Summary
Birds introduce complex food-safety risks, as they carry multiple pathogens, are difficult to exclude from farms, and regularly defecate on crops. Yet very few wild bird species have been studied, and those that have form a minority of farm bird communities. Moreover, existing studies stop at examining pathogen prevalence in birds and do not holistically assess foodsafety risk. For a species to pose a significant risk, it must carry pathogens, visit fields, defecate on crops, and produce feces that support pathogen survival. Here, we propose to first identify species that carry pathogenic E. coli, Salmonella, and Campylobacter by coupling existing studies with assays of field-collected feces. Second, we will survey birds and collect feces on 15-20 farms near rangeland, natural habitats, or produce farms to determine which species enter farms and defecate on crops and in which contexts. Third, we will compare E. coli survival between feces placed on different substrates (crops, organic/conventional soils, plastic mulch) and between feces from different species. Finally, we will compile holistic risk assessments for >50 species into a photographic guide to help growers identify and manage birds. Ultimately, we hope to help growers implement practices that bolster beneficial species without compromising food safety.
Technical Abstract
Foodborne disease outbreaks attributed to wildlife have heightened pressure on growers to prevent wildlife from entering their farms (Beretti and Stuart 2007, Gardner et al. 2011, Langholz and Jay-Russell 2013, Baur et al. 2016). Birds are of particular concern as they carry enteric pathogens and move long distances, including between livestock operations and fresh produce fields (Rivadeneira et al. 2016, Navarro-Gonzalez et al. 2019, Smith et al. 2020b). As a result, growers often implement economically and ecologically costly measures to prevent bird intrusion (e.g., bird netting and habitat removal; Beretti and Stuart 2007, Karp et al. 2015, Olimpi et al. 2019). However, despite widespread concern, our knowledge of the risks posed by different species by farming context is still in its infancy. Few species have been studied, with disproportionate focus on species that frequent feedlots, refuse sites, or water bodies rather than crop fields (Smith et al. 2020b). Moreover, no studies have assessed the entire pathogen spillover cycle; that is, the combined likelihood that bird species carry pathogens, enter farms, defecate on crops, and produce feces that enable pathogen survival (Smith et al. 2020b). We will produce holistic food-safety risk assessments for wild birds on produce farms in California. We have already assembled a database of ~10,000 pathogen tests across ~100 bird species (i.e., Campylobacter spp., Shiga-toxin producing E. coli, and Salmonella spp. assays). First, we will capture wild birds on or near farms, collect their feces, and test them for each pathogen, prioritizing birds that are poorly represented in our database, especially those that use nest boxes. Second, we will quantify how proximity to rangeland affects bird abundance on farms and identify species most likely to defecate on crops. Specifically, across 15-20 farms, we will census birds, collect feces, and use DNA barcoding to identify which species produced ~1,000 fecal samples. Third, we will conduct laboratory and field experiments to estimate E. coli survival curves in feces from different bird species, placed on lettuce, organic/conventional soils, or plastic. Finally, we will combine our data on pathogen prevalence, defecation rates, and pathogen survival to develop risk assessments for common farmland bird species. Assessing which species increase near rangeland will allow us to contextualize our findings and help farmers develop farm-specific management strategies. For example, based on preliminary data, we suspect birds associated with livestock will be more likely to carry pathogens, intrude into farms, and defecate on crops. If true, then growers near rangeland would be advised to deter birds, whereas those further away may be able to co-manage their farms for food safety and bird conservation. Indeed, farmers regularly use nest boxes to attract insect-eating birds to their farms and control crop pests (Jedlicka et al. 2011): we will assess the food-safety risks associated with these species. Upon completion, we will disseminate our risk assessments and management strategies through webinars and a photographic guide that will help growers identify birds on their farms and assess their risks.
Research Objectives
Our objectives are four-fold (Figure 1 (see poster PDF for figures):
1. Combine existing pathogen databases with Campylobacter, Salmonella, and STEC assays of field-collected feces, focusing on under-sampled species that frequent produce farms.
2. Quantify how proximity to rangeland affects bird community composition and fecal densities across 20 farms by censusing birds, collecting feces, and using DNA barcoding to identify species defecating on crops.
