Impacts of Migratory Sandhill Cranes (Grus canadensis) on Microbial Water Quality in the Central Platte River, Nebraska, USA

Vogel, Jason R.; Griffin, Dale W.; Ip, Hon S.; Ashbolt, Nicholas J.; Moser, Matthew T.; Lu, Jingrang; Beitz, Mary K.; Ryu, Hodon; Domingo, Jorge W. Santo

doi:10.1007/s11270-013-1576-3

Cited by 14 publications

(14 citation statements)

References 61 publications

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“…For example, sandhill cranes ( Grus canadensis ), which are commonly infected with Campylobacter spp. during migration, increase enteric bacteria levels in water bodies where they forage (Pacha et al ., ; Lu et al ., ; Vogel et al ., ). Indeed, the only foodborne illness outbreak traced back to a wild bird source occurred from migrating sandhill cranes stopping over at a pea farm in Alaska (Gardner et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Are we overestimating risk of enteric pathogen spillover from wild birds to humans?

2020

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Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild birds are suspected sources for human infection. This has led to efforts to reduce pathogen spillover through deterrence of wildlife and removal of wildlife habitat, particularly within farming systems, which can compromise conservation efforts and the ecosystem services wild birds provide. Further, Salmonella spp. are a significant cause of avian mortality, leading to additional conservation concerns. Despite numerous studies of enteric bacteria in wild birds and policies to discourage birds from food systems, we lack a comprehensive understanding of wild bird involvement in transmission of enteric bacteria to humans. Here, we propose a framework for understanding spillover of enteric pathogens from wild birds to humans, which includes pathogen acquisition, reservoir competence and bacterial shedding, contact with people and food, and pathogen survival in the environment. We place the literature into this framework to identify important knowledge gaps. Second, we conduct a meta-analysis of prevalence data for three human enteric pathogens, Campylobacter spp., E. coli, and Salmonella spp., in 431 North American breeding bird species. Our literature review revealed that only 3% of studies addressed the complete system of pathogen transmission. In our meta-analysis, we found a Campylobacter spp. prevalence of 27% across wild birds, while prevalence estimates of pathogenic E. coli (20%) and Salmonella spp. (6.4%) were lower. There was significant bias in which bird species have been tested, with most studies focusing on a small number of taxa that are common near people (e.g. European starlings Sturnus vulgaris and rock pigeons Columba livia) or commonly in contact with human waste (e.g. gulls). No pathogen prevalence data were available for 65% of North American breeding bird species, including many commonly in contact with humans (e.g. black-billed magpie Pica hudsonia and great blue heron Ardea herodias), and our metadata suggest that some under-studied species, taxonomic groups, and guilds may represent equivalent or greater risk to human infection than heavily studied species. We conclude that current data do not provide sufficient information to determine the likelihood of enteric pathogen spillover from wild birds to humans and thus preclude management solutions. The primary focus in the literature on pathogen prevalence likely overestimates the probability of enteric pathogen spillover from wild birds to humans because a pathogen must survive long enough at an infectious dose and be a strain that is able to colonize humans to cause infection. We propose that future research should focus on the large number of under-studied species commonly in contact with people and food production and demonstrate shedding of bacterial strains pathogenic to humans into the environment where people may contact them. Finally, studies assessing the duration and intensity of bacterial shedding and survival of bacteria in the environme...

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Section: Introductionmentioning

confidence: 97%

Are we overestimating risk of enteric pathogen spillover from wild birds to humans?

2020

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“…Therefore, the transfer of both non-pathogenic and pathogenic microorganisms between conspecific hosts is likely to be highly facilitated in colonial birds (Rifkin et al, 2012). Investigation of 16S rRNA gene sequences in waterbird feces has revealed a high prevalence of waterborne gastrointestinal pathogenic strains of E. coli, Campylobacter and Salmonella (Lu et al, 2011; e.g., Waldenström et al, 2002; Wetzel and LeJeune, 2007; Vogel et al, 2013; Telesford-Checkley et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species

