Emerging infectious disease: An underappreciated area of strategic concern for food security
Funding information
WAB receives support from the Conselho Nacional em Ciência e Tecnologia (CNPq-Brazil; ref: 303940/2015-8).
Abstract
Emerging infectious diseases (EIDs) increasingly threaten global food security and public health. Despite technological breakthroughs, we are losing the battle with (re)emerging diseases as treatment costs and production losses rise. A horizon scan of diseases of crops, livestock, seafood and food-borne illness suggests these costs are unsustainable. The paradigm of coevolution between pathogens and particular hosts teaches that emerging diseases occur only when pathogens evolve specific capacities that allow them to move to new hosts. EIDs ought to be rare and unpredictable, so crisis response is the best we can do. Alternatively, the Stockholm Paradigm suggests that the world is full of susceptible but unexposed hosts that pathogens could infect, given the opportunity. Global climate change, globalized trade and travel, urbanization and land-use changes (often associated with biodiversity loss) increase those opportunities, making EID frequent. We can, however, anticipate their arrival in new locations and their behaviour once they have arrived. We can ‘find them before they find us’, mitigating their impacts. The DAMA (Document, Assess, Monitor, Act) protocol alters the current reactive stance and embodies proactive solutions to anticipate and mitigate the impacts of EID, extending human and material resources and buying time for development of new vaccinations, medications and control measures.
1 INTRODUCTION
Our world is experiencing rapid and accelerating climate changes that affect the sustainability, availability and security of global food resources. In 2011, the Consultative Group on International Agricultural Research (CGIAR) under the Research Program on Climate Change, Agriculture and Food Security (CCAFS) summarized and mapped projected hotspots for food insecurity induced by climate change. A core finding was that increasing temperatures will negatively and directly affect security and hunger among more than 170 million food-insecure and crop-dependent people across West, Central and East Africa, India and Bangladesh and South-East Asia within a few decades (Ericksen et al., 2011).
Pathogens and diseases have only recently been viewed as direct threats to food security. The initial emergence of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (Coronaviridae, Sarbecovirus sp.) from live animal food markets changed that, implicating emerging infectious diseases as substantial factors limiting the production and distribution of food, contributing to global food insecurity (Baudron & Liégeois, 2020; Benton, 2020; Laborde et al., 2020). The cumulative monetary impact is considerable, with a conservative global estimate in the range of 21 to 31 trillion dollars (Giggacher, 2020). In the United States, costs have exceeded 16 trillion dollars or about 90% of the annual gross domestic product (Cutler & Summers, 2020). The cost in human suffering and mortality cannot be measured empirically. Of considerable concern are conditions in food-crisis countries where an estimated 80% of regional populations rely on agriculture directly and indirectly. Especially critical are disruptions to food production and distribution, and impacts from market losses, breakdown in transportation supply chains and restrictions for access to arable lands (FAO, 2020).
Prior to the ongoing pandemic, however, a broad array of pathogens infecting people, animals and crops have produced a threat network that challenges the sustainability and security of agricultural and food systems (Brooks et al., 2019, 2020). A recent projection based on general circulation models (GCMs) suggested that, while yields of major temperate and tropical crops are likely to increase, disease risk will expand more at higher latitudes with increasing burdens of known pathogens (Chaloner et al., 2020). In the so-called food-secure regions of the Northern Hemisphere, emerging pathogens are anticipated to significantly and directly increase the threats to food resources. Climate-mediated impacts are in synergy with pathogens heightening vulnerability of food resources broadening and accelerating challenges to sustainability of food production systems and trade (Scheelbeek et al., 2020). Global trade and land-use change also trigger pathogen emergence, elevating threats to crop yield and agricultural systems (Baudron & Liégeois, 2020; Bebber et al., 2014). Furthermore, a recent Global Survey on Crop Losses indicated that current impacts and disruption occur where crop health management is poor or underdeveloped, and recommended devoting more effort to improving management of pests and pathogens (Savary et al., 2019). Plant diseases may also produce indirect effects, such as health and environmental issues associated with pesticides (Bernardes et al., 2015; Rohr et al., 2019), that are difficult to monetize (Ibrahim, 2016).
Despite nearly two centuries of accumulated experience and technological expertise, we are losing the battle to contain and diminish emerging diseases of our crops and livestock. Why is that so? One reason is that we take diseases of the species we eat less seriously than we do the diseases of us. Treatment costs and production losses due to infectious disease in crops and livestock are viewed as the cost of business and passed along to consumers as higher food prices. Even when there is a significant event, such as the recent African swine fever (African swine fever virus, Asfiviridae, Asfivirus sp.) outbreak in Asia and Europe, emerging diseases in food species rarely become news items. A second, more important reason pertains to how scientists perceive the relationship between pathogens and their hosts.
The prevailing paradigm assumes that pathogen capacities are selected strongly for coping with one host. The more narrowly specialized a pathogen is with respect to that host, the less likely it is thought to have the capacity to switch to novel hosts. Pathogens must evolve new capacities in order to colonize new hosts and produce emergent disease (Parrish & Kawaoka, 2005). Those novel capacities must satisfy two contradictory demands—endow some members of the pathogen population in the original host with the ability to survive in another host, but not be eliminated from the original host by strong selection against less than optimally adapted variants. Given that mutations are rare and undirected, the emergence of such specific mutations means that host switching should be rare. This process of coevolution is thus seen as a kind of evolutionary firewall against emerging disease. Nonetheless, emerging diseases have become increasingly common throughout the world in the past two generations. Because this is inconsistent with the traditional paradigm, it has been dubbed the Parasite Paradox. A new understanding of the evolutionary biology of pathogen–host associations called the Stockholm Paradigm resolves this paradox (Agosta & Brooks, 2020; Agosta et al., 2010; Araujo et al., 2015; Brooks et al., 2014, 2019; Hoberg et al., 2015; Hoberg & Brooks, 2015; Nylin et al., 2018).
