could affect and increase the pressure of parasites in species with small populations such as the golden‐headed lion tamarin. Monteiro, Dietz, and Jansen (2010) reported an intestinal helminth egg prevalence of 49% for Prosthenorchis sp.…”