et al. 2019

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High dispersal rates are known to homogenize host’s population genetic structure in panmictic species and to disrupt host local adaptation to the environment. Long-distance dispersal might also spread micro-organisms across large geographical areas. However, so far, to which extent selection mechanisms that shape host’s population genetics are mirrored in the population structure of the enteric microbiome remains unclear. High dispersal rates and horizontal parental transfer may homogenize bacterial communities between breeding sites (homogeneous hypothesis). Alternatively, strong selection from the local environment may differentiate bacterial communities between breeding sites (heterogeneous hypothesis). Furthermore, selection from age-specific environmental or physiological factors may differentiate the microbiome between juveniles and adults. Here, we analyzed the cloacal bacterial 16S rRNA gene of fledgling greater flamingos, Phoenicopterus roseus, across nine western Mediterranean breeding sites and four breeding seasons (n = 731) and adult birds (n = 27) from a single site. We found that fledgling cloacal microbiome, as measured by alpha diversity, beta diversity, the relative abundance of assigned sequence variants (ASVs) belonging to a phylum and genus composition within phylum, varied significantly between sampling sites and across time within site despite high adult dispersal rates. The spatio-temporal effects were stronger on individual ASV absence/presence than on ASV abundance (i.e., than on core microbiome composition). Spatial effects had a stronger effect than temporal effects, particularly on ASV abundance. Our study supports the heterogeneous hypothesis whereby local environmental conditions select and differentiate bacterial communities, thus countering the homogenizing effects of high-dispersing host species. In addition, differences in core microbiome between adult vs. fledgling samples suggests that differences in age-specific environmental and/or physiological factors result in differential selection pressure of core enteric microbiome between age classes, even within the same environment. In particular, the genus Corynebacterium, associated with both seasonal fat uptake and migration in previous studies, was much more abundant in high-dispersing fledglings than in more resident adults. To conclude, selection mechanisms that shape the host’s genetic structure cannot be extended to the genetic structure of the enteric microbiome, which has important implications regarding our understanding of both host local adaptation mechanisms and enteric microbiome population genetics.

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“…One of the 21 field studies (Numberger et al 2019) was excluded because no location for field sampling sites was provided, and sampling sites from three studies (n¼2 sediment, n¼1 multiple) could only be approximated by a random point within Cambodia due to the lack of a more precise site description (Horm et al 2011(Horm et al , 2012aDeboosere et al 2012). The map was replicated by sample type, whereby the multiple category contained sampling sites where either water and feathers (n¼1 sampling site; Gaidet et al 2018) or water and sediment were collected (n¼6 sampling sites; Vong et al 2008;Stallknecht et al 2010;Horm et al 2012a;Vogel et al 2013).…”

Section: Methodsmentioning

confidence: 99%

“…Other solutions used to provide additional ecological context regarding the species of origin included collecting samples from single-species flocks (Gaidet et al 2018) and recording observed waterbird species abundance at the field site (Pé rez- Ramírez et al 2012). For studies collecting observational data, the majority reported on the most common waterbird species observed (Vogel et al 2013), whereas fewer performed systematic surveys of all waterbirds present (Zhang et al 2006;Hé naux et al 2012;Pé rez-Ramírez et al 2012;Densmore et al 2017).…”

Section: )mentioning

confidence: 99%

“…This limitation can be overcome by environmental DNA-or DNA barcoding-by using wild bird DNA found within the environmental sample itself to infer the host species (Lee et al 2010). Theoretically, environmental DNA could be used with all sample types, but has only been used with fecal and water samples in association with AIV surveillance (Lee et al 2010;Vogel et al 2013).…”

Section: Data Analysis and Interpretationmentioning

confidence: 99%

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A Systematic Review and Narrative Synthesis of the Use of Environmental Samples for the Surveillance of Avian Influenza Viruses in Wild Waterbirds

Coombe

Iwasawa

Byers

et al. 2021

Journal of Wildlife Diseases

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Impacts of Migratory Sandhill Cranes (Grus canadensis) on Microbial Water Quality in the Central Platte River, Nebraska, USA

Cited by 14 publications

References 61 publications

Are we overestimating risk of enteric pathogen spillover from wild birds to humans?

Are we overestimating risk of enteric pathogen spillover from wild birds to humans?

Offspring Microbiomes Differ Across Breeding Sites in a Panmictic Species

A Systematic Review and Narrative Synthesis of the Use of Environmental Samples for the Surveillance of Avian Influenza Viruses in Wild Waterbirds

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