2 THE STOCKHOLM PARADIGM AND EMERGING INFECTIOUS DISEASES IN FOOD SECURITY
Two Darwinian principles underly the Stockholm Paradigm. First, all outcomes of natural selection are local. All hosts in all parts of the world that could be infected by a pathogen form the pathogen's ‘fundamental fitness space’ while hosts that are infected comprise the pathogen's ‘realized fitness space’. A coevolutionary arms race involving one pathogen and one host at one place involves only realized fitness space, and thus will not affect susceptible but unexposed hosts in other places. The smaller the realized fitness space compared to fundamental fitness space, the greater the potential for pathogens to colonize new hosts without having to wait for new genetic capacities to evolve. This potential is called ecological fitting. Second, evolution is conservative. Pathogens and hosts must exploit resources in their surroundings in order to survive, so all species are specialized in some way. If their specialized traits are phylogenetically conservative, even distantly related species may serve as competent hosts for a particular pathogen and conversely, multiple pathogens may be capable of infecting novel hosts. The specific receptors necessary for SARS-CoV-2 to live successfully in bats, for example, are broadly distributed among diverse mammalian groups (Gryseels et al., 2020; Hoffmann et al., 2020; Parrish et al., 2008; Parrish & Kawaoka, 2005), making them all potential reservoirs (Damas et al., 2020).
Any change in geographic distribution or ecological structure creates new conditions for pathogens by giving pathogens more opportunities to encounter susceptible hosts, increasing their realized fitness space (Agosta et al., 2010). The route from an original host to one we care about can be circuitous. When a pathogen is exposed to an array of novel hosts, and becomes established in at least one, pathogen variants already present at low levels in the original host may find the new host more to their liking, in which case they will proliferate rapidly and then produce additional variants that are capable of colonizing yet more hosts. This ‘stepping-stone dynamic’ has been predicted to be common (Araujo et al., 2015; Braga et al., 2015; Brooks et al., 2019), and the emergence of severe acute respiratory syndrome coronavirus (SARS-CoV) (Coronaviridae, Sarbecovirus sp.) in 2003, Middle East respiratory syndrome coronavirus (MERS-CoV) (Coronaviridae, Merbacovirus sp.) in 2012 and SARS-CoV-2 in 2019 appears to have been driven by stepping-stone switches (Morens & Fauci, 2020; Rodriguez-Morales et al., 2020).
Emerging infectious disease is more a matter of taking advantage of new opportunities than of evolving new capacities when viewed from the pathogen's perspective. Throughout evolutionary history, pathogens have experienced alternating episodes of geographic expansion and isolation catalysed by climate change events. Host ranges increase during expansion and decrease during isolation. Episodes of climate change are always followed by extended periods of climate stability, marked by the emergence of novel diversity in restricted geographic areas. This links the emerging infectious disease (EID) crisis to the climate change crisis in a surprisingly simple and direct way. Climate change leads to movement, bringing susceptible hosts into contact with pathogens they have never seen before (e.g. Brooks et al., 2019; Hoberg et al., 2012, 2017). This produces oscillations in both host range (Janz & Nylin, 2008; Janz et al., 2006; Nylin et al., 2014) and geographic distributions, so that the emergence of novel diversity in restricted settings sets the stage for geographic and host expansion—disease emergence—each time there is a climate change event (Brooks et al., 2019; Hoberg & Brooks, 2015; Kafle et al., 2020). Audy (1958) glimpsed this when he noted that the geographic distribution of a pathogen is substantially greater than that of disease caused by the pathogen. Emerging diseases are a built-in evolutionary feature of global diversity. We next consider briefly four categories of EID that pertain to food security.
2.1 Crops and crop-related plant pathogens
While food plants are susceptible to a wide range of pathogens, current reviews focus on fungal diseases. Somewhat neglected emerging outbreaks of bacterial plant pathogens also pose a serious challenge to all the macroregions (Table S1). In particular, a group of recently discovered Gram-positive bacteria (phytoplasmas; Mollicutes: Acholeplasmataceae) is disrupting traditional phytosanitary models and established farming systems. Here, we provide an exemplar in the phytoplasmas associated with Flavescence dorée (FD) disease in Europe, currently listed in the EU2000/29 Council Directive on Harmful Organisms and the EPPO A2 quarantine list of pests.
Viticulture and winemaking have a large impact on different socio-economic sectors in many countries. In 2018, the grape and wine industries worldwide registered 77.8 mt of grapes and 292 mhl of wine production (OIV, 2019) and the wine market is projected to grow by 140.2 billion dollars, driven by a compounded growth of 5.5% (ReportLinker, 2020). The largest markets are European, accounting for 45% of world wine-growing areas, 65% of production, 60% of global consumption and 70% of exports (European Commission, 2020).
