Urbanized White Ibises (Eudocimus albus) as Carriers of Salmonella enterica of Significance to Public Health and Wildlife

Abstract

Worldwide, Salmonella spp. is a significant cause of disease for both humans and wildlife, with wild birds adapted to urban environments having different opportunities for pathogen exposure, infection, and transmission compared to their natural conspecifics. Food provisioning by people may influence these factors, especially when high-density mixed species flocks aggregate. White Ibises (Eudocimus albus), an iconic Everglades species in decline in Florida, are becoming increasingly common in urbanized areas of south Florida where most are hand-fed. We examined the prevalence of Salmonella shedding by ibises to determine the role of landscape characteristics where ibis forage and their behavior, on shedding rates. We also compared Salmonella isolated from ibises to human isolates to better understand non-foodborne human salmonellosis. From 2010-2013, 13% (n = 261) adult/subadult ibises and 35% (n = 72) nestlings sampled were shedding Salmonella. The prevalence of Salmonella shedding by ibises significantly decreased as the percent of Palustrine emergent wetlands and herbaceous grasslands increased, and increased as the proportion of open-developed land types (e.g. parks, lawns, golf courses) increased, suggesting that natural ecosystem land cover types supported birds with a lower prevalence of infection. A high diversity of Salmonella serotypes (n = 24) and strain types (43 PFGE types) were shed by ibises, of which 33% of the serotypes ranked in the top 20 of high significance for people in the years of the study. Importantly, 44% of the Salmonella Pulsed-Field Gel Electrophoresis patterns for ibis isolates (n = 43) matched profiles in the CDC PulseNet USA database. Of these, 20% came from Florida in the same three years we sampled ibis. Importantly, there was a negative relationship between the amount of Palustrine emergent wetland and the number of Salmonella isolates from ibises that matched human cases in the PulseNet database (p = 0.056). Together, our results indicate that ibises are good indicators of salmonellae strains circulating in their environment and they have both the potential and opportunity to transmit salmonellae to people. Finally, they may act as salmonellae carriers to natural environments where other more highly-susceptible groups (nestlings) may be detrimentally affected.

Fig 1. Map of Sites.

Fecal samples were collected from adult/subadult and nestling white ibises in Palm Beach, Broward and Miami-Dade counties, FL. The land cover for a 1 km radius surrounding each sampling site was determined using land cover maps.

Fig 2. Salmonella prevalence and habitat type.

Salmonella prevalence in white ibises is negatively influenced by cover of emergent wetlands (a) herbaceous grasslands (b) and positively influenced by open, developed land (c) in Palm Beach County, Florida.

Fig 3. Cluter analysis of Salmonella.

Cluster analysis of Salmonella isolated from ibises by pulsed-field gel electrophoresis (PFGE) patterns generated with the restriction enzyme XbaI. Tiff images of Salmonella PFGE patterns were compared using DNA pattern recognition software, BioNumerics (Applied Maths, Austin, TX). Level of similarity was calculated using the band-based Dice similarity coefficient, and clustering of samples was performed using the unweighted pair-group method with arithmetic averaging (UPGMA). Salmonella PFGE patterns, generated in this study, were compared to a BioNumerics database of PFGE entries of Salmonella isolates from water and various animal species. PFGE patterns generated for ibis isolates were compared against an in-house database of Salmonella PFGE profiles for isolates from water or other animal species. A dendrogram was generated of PFGE patterns including those from isolates with the same or similar pattern (≥75% similarity). Clusters with >75% similarities were labeled A-Z, a-c on dendrogram tree on the left.

Fig 4. Salmonella matches and emergent wetland habitat type.

Salmonella isolates from white ibises in Florida that matched human isolates in the PulseNet database were negatively, and marginally statistically significantly related with the land cover type Palustrine emergent wetland.