3. Compare E. coli survival in bird feces placed on lettuce plants, soils, and plastic mulch, including farmland species that defecate large (e.g., Wild Turkey) and small (e.g., Western Bluebird) feces.
4. Combine data on pathogen prevalence, fecal densities, and pathogen survival to develop holistic risk assessments for farmland birds as well as associated photo guides to aid on-farm management.
Findings & Recommendations
Results from this project answered at least three questions of relevance to the produce industry that could be used to guide future risk assessments and farming practices for food-safety.
First, which, if any, bird species carry significant food-safety risks? Especially when combined with prior datasets [13], data from this project suggest that foodborne pathogens are very rare in wild birds within farming landscapes. Across 5,247 and 4,647 individuals, STEC and Salmonella have been detected in only 0.2% and 0.4% of identified birds. While Campylobacter spp. were more prevalent (5.8% of 3,577 birds), it remains unclear whether the strains found in birds cause human illnesses [10,13,20,21]. Still, some bird species present higher risks than others. Holistic risk analyses singled out three species as potentially problematic: Common Raven, American Robin, and European Starling. More generally, data from this project and prior studies [13] suggest that some level of concern may be warranted if livestock-associated species, species that form large flocks, and larger species that defecate large feces are regularly seen in vulnerable produce fields [13]. On the other hand, results suggest that small, insect-eating birds carry low food-safety risks, including species that occupy artificial nest boxes in the Western United States. Erecting nest boxes to attract pest-eating birds is thus unlikely to compromise food safety. That said, several non-native species occasionally usurp nest boxes and carry relatively higher risks (i.e., House Sparrows and European Starlings). Following established guidance for deterring nesting and/or removing nests from these species may thus be prudent, from both a food-safety and a conservation perspective (https://nestwatch.org/learn/all-aboutbirdhouses/managing-house-sparrows-and-european-starlings/).
Second, when and where might food-safety risks from birds be greatest? Though most prior studies of birds and food safety focused on spring and summer [14,47,48] (but see [11,49]), bird abundance and fecal contamination risk were highest in fall. Large flocks were also prevalent in fall, suggesting more vigilance may be needed during late-season harvests. Within farms, fecal contamination appears to be more likely at field edges. Across farms, landscape analyses are ongoing. Still, prior work suggests food-safety risks from birds may be higher near livestockgrazed areas and in crop monoculture landscapes compared to diversified farms surrounded by semi-natural habitats [12–14,47,48]. This is likely because large flocks of livestock-associated species are often found in monoculture landscapes, whereas diverse communities of species unlikely to carry pathogens are often found in more complex landscapes [12–14,47,48]. These findings align with a broader literature that has coalesced around the idea that removing noncrop vegetation near farms does not help achieve food-safety goals [1,50–52].
Third, and finally, what should growers do when they encounter bird feces in their fields? Because bird feces are so ubiquitous in farm fields, implementing no-harvest buffers around every fecal deposit in the field would be cost prohibitive. Pathogen survival experiments suggest that E. coli persistence in bird feces is very low, especially in small feces deposited on soil. Because pathogens are rare in wild birds, growers could thus choose to implement no-harvest buffers around large bird feces deposited on crops and ignore small feces on soil without incurring major food-safety risks. Fortuitously, small birds that defecate small feces dominate farmland bird communities and most feces are deposited on soil. Thus, ignoring small feces on soils would dramatically decrease crop losses associated with no-harvest buffers.
In summary, results from this project suggest that produce farms can be co-managed for food safety, crop production, and bird conservation. Birds are ubiquitous across nearly all farming contexts, and their presence is not necessarily a problem. Indeed, foodborne pathogens are rare in birds, and, in most cases, pathogens do not persist in bird feces for long. Therefore, instead of a deterring all birds from farm fields, exclusion efforts might instead focus on specific contexts; for example, if large flocks of large-bodied birds are visiting produce fields near a potential pathogen source (e.g., livestock operations). Doing so could help growers avoid unnecessary losses associated with no-harvest buffers, contribute to bird conservation, and even enhance pest control or other recognized benefits associated with birds on farms.