In Europe, the phylloxera epidemic swept through the grape production and wine trade industries in late 19th century (Tello et al., 2019); they successfully coped with the new pathogen by replacing the indigenous species of Vitis with disease-resistant inter-specific hybrids (This et al., 2006). In the 1950s, another devastating and more elusive pathogen struck European viticulture, emerging initially in south-western France. The pathogen was initially assumed to be an unknown virus, and the associated diseases have been named Grapevine Yellows (GY). In 1967, electron microscopy provided the first evidence of the association of a new pathogen with GY diseases (Doi et al., 1967), as well as with numerous plant diseases worldwide (Bertaccini et al., 2014). The pathogen (phytoplasma) has been classified as a cell wall-less bacterium with small genome sizes (530–1350 kb) belonging to the class Mollicutes, transmitted by sap-feeding hemipteran insect vectors (IRPCM, 2004; Lee et al., 2000; Trivellone, 2019; Weintraub & Beanland, 2006).
The most severe outbreaks in Europe have been associated with FD and FD-related phytoplasmas (for a review see Angelini et al., 2018). An exclusive association between the FD-related genotypes, plant hosts and their insect vectors has been suggested (EFSA, 2014), and the emergence of the first epidemic episodes has been linked to anthropogenic introduction of an exotic leafhopper vector, Scaphoideus titanus Ball 1932 (Cao et al., 2020).
Previous studies showed that FD phytoplasma strains associated with grapevine and indigenous wild plants form a monophyletic group, and some strains occur in both crop and wild plants (Angelini et al., 2003; Filippin et al., 2009). Some authors hypothesized that common indigenous arboreal plants in the wild habitats surrounding vineyards could be the original reservoirs for recently evolved strains associated with grapevines (Angelini et al., 2004; Malembic-Maher et al., 2020). Colonization by wild FD strains to grapevines may have happened at least three times in different geographic areas of Europe (Arnaud et al., 2007), in each case associated with a rapid spread of the efficient insect vector S. titanus.
Possible host range expansions into crop fields might have been caused by expansion to host plants of indigenous vectors associated with European alders (Alnus glutinosa (L.) Gaertn.), which then allowed FD-related (indigenous) genotypes to infect grapevine (Malembic-Maher et al., 2020). Colonization of the exotic vector and novel host plant by pre-existing genotypes set the stage for the rapid emergence of severe epidemic outbreaks in the new plant host (Trivellone & Dietrich, 2020). Analysis of membrane protein interactions among immunodominant membrane protein of an FD phytoplasma strain and membrane proteins of known and potential vectors provided evidence for a continuum in interaction capability with the FD pathogen among phylogenetically unrelated insect species, suggesting that the ecological fitting is phylogenetically constrained in sloppy molecular space (Trivellone et al., 2019).
The first timetree for phytoplasmas supported the theory that the introduction of the exotic vector S. titanus into Europe mediated the rapid diversification of FD wild indigenous strains by colonization events among species of novel hosts (Cao et al., 2020). Based on plant host data, they also revealed a history of acquisition of a new insect vector and shifts in host plants for at least two other biological associations among an assemblage of distantly related phytoplasma strains. Colonization events among their plant and insect hosts appear to have driven rapid phytoplasmas radiation during the last 300my.
2.2 Terrestrial livestock
The emergence of African swine fever virus (ASFV) serves as a powerful exemplar of animal pathogens that directly influence health of production livestock and the role of environmental/ ecological interfaces and reservoirs in patterns of distribution, dissemination and downstream impacts (Hoberg et al., 2008; Wells et al., 2020) (Table S1). Aside from the direct consequences and cumulative costs of disease, production losses, management and mitigation, domestic stock are a significant source of zoonoses (Cleaveland et al., 2001; Wells et al. 2020).
The history of globalization for ASFV involves a stepping-stone dynamic through ecological fitting and repeated and independent events of continental translocation and introduction for an arthropod-borne virus circulating historically among endemic Suidae from east Africa (Sánchez-Vizcaíno et al., 2012). Discovered in the early 1900s, based on emergent devastating disease in domestic swine (Sus scrofa domesticus Erxleben, 1777), ASFV has been shown to circulate in an endemic cycle among warthogs (Phacocoerus africanus (Gmelin, 1788)), bush pig (P. larvatus (Cuvier, 1822)) and soft ticks (species of Ornithodorus Koch, 1837) often associated with burrow systems. Maintenance and persistence of the life cycle in the sub-Sahara are consistent with an ancient association between the virus and largely asymptomatic east African suid reservoir hosts. Opportunity and distribution were expanded by domestic swine husbandry in Africa, and later introduction of farmed domestic stock with ASFV into Spain in 1957 and Portugal in 1960 (Sánchez-Cordón et al., 2018; Sánchez-Vizcaíno et al., 2012). The virus was more broadly introduced in Europe and to South America and the Caribbean region. Geographic islands, representing viral introduction and establishment outside of Africa, were largely eradicated by 1990. ASFV was re-introduced to central and eastern Europe in 2007, where it now circulates among populations of wild boar (Sus scrofa Linnaeus, 1758) and domestic swine across the Transcaucasus region (Russia, Georgia), Ukraine, Poland, Latvia, Lithuania, Estonia, Czech Republic, Hungary and Romania. ASF in domestic swine has also been reported in eastern Russia adjacent to the Mongolian border (Sánchez-Cordón et al., 2018).
