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Synthesizing the connections between environmental disturbances and zoonotic spillover

JOEL HENRIQUE ELLWANGER PHILIP MARTIN FEARNSIDE MARINA ZILIOTTO JACQUELINE MARÍA VALVERDE-VILLEGAS ANA BEATRIZ G. DA VEIGA GUSTAVO F. VIEIRA EVELISE BACH JÁDER C. CARDOSO NÍCOLAS FELIPE D. MÜLLER GABRIEL LOPES LÍLIAN CAESAR BRUNA KULMANN-LEAL VALÉRIA L. KAMINSKI ETIELE S. SILVEIRA FERNANDO R. SPILKI MATHEUS N. WEBER SABRINA E. DE MATOS ALMEIDA VANUSA P. DA HORA JOSÉ ARTUR B. CHIES About the authors

Abstract

Zoonotic spillover is a phenomenon characterized by the transfer of pathogens between different animal species. Most human emerging infectious diseases originate from non-human animals, and human-related environmental disturbances are the driving forces of the emergence of new human pathogens. Synthesizing the sequence of basic events involved in the emergence of new human pathogens is important for guiding the understanding, identification, and description of key aspects of human activities that can be changed to prevent new outbreaks, epidemics, and pandemics. This review synthesizes the connections between environmental disturbances and increased risk of spillover events based on the One Health perspective. Anthropogenic disturbances in the environment (e.g., deforestation, habitat fragmentation, biodiversity loss, wildlife exploitation) lead to changes in ecological niches, reduction of the dilution effect, increased contact between humans and other animals, changes in the incidence and load of pathogens in animal populations, and alterations in the abiotic factors of landscapes. These phenomena can increase the risk of spillover events and, potentially, facilitate new infectious disease outbreaks. Using Brazil as a study model, this review brings a discussion concerning anthropogenic activities in the Amazon region and their potential impacts on spillover risk and spread of emerging diseases in this region.

Key words
Amazon Forest; biodiversity; disease ecology; outbreak; spillover; zoonosis

INTRODUCTION

A robust set of evidence shows that conservation of biodiversity and of balance in ecosystems and food webs reduces the risk of emergence and spread of infectious diseases of zoonotic origin, in addition to contributing to human well-being in general (Ostfeld 2009OSTFELD RS. 2009. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect 15: 40-43., Keesing et al. 2010KEESING F ET AL. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647-652., Pecl et al. 2017PECL GT ET AL. 2017. Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355: eaai9214., IPBES 2020). From a practical point of view, limiting anthropogenic activity in environments with high abundance and diversity of species contributes to the maintenance of human and environmental health, containing emerging infectious diseases by multiple ecological mechanisms. On the other hand, anthropogenic disturbances (e.g., deforestation, habitat fragmentation, intensive agricultural practices, unplanned urbanization) indeed affect this balance, facilitating the emergence of new pathogens and the spread of diseases (Ellwanger et al. 2020ELLWANGER JH ET AL. 2020. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc 92: e20191375., IPBES 2020). On a global scale, land-use change was the major driver of more than 30% of new emerging infectious-disease events since 1960 (IPBES 2020IPBES - WORKSHOP REPORT ON BIODIVERSITY AND PANDEMICS OF THE INTERGOVERNMENTAL PLATFORM ON BIODIVERSITY AND ECOSYSTEM SERVICES. DASZAK P ET AL. 2020. IPBES secretariat, Bonn, Germany. doi: 10.5281/zenodo.4147317.).

Currently, there are more than 7.7 billion humans on Earth. Projections indicate that the world population will reach 9.4 to 10.2 billion people by 2050 (Boretti & Rosa 2019BORETTI A & ROSA L. 2019. Reassessing the projections of the World Water Development Report. npj Clean Water 2: 15.). Economic, political, social, and cultural factors dictate human activities in the natural environment, many of which cause damage and disturbances to the environment and to animal populations. The food, water, and consumption demands of the global population are putting great pressure on nature and triggering a range of environmental problems, with expected exacerbation of this scenario in the near future due to the growing world population (Conijn et al. 2018CONIJN JG, BINDRABAN PS, SCHRÖDER JJ & JONGSCHAAP REE. 2018. Can our global food system meet food demand within planetary boundaries? Agric Ecosyst Environ 251: 244-256., Boretti & Rosa 2019BORETTI A & ROSA L. 2019. Reassessing the projections of the World Water Development Report. npj Clean Water 2: 15., Pastor et al. 2019PASTOR AV, PALAZZO A, HAVLIK P, BIEMANS H, WADA Y, OBERSTEINER M, KABAT P & LUDWIG F. 2019. The global nexus of food-trade-water sustaining environmental flows by 2050. Nat Sustain 2: 499-507.).

The connections between environmental disturbances and infectious diseases are increasingly worrying because efforts to contain deforestation, climate change, and other environmental impacts are still very modest. Globally, habitat loss and extinction rates are on the rise (Ceballos et al. 2015CEBALLOS G, EHRLICH PR, BARNOSKY AD, GARCÍA A, PRINGLE RM & PALMER TM. 2015. Accelerated modern human-induced species losses: Entering the sixth mass extinction. Sci Adv 1: e1400253., Newbold et al. 2016NEWBOLD T ET AL. 2016. Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science 353: 288-291., Powers & Jetz 2019POWERS RP & JETZ W. 2019. Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nature Clim Change 9: 323-329.), and the detrimental effects of climate change on the human population and other species are increasingly evident (Beyer et al. 2021BEYER RM, MANICA A & MORA C. 2021. Shifts in global bat diversity suggest a possible role of climate change in the emergence of SARS-CoV-1 and SARS-CoV-2. Sci Total Environ 767: 145413., Ma & Yuan 2021MA F & YUAN X. 2021. Impact of climate and population changes on the increasing exposure to summertime compound hot extremes. Sci Total Environ 772: 145004.). Concomitant with this scenario of environmental neglect, the number of emerging infectious disease events per decade is increasing (Jones et al. 2008JONES KE, PATEL NG, LEVY MA, STOREYGARD A, BALK D, GITTLEMAN JL & DASZAK P. 2008. Global trends in emerging infectious diseases. Nature 451: 990-993.). Table I shows several examples of infectious disease outbreaks associated with anthropogenic pressures on the environment and animal populations. Also, the economic impacts and losses of human lives related to Coronavirus Disease 19 (COVID-19), which is a zoonotic disease, make clear the magnitude and severity of the situation and the need to understand how to reduce the risks of new pandemics (Dobson et al. 2020DOBSON AP ET AL. 2020. Ecology and economics for pandemic prevention. Science 369: 379-381., Holmes et al. 2021HOLMES EC ET AL. 2021. The origins of SARS-CoV-2: A critical review. Cell 184: 4848-4856.). As of February 2, 2022, COVID-19 had caused more than 381 million infection cases and 5,688,009 deaths worldwide (Dong et al. 2020DONG E, DU H & GARDNER L. 2020. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis 20: 533-534., Johns Hopkins University 2022JOHNS HOPKINS UNIVERSITY. 2022. COVID-19 DASHBOARD BY THE CENTER FOR SYSTEMS SCIENCE AND ENGINEERING (CSSE) AT JOHNS HOPKINS UNIVERSITY. Available at: https://coronavirus.jhu.edu/map.html. Accessed on February 2, 2022.
https://coronavirus.jhu.edu/map.html...
). It is increasingly clear that when a pathogen emerges in a given human population after an event of zoonotic spillover, even in a remote location, the pathogen can quickly