skip to main content


Title: A trait‐based framework for predicting foodborne pathogen risk from wild birds
Abstract

Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from farms, jeopardizing conservation efforts. However, it remains unclear which species, particularly birds, pose the greatest risk to food safety. Using >11,000 pathogen tests and 1565 bird surveys covering 139 bird species from across the western United States, we examined the importance of 11 traits in mediating wild bird risk to food safety. We tested whether traits associated with pathogen exposure (e.g., habitat associations, movement, and foraging strategy) and pace‐of‐life (clutch size and generation length) mediated foodborne pathogen prevalence and proclivities to enter farm fields and defecate on crops.Campylobacterspp. were the most prevalent enteric pathogen (8.0%), whileSalmonellaand Shiga‐toxin producingEscherichia coli(STEC) were rare (0.46% and 0.22% prevalence, respectively). We found that several traits related to pathogen exposure predicted pathogen prevalence. Specifically,Campylobacterand STEC‐associated virulence genes were more often detected in species associated with cattle feedlots and bird feeders, respectively.Campylobacterwas also more prevalent in species that consumed plants and had longer generation lengths. We found that species associated with feedlots were more likely to enter fields and defecate on crops. Our results indicated that canopy‐foraging insectivores were less likely to deposit foodborne pathogens on crops, suggesting growers may be able to promote pest‐eating birds and birds of conservation concern (e.g., via nest boxes) without necessarily compromising food safety. As such, promoting insectivorous birds may represent a win‐win‐win for bird conservation, crop production, and food safety. Collectively, our results suggest that separating crop production from livestock farming may be the best way to lower food safety risks from birds. More broadly, our trait‐based framework suggests a path forward for co‐managing wildlife conservation and food safety risks in farmlands by providing a strategy for holistically evaluating the food safety risks of wild animals, including under‐studied species.

 
more » « less
Award ID(s):
1824871
NSF-PAR ID:
10365940
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  more » ;   « less
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecological Applications
Volume:
32
Issue:
2
ISSN:
1051-0761
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The impacts of urbanization on bird biodiversity depend on human–environment interactions that drive land management. Although a commonly studied group, less attention has been given to public perceptions of birds close to home, which can capture people's direct, everyday experiences with urban biodiversity. Here, we used ecological and social survey data collected in the metropolitan region of Phoenix, Arizona, USA, to determine how species traits are related to people's perceptions of local bird communities. We used a trait‐based approach to classify birds by attributes that may influence human–bird interactions, including color, size, foraging strata, diet, song, and cultural niche space based on popularity and geographic specificity. Our classification scheme using hierarchical clustering identified four trait categories, labeled as Metropolitan (gray, loud, seedeaters foraging low to ground), Familiar (yellow/brown generalist species commonly present in suburban areas), Distinctive (species with distinguishing appearance and song), and Hummingbird (hummingbird species, small and colorful). Strongly held beliefs about positive or negative traits were also more consistent than ambivalent ones. The belief that birds were colorful and unique to the regional desert environment was particularly important in fortifying perceptions. People largely perceived hummingbird species and birds with distinctive traits positively. Similarly, urban‐dwelling birds from the metropolitan trait group were related to negative perceptions, probably due to human–wildlife conflict. Differences arose across sociodemographics (including income, age, education, and Hispanic/Latinx identity), but explained a relatively low amount of variation in perceptions compared with the bird traits present in the neighborhood. Our results highlight how distinctive aesthetics, especially color and song, as well as traits related to foraging and diet drive perceptions. Increasing people's direct experiences with iconic species tied to the region and species with distinguishing attributes has the potential to improve public perceptions and strengthen support for broader conservation initiatives in and beyond urban ecosystems.

     
    more » « less
  2. Abstract

    Crop raiding by wildlife poses major threats to both wildlife conservation and human well‐being in agroecosystems worldwide. These threats are particularly acute in many parts of Africa, where crop raiders include globally threatened megafauna such as elephants, and where smallholder agriculture is a primary source of human livelihood. One framework for understanding herbivore feeding behaviour, the forage‐maturation hypothesis, predicts that herbivores should align their movements with intermediate forage biomass (i.e., peak green‐up); this phenomenon is known as “surfing the green wave.” Crop‐raiding elephants, however, often consume not just foliage, but also fruits and tubers (e.g., maize and potatoes), which generally mature after seasonal peaks in photosynthetic activity. Thus, although elephants have been reported to surf the green wave in natural habitats, they may utilize a different strategy in cultivated landscapes by selecting crops that are “browning down.”

    We sought to understand the factors that underpin movement of elephants into agricultural landscapes.

    In Mozambique's Gorongosa National Park, we used movement data from GPS‐collared elephants, together with precipitation records, remotely sensed estimates of landscape greenness (NDVI), DNA‐based diet analysis, measurements of plant nutritional quality and survey‐based metrics of crop availability to understand spatiotemporal variation in elephant crop‐raiding behaviour.

    Elephants tracked peak NDVI while foraging inside the Park. During the dry season, however, when NDVI within the Park declined and availability of mature crops was high, crop raiding increased dramatically, and elephants consistently selected crop plants that were browning down while foraging in cultivated landscapes. Crops contained significantly higher digestible energy than wild food plants, but comparable (and sometimes lower) levels of digestible protein, suggesting that this foraging strategy maximized energy rather than protein intake.