African swine fever virus emerged in eastern Asia in 2018, causing considerable socio-economic impact (BBC News, 2019a; FAO, 2019) (Table S1). Disease was initially reported in China during August of that year, followed by rapid geographic expansion across eastern Asia where currently 10 countries report infected swine (Mason-D’Croz et al., 2020). Populations of swine from all mainland provinces of China were involved, leading to culling of millions of swine in an attempt to limit infection. The massive decline in production was accompanied by increases in pork prices ranging from 17% to 85% (Santorelli, 2019; Tian & von Cramon-Taubadel, 2020). As the impact of a shortage of pork products unfolded, consumers shifted to cheaper or alternative food sources including wildlife species. That in turn drove overall increases in food costs and heightened insecurity. Similar dietary shifts may also lead to food insecurity in regions such as sub-Saharan Africa (Mason-D’Croz et al., 2020; Tian & von Cramon-Taubadel, 2020).
ASFV outside of Africa is transmitted primarily among wild boar, feral swine and domestic swine, apparently with minimal amplification through tick vectors. Although arthropod vectors remain important in Africa and the virus can survive for extended periods up to 5 years in Ornithodorus ticks representing an assemblage of species (Oleaga-Pérez et al., 1990), direct transmission is more significant globally. Dissemination involves contaminated meat and meat products, food waste, and with anthropogenic movement and natural dispersal of infected hosts. For example, ASFV was documented in wild boar from the demilitarized zone (DMZ) separating North and South Korea, highlighting the role of wildland habitats in harbouring infected reservoirs for dissemination to domestic swine (BBC News, 2019b). It is currently postulated that ASFV arrived across the buffer region of the DMZ despite attempts for exclusion of boars using a system of fencing. Failures in biosecurity protocols were also implicated in spread, and a stepping-stone pathway for a highly pathogenic strain of ASFV. Food waste from a South African ship was fed to domestic swine in Georgia in 2007. An initial introduction and establishment of infections in domestic pigs led to subsequent expansion into wild boar populations across the Transcaucasus region (Sánchez-Vizcaino et al., 2012).
The primary risk space outside Africa is defined by the presence of wild boar and feral pigs and potential interfaces with domestic swine exacerbated by illegal trade, contaminated vehicles and associated fomites. There is potential for widespread introduction globally to Australia and the Western Hemisphere due to inadequate control measures (Sánchez-Cordón et al., 2018; USDA, 2020). There are no current interventions based on therapeutics or vaccines, so attempts to control emergence, dissemination or disease depend on culling and quarantine. The continuing emergence of ASF, with minimal suppression, directly influences supply and demand for food resources and is a threat multiplier contributing directly to food insecurity. More generally, outbreaks of livestock disease have led to reduced demand due to loss of trust in food quality and commodity safety (Mason-D’Croz et al., 2020; Tian & von Cramon-Taubadel, 2020).
2.3 Aquatic food systems
The detection and study of diseases associated with marine species, even those of economic interest, are inherently difficult. Despite that understanding, an increase in the incidence of new infirmities has been cumulatively reported in the recent years (Lafferty et al., 2004), including fish and shellfish (Hoenig et al., 2017; Walker & Winton, 2010) and members of other groups such as corals, echinoderms and marine mammals (Baskin, 2006; Groner et al., 2016; Harvell, 2019; Sweet & Bateman, 2015; Tracy et al., 2019). With the expansion of aquaculture, however, the contemporary emergence of diseases in cultured aquatic organisms has become more evident (Murray & Peeler, 2005; Sweet & Bateman, 2015; Tracy et al., 2019). Reduction in seafood production (Stentiford et al., 2012) and associated economic (Ganjoor, 2015; Lafferty et al., 2015; Tavares-Dias & Martins, 2017) and social losses (Vicente et al., 2018; Walker & Winton, 2010) have been reported from both marine and freshwater environments (Table S1). Many emergence events are associated with climate change (Baker-Austin et al., 2013; Burge et al., 2014; Harvell et al., 1999; Mueter et al., 2011; Paz et al., 2007), directly (Ford & Chintala, 2006; Staehli et al., 2009), including altered distributions of hosts or vectors. Emergence and re-emergence of infectious diseases in important seafood resources along with the predicted reduction in the ocean's productivity (Behrenfeld et al., 2006), and human-based geographic expansion of aquaculture (De Silva & Soto, 2009) are expected to combine to hinder future yields of food production in aquatic environments.
The mangrove land crab (Ucides cordatus (L.)) represents the most important among the few marine resources available to be exploited by the economically hampered population in the coast of Brazil, especially in the Northeast (Glaser, 2003). To collect from 10 to 15 large bags of crabs a day, fishermen only need their hands to dig into the burrows and capture enough crabs that can provide minimum sustainability for their families. In north-eastern Brazil, U. cordatus is a particularly important resource for the local population and tourism (CEPENE, 1999) and it is the foundation for the most important commercial activity in mangroves across the region (Castilho-Westphal et al., 2008). The annual production of the mangrove land crab was estimated to be greater than 8,912 tons during the 1980s and 1990s (Castilho-Westphal et al., 2008).
Extensive mortality of populations of the mangrove land crab dates from 1997 in a locality known as Goiana, close to the city of Recife, Brazil (Vicente et al., 2018). As far as we know, the epidemics spread from there to both northern and southern mangroves, reaching 8 of the 17 coastal states in Brazil and app. 3,500 km of coastline. The dispersion of the epidemics occurred as multiple waves (Ferreira et al., 2009) reaching estuaries farther from Goiana each year. Mangroves in the states of Paraíba and Bahia reported reductions in crab yields of 84 and 97.6%, respectively (da Nóbrega Alves & Kioharu Nishida, 2003), causing severe socio-economic problems in the affected regions.
While recognized as an epidemic, it was only 8 years later that the putative causative agent of the lethargic crab disease (LCD) was proposed (Boeger et al., 2005). While two species of black yeasts have been detected in diseased crabs (Vicente et al., 2012), Exophiala cancerae de Hoog, Vicente, Najafzadeh, Badali, Seyedmousavi & Boeger, 2005 was present in the crab's system in every event of mortality studied. Confirmation of the causative agent of LCD was reported only after experimental challenges of U. cordatus to injections containing spores of E. cancerae in the laboratory (Orélis-Ribeiro et al., 2011).
The epidemics spread to north and southern mangroves but did not reach every mangrove in coastal of Brazil. The southernmost limit were mangroves in the state of Espirito Santo—with records extending from 2006 and with unconfirmed records of mortalities up to 2016—while the northern limit of records of mortalities caused by LCD were the mangroves of the State of Piauí (Vicente et al., 2018). Oceanographic conditions, such as elevated salinity and temperature of the water in the northern limit and the reduction in density of mangroves in the areas southern to the southernmost limit appear to have influenced the geographic extent of the epidemic (Orélis-Ribeiro et al., 2017).
The origin of E. cancerae in the Brazilian mangroves and the total socio-economic cost of the LCD are yet unknown. The disease generated no interest from the Brazilian federal or state governments, except for the smallest state of the country, Sergipe, which funded the project that revealed many important aspects of the epidemics. That same species, however, was detected previously from different countries (Europe, Australia) and substrates, including human samples, drinking water, amphibians and fruit juice and thus appears considerably widespread (de Hoog et al., 2011).
During 1997–2006, however, the daily catch per crab harvesters was reduced to 1 bag/day; in most cases, the crabs died in the way to the market. The species is always commercialized alive, so crab harvesters suffered an immense reduction in their income during the period and many had to accept underpaid salaries in the more formal fishery industry, mostly artisanal (Vicente et al., 2018). Crab stocks have apparently recovered to the pre-epidemic population levels, for the time being. During the period of the epidemics, however, crab harvesters did not receive any social nor economic support from governmental agencies since the disease was not recognized by most of them, at municipal, state or federal levels.
2.4 Food-borne pathogens of humans
Food-borne human pathogens and zoonoses constitute another threat multiplier for food security, costing billions of dollars in morbidity and mortality (Robertson et al., 2013, 2014) (Table S1). The emergence of SARS-CoV-2 provides a real-time exemplar of that phenomenon.
SARS-CoV-2 is a member of a large group of viral pathogens, the coronaviruses, that occur in bats and a diverse assemblage of mammalian taxa and species beyond Chiroptera (Calderon et al., 2016; Damas et al., 2020; Fan et al., 2019; Gryseels et al., 2020; Hu et al., 2017; Joffrin et al., 2018; Kemenesi et al., 2014; Xie & Chen, 2020; Zheng et al., 2019; Zhou et al., 2020). Direct infection of humans from non-human hosts appears infrequent, but there are numerous stepping-stone pathways through food chains linking wild infected mammals and people, potentially facilitating exposure and transmission (Araujo et al., 2015; Hoberg & Brooks, 2015; Kemenesi et al., 2014). An interface and pathway emerged through densely populated open-air markets maintaining considerable diversity of exotic wildlife species consumed as food (Lee et al., 2020; Staits Times, 2020; Xie & Chen, 2020). Such wet markets link wildlands and urban centres, becoming pathways for interspecies circulation and emergence of pathogens (Agosta et al., 2010; Cleaveland et al., 2001; Morens & Fauci, 2020).
Colonization from humans through companion and farmed animals (e.g, domestic cats, dogs, mustelids such as ferrets and farmed mink) has the real potential to introduce this global virus into populations of free-ranging carnivores and other mammals. Further, infection and cross-transmission between people and synanthropic mammalian hosts such as domesticated mink by SARS-CoV-2 has now been recognized and may serve as the source for focal islands of infection (Briggs, 2020; Gryseels et al., 2020; Santini & Edwards, 2020; Staff, 2020). Of significance is a process of infection that relies on the widespread distribution of appropriate and evolutionarily conserved pulmonary receptors in mammals which constitutes the capacity (ecological fitting in sloppy fitness space) by coronaviruses for host colonization. Selection and mutation, once infection is established in mammalian hosts, can alter future dynamics for disease as predicted by the Stockholm Paradigm as initially observed among infections established in European domesticated mink and people, and the origins of 3 recently emergent variants with high transmissibility in the United Kingdom, South Africa and Japan that are under rapid dissemination globally (WHO, 2021). Transmission pathways emerging across urban to rural centres and sources, in the context of expanding host range and ecological fitting, represent the interface for viral capacity and environmental opportunity (Agosta et al., 2010; Araujo et al., 2015; Brooks et al., 2019; Damas et al., 2020; Gibb et al., 2020; Gryseels et al., 2020).