    Our study is the first to combine GPS tracking data with high‐resolution diet analysis and community‐based reporting of crop availability to reveal fine‐scale plasticity in foraging behaviour of elephants at the human–wildlife interface. Our results extend the forage‐maturation hypothesis by showing that elephants surf waves of plant brown‐down in cultivated landscapes. These findings can aid efforts to reduce human–elephant conflict by enabling wildlife managers to prioritize mitigation actions in time and space with limited resources.

     
    more » « less
  3. In September 2018, Hurricane Florence caused extreme flooding in eastern North Carolina, USA, a region highly dense in concentrated animal production, especially swine and poultry. In this study, floodwater samples (n=96) were collected as promptly post-hurricane as possible and for up to approx. 30 days, and selectively enriched for Campylobacter using Bolton broth enrichment and isolation on mCCDA microaerobically at 42°C. Only one sample yielded Campylobacter , which was found to be Campylobacter jejuni with the novel genotype ST-2866. However, the methods employed to isolate Campylobacter readily yielded Arcobacter from 73.5% of the floodwater samples. The Arcobacter isolates failed to grow on Mueller-Hinton agar at 25, 30, 37 or 42°C microaerobically or aerobically, but could be readily subcultured on mCCDA at 42°C microaerobically. Multilocus sequence typing of 112 isolates indicated that all were Arcobacter butzleri. The majority (85.7%) of the isolates exhibited novel sequence types (STs), with 66 novel STs identified. Several STs, including certain novel ones, were detected in diverse waterbody types (channel, isolated ephemeral pools, floodplain) and from multiple watersheds, suggesting the potential for regionally-dominant strains. The genotypes were clearly partitioned into two major clades, one with high representation of human and ruminant isolates and another with an abundance of swine and poultry isolates. Surveillance of environmental waters and food animal production systems in this animal agriculture-dense region is needed to assess potential regional prevalence and temporal stability of the observed A. butzleri strains, as well as their potential association with specific types of food animal production. IMPORTANCE Climate change and associated extreme weather events can have massive impacts on the prevalence of microbial pathogens in floodwaters. However, limited data are available on foodborne zoonotic pathogens such as Campylobacter or Arcobacter in hurricane-associated floodwaters in rural regions with intensive animal production. With high density of intensive animal production as well as pronounced vulnerability to hurricanes, Eastern North Carolina presents unique opportunities in this regard. Our findings revealed widespread incidence of the emerging zoonotic pathogen Arcobacter butzleri in floodwaters from Hurricane Florence. We encountered high and largely unexplored diversity while also noting the potential for regionally-abundant and persistent clones. We noted pronounced partitioning of the floodwater genotypes in two source-associated clades. The data will contribute to elucidating the poorly-understood ecology of this emerging pathogen, and highlight the importance of surveillance of floodwaters associated with hurricanes and other extreme weather events for Arcobacte r and other zoonotic pathogens. 
    more » « less
  4. null (Ed.)
    Provisioning of wildlife, such as backyard bird feeding, can alter animal behavior and ecology in diverse ways. For species that are highly dependent on supplemental resources, it is critical to understand how variation in the degree of provisioning, as occurs naturally across backyards, alters wildlife behavior and ecology in ways potentially relevant to disease spread. We experimentally manipulated feeder density at suburban sites and tracked local abundance, foraging behaviors, body mass, and movement in House Finches (Haemorhous mexicanus (P.L. Statius Müller, 1776)), the primary host of a pathogen commonly spread at feeders. Sites with high feeder density harbored higher local House Finch abundance, and birds at these sites had longer feeding bouts and total time on feeders relative to sites with low feeder density. House Finches at high-density feeder sites had lower residual body mass despite greater apparent feeder access. Finally, birds first recorded at low-density feeder sites were more likely to move to neighboring high-density feeder sites than vice versa. Because local abundance and time spent on feeders have both been linked with disease risk in this species, the effects of heterogeneity in bird feeder density on these traits may have important consequences for disease dynamics in this system and more broadly. 
    more » « less
  5. Introduction Campylobacter spp. infections are responsible for significant diarrheal disease burden across the globe, with prevalence thought to be increasing. Although wild avian species have been studied as reservoirs of Campylobacter spp., our understanding of the role of wild mammalian species in disease transmission and persistence is limited. Host factors influencing infection dynamics in wild mammals have been neglected, particularly life traits, and the role of these factors in zoonotic spillover risk is largely unknown. Methods Here, we conducted a systematic literature review, identifying mammalian species that had been tested for Campylobacter spp. infections (molecular and culture based). We used logistic regression to evaluate the relationship between the detection of Campylobacter spp. in feces and host life traits (urban association, trophic level, and sociality). Results Our analysis suggest that C. jejuni transmission is associated with urban living and trophic level. The probability of carriage was highest in urban-associated species ( p = 0.02793) and the most informative model included trophic level. In contrast, C. coli carriage appears to be strongly influenced by sociality ( p = 0.0113) with trophic level still being important. Detection of Campylobacter organisms at the genus level, however, was only associated with trophic level ( p = 0.0156), highlighting the importance of this trait in exposure dynamics across host and Campylobacter pathogen systems. Discussion While many challenges remain in the detection and characterization of Camploybacter spp., these results suggest that host life traits may have important influence on pathogen exposure and transmission dynamics, providing a useful starting point for more directed surveillance approaches. 
    more » « less