3 PATHOGENS AND FOOD INSECURITY, A CONVERGENT CRISIS
Famine, especially in the developing world of Africa and Asia, has accompanied major emergences of viral (e.g. Ebola virus, highly pathogenic avian influenzas) and bacterial (e.g. Cholera, Plague) pathogens (Table S1). Such agents of human diseases exacerbate already challenging circumstances for food production and distribution that are a consequence of climate warming, altered patterns of precipitation, aridification, drought, environmental disruption and changing patterns of land use on regional and global scales (Brooks et al., 2019; Daszak et al., 2020; Robbins, 2020; Scheelbeek et al., 2020). Limited infrastructure in developing regions of the world must be continually reallocated to address emergent disease, leading to disrupted food distribution. In more affluent regions, economic continuity has been dramatically impaired by pervasive impacts for global food production and supply chains, with cumulative costs now exceeding trillions of dollars.
The coronavirus disease 2019 (COVID-19) pandemic caused by SARS-CoV-2 has driven a spike in global food costs and disruption of supply chains that will be especially devastating in the developing world (Benton, 2020; Laborde et al., 2020; Reinhart & Subbaraman, 2019; FAO, 2020). For example, in regions of Africa, Asia and South America resources of 40%–60% of household income and resources are expended in acquisition of food, representing 5–6 times the costs in developed countries. China had already experienced an increase of 15%–22% in consumer costs for pork due to ASFV infections in 2019. Rising food prices and food scarcity further exacerbate food security leading to increasing consumption of bushmeat and broadening reliance on the wildlife trade (legal and illegal). Supply chains, for human consumption emanating from wildlife, can be associated with amplification of pathogens, with changing patterns of diversity and occurrence and distribution of disease. For example, in Vietnam, a 10-factor increase in detection of coronavirus in bamboo rats, from the field to the restaurants, was considered an indicator of a broadening threat for spillovers (see Daszak et al., 2020 and references within). The locust blight across East Africa in 2019 increased the costs of maize by 60% in 2019 (George, 2020). This is a vivid example of the way the emerging disease crisis creates global socio-economic impact (Garrett, 1994; Quammen, 2020). ‘COVID-19 is amplifying the risk of a worldwide food price spike, which would trigger crises in many developing countries’ (Laborde et al., 2020; Reinhart & Subbaraman, 2020; UNSCN, 2020).
Technological innovations revolutionized food production in the past century. During that time, we assumed this growing technological expertise would limit or resolve issues associated with infectious disease. As a consequence, humanity is now surprised to be experiencing accumulating emerging infectious disease challenges to our food resources and security. That surprise arises from a fundamental misunderstanding about the nature of pathogen–host associations. Twentieth-century explanations have been dominated by evolutionary concepts leading us to think that infectious disease emergence would be rare and unpredictable. Colonization of novel animal or plant hosts was thought to require the evolution of new capacities—or special mutations—in order for diverse pathogens to exploit a broader range of potential hosts (see Brooks et al., 2019 for a summary). Pathogens, however, are finding us and the plants and animals upon which we rely far more often than traditional models predicted.
The Stockholm Paradigm (Brooks et al., 2014) contrasts with the prevailing paradigm in a way that explains the risk posed by emerging infectious diseases. Emerging infectious diseases occur when pathogens come into contact with hosts that are compatible but have never been exposed and have never had the opportunity to evolve resistance. Infectious disease can emerge rapidly whenever changing conditions lead to new opportunities without the need for novel genetic capacities to evolve. And we live in a world of changing conditions which maximizes ecological interfaces and opportunities of encounter among species and species assemblages. Some pathogens kill large numbers of humans, by infecting them or by killing their food sources. Most reduce human productivity and agricultural production, increasing costs associated with public and agricultural health. The socio-economic impact of these latter pathogens is staggering. The planet is a minefield of evolutionary accidents waiting to happen (Brooks & Ferrao, 2005)—and they are happening daily.
Anthropogenic activities are a major source of environmental change increasing the opportunities for pathogens to encounter compatible hosts (Hoberg et al., 2010). Global climate change is the primary driver of shifting environments and disruption of habitats across spatial and temporal scales, altering conditions within particular places and connections across landscapes and regions (e.g. Kafle et al., 2020). Climate warming is the ultimate driver and in synergy with habitat perturbation, changing land use and biodiversity loss are the source of overlapping crises for the biosphere creating novel interfaces where pathogens can be shared among humans, crops and livestock, and assemblages of wild animals (Brooks & Hoberg, 2013; Daszak et al., 2020; Dobson et al., 2020; Gibb et al., 2020). For humans and livestock, movement across ecotones, such as incursion into new habitats, or adoption of new behaviours or management practices alters patterns of ecological interactions that have historically restricted pathogens to a limited number of hosts. Globalized trade and travel changed a slow and large world into one that is small and fast. Humans, the plant and animals they rely on, and species who hitch a ride with them, have been spread farther and faster than ever before. This increases the number of opportunities for pathogens to encounter compatible hosts. Finally, the global spread of human civilization, either by intention or displacement, has been accompanied by increasing urbanization.
More than 50% of humans now reside in cities and that percentage is projected rise to 70% by 2050 (United Nations, 2019). Technologically advanced cities should be able to offset the risk of new pathogens being introduced as a result of trade, travel and migration by detecting incoming pathogens at their point of entry. In theory, yes. But programmes of inspection and quarantines cost time, money, and human resources and slow the flow of goods. Urbanized humanity is highly vulnerable to emerging infectious disease outbreaks. Cities pose challenges: (a) as incubators for many pathogens and their vectors and as insular environments often warmer than 3°C relative to peri-urban areas; (b) are totally dependent on a constant flow of materials, including water and food, from outside sources, increasing the chances for pathogen introduction; (c) support a focal interface for a large number of species of that are themselves vectors or reservoirs of diseases affecting people and their companion animals, particularly in urban green spaces and areas where food supplies and wastes concentrate (Földvári et al., 2011, 2014; Kurucz et al., 2018, 2019; Szerkes et al., 2019); (d) represent high-density concentrations of people, meaning that in any disease outbreak the chances of exposure are elevated in proportion to the number of people living in the city; (e) exhibit extreme division of labour and extreme inter-dependency, meaning that there is little redundancy in the workforce to maintain food security in case of disease outbreak; and (f) include residents who are poorly educated, poorly nourished and poorly paid people, often working in jobs related to food distribution and production, they are often invisible to the public health and social services networks, and cannot afford to stay at home when they are ill.
4 PROACTIVE POLICY: THE DAMA PROTOCOL
Infectious diseases will continue to emerge so long as climate change perturbations continue, and these will continue indefinitely. We must adopt policies that buy time and lower costs, so humanity can cope with a future characterized by a complex mosaic of hosts, geography, pathogens and disease. Humanity can and must anticipate and mitigate the effects of these EID. The Stockholm Paradigm provides hope for a pathway to effectively anticipate and mitigate emerging infectious diseases. Evolutionarily and ecologically conserved capacities that allow pathogens to persist in one place, or among a particular spectrum of hosts, allow us to predict how they will behave in novel conditions. We can anticipate their arrival and their behaviour if they become established in new geographic areas/hosts. In a proactive mode, we must ‘find them before they find us’.
Many countries recognize the magnitude of the EID crisis, but coping with emerging infectious disease has been largely in the form of crisis-response measures. The DAMA protocol (Document–Assess–Monitor–Act) (Brooks et al., 2014, 2019; Hoberg et al., 2015) adds a preventive dimension to those efforts, aimed at extending human and material resources devoted to coping with the wave of emerging diseases. The DAMA protocol combines efforts ranging from ‘boots on the ground’ contributions of citizen scientists working with field biologists to sophisticated archival repositories, bioinformatics, molecular biology and satellite surveillance. Its focus is anticipating emerging diseases on the basis of knowing what pathogens are present in the environment before these become a problem, then taking steps to diminish the risk space and to mitigate the impact of their emergence.
DAMA begins with Documenting pathogens actually or potentially residing in each location studied. We can cope with potentially emergent pathogens only when we know who they are, where they occur, the dynamics by which they are transmitted and who they can infect. We do not have the time or human capacity to document every pathogen in every host everywhere on the planet, and we do not need to try. DAMA, however, does provide the connectivity and context for understanding the relationship that pathogens have within the biosphere. Most pathogens reside in at least one host species that is not diseased, called reservoir hosts. Reservoirs are often known or suspected, allowing us to focus on a manageable subset of the species of plants and animals living in an area of interest. Reservoirs become important when they occur in habitats adjacent to places where humans, their crops and their livestock live. It is in these habitat interfaces that disease transmission occurs. And finally, the means by which disease-causing agents are transmitted from host to host are highly specific for each pathogen; some are transmitted in food, some in water, some by contact between infected hosts or surfaces that have been in contact with infected hosts. Vectors, such as mosquitoes, ticks and leafhoppers transmit many pathogens of animals and plants. We can be efficient about documenting potential emergent pathogens, but the scope of the problem still requires the cooperation of people living in the areas at risk, who represent an immense storehouse of traditional ecological and local knowledge (Brook et al., 2009; Kutz et al., 2009; Tomaselli et al., 2018). Participating scientists need to expend significant time and energy talking with people at the grassroots, obtaining their trust and cooperation. Discovery is effective only in the context of archival repositories for specimens and information that are the cumulative historical baselines describing pathogen distribution (McLean et al., 2019; Schindel & Cook, 2018).
The next stage is Assessing the relative importance of pathogens encountered in documentation activities. By applying what we know about the evolutionary history (phylogeny) of each species we find, we can quickly ask if the species or its relatives are known to cause disease in another place—this is called phylogenetic triage. Species that are assessed as being of potential threat(s) are targeted for special attention. All other specimens are archived for future reference in the event that new information may implicate these assemblages of hosts and pathogens with disease (Dunnum et al., 2017). Our process is built on strategic sampling with the understanding that considerable knowledge of the global biosphere remains to be revealed, especially the diverse assemblage of pathogens that circulate among animals and plants.
Potentially threatening pathogens must be Monitored in order to know when we require action to mitigate their impact or to make their arrivals less certain. We are looking for changes—in geographic distribution, in host range, in transmission dynamics and life history, in geographic variation, in patterns of occurrence and behaviour, and early signs of arrival of anticipated pathogens. Collaboration with local stakeholders is vitally important in this phase. Many cell phone-based applications have been developed—and more are coming—for real-time reporting of information from the grassroots to community, government and academic centres to facilitate rapid assessment and dissemination of knowledge from ongoing changes at the interface of hosts, pathogens and geography.
Finally, information about pathogen threats emerging from monitoring pathogens of special interest must be turned into effective Action, as rapidly as possible. Such information has too seldom been converted into concrete action. For example, a coronavirus highly similar to SARS-CoV-2 was documented in bats from a cave in Yunnan Province, China, more than 15 years ago (Cyranowski, 2017; Li et al., 2005; Poon et al., 2005) and the potential for it to cause disease in humans was assessed shortly thereafter (Cheng et al., 2007). Subsequently, no actions were taken to monitor the virus or mitigate its potential contact with food animals and secondarily, via the stepping stones, to humans.
5 CONCLUSIONS
Emerging infectious diseases are a growing threat to global food security. Direct impacts are attributable to disease, morbidity and mortality in production and wildland food animal systems that determine availability and stability of food resources (WHO, 2020). Costs of mitigation, intervention, pathways for control and eradication and limits on cross-border commerce are additive or multiplying impacts (Table S1). Direct pathways are linked to zoonoses and circulation of pathogens across interfaces for wildlands, managed agricultural systems and urban environments that influence suitability and safety of food resources from terrestrial, aquatic and marine environments (Jenkins et al., 2013; Robertson et al., 2013, 2014). Indirect pathways include emerging diseases in human populations that influence stability and continuity of production, harvesting, processing, dissemination and food resource supply chains (Laborde et al., 2020). Rapidly increasing treatment costs and production losses associated with crisis response policies no longer can be sustainably passed on to consumers as the cost of doing business.
How we choose to anticipate and mitigate emerging infectious diseases is directly influenced by perceptions of urgency and opportunities for funding. Not surprisingly, research that has a focus on pathogens in food animals and crops reflects the immediacy of priorities established by agencies at national to regional levels. Research trajectories, although initially driven by short-term events such as responses to emerging infectious disease attributed to varying classes of pathogens, dominate the funding arena over 8- to 10-year cycles (Ducrot et al., 2016). Such decisions and oscillations in funding dampen or impede long-term, comprehensive and strategic planning and directly exacerbate potential gaps in knowledge with respect to a broad-based science infrastructure. In a resource-limited arena, rapid shifts in short-term resource allocation for pathogens and diseases can drive loss of skills, special knowledge and significant institutional memory. These strategic shortcomings contribute to the crisis response mode that characterizes emerging disease policies and research funding. They represent a business as usual mindset in the broader science community, at a time when our activities and focus must transcend a series of short-term and poorly coordinated approaches.
Given the state of the planet and our influence on it, it is a certainty that there will be a continuing parade of emerging and persisting pathogens. DAMA, therefore, cannot be an afterthought in our policies about emerging disease and food security, if colonization of a new host requires new opportunities given specific pre-existing capacities. Those pre-existing capacities are predictable, allowing us to anticipate disease emergence. Once a pathogen becomes established in a new host as a result of predictable pre-existing capacities, new capacities may emerge that are not predictable. When that occurs, unsustainably expensive crisis response becomes our only option. The DAMA protocol is analogous to changing from a siege mentality to a mentality of taking the fight to the enemy. In the large, slow world of 1918, deaths from disease were the biggest concern. In today's small, fast world, loss of productivity due to disease may be even more significant as death in socio-economic terms. A pathogen can be disseminated globally on time scales of days, if not hours. Each new EID exacts a cost and persists as pathogen pollution after its initial acute outbreak, always having the potential to break out anew.
We need to adopt a proactive capacity and an ethos of prevention to cope with the EID threat to global food security. We must initiate DAMA programmes now, even as the SARS-CoV-2 pandemic continues and ongoing outbreaks of wheat stem rust fungus, African swine fever and avian influenza threaten food production throughout Europe and beyond. SARS-CoV-2 will persist globally as an element of pathogen pollution, although no longer among the array of unknown and potential disease agents. DAMA requires that we use our resources and insights about the biosphere and biodiversity to strategically and selectively document and understand the connectivity for pathogens on a global stage. A cornerstone for all successful DAMA programmes is revitalizing and augmenting archival capacities (specimen-based collections) and associated informatics services (baselines) that describe the biosphere, concurrent with a broadened context and renewed emphasis on natural history translated from the local level to the policy arena.
Implementing the DAMA protocol will be expensive, but projected costs of the interminable cycles of emergence, reaction and response are unsustainable (McLean et al., 2019; Schindel & Cook, 2018). Not implementing the DAMA protocol, however, will be catastrophic. The global meltdown caused by the SARS-CoV-2 pandemic is the cost of not adopting the DAMA protocol. The challenge of adapting to a world in which global climate change is a real and long-lasting phenomenon requires long-term commitment to changes in human capacity, behaviour and infrastructure. These actions must be permanent societal investments in new forms of communication, education, scientific research and clinical practices.
ACKNOWLEDGEMENTS
DRB thanks the organizers of the joint US National Academy of Science and UK Royal Society Forum on Sustainable Agriculture and Food Production convened in Washington, D. C., during early March 2020 for the invitation to participate in the forum. Our current exploration of EID and food security emerged from this forum. VT warmly thanks Dr. Christopher Dietrich, Dr. Brenda Molano Flores and the Illinois Natural History Survey (University of Illinois) to continue offering the opportunity to review and discuss this issue of globally emerging relevance with the hope to stimulate the interest of younger researchers and in investing more funds on the evolution of plant–insect–pathogen interactions in natural and managed systems.
CONFLICT OF INTEREST
The authors have no conflicts of interest to declare.
AUTHORS’ CONTRIBUTIONS
All contributed equally; sequence of authors agreed upon mutually.
ETHICAL STATEMENT
The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to. No ethical approval was required as this is a review article with no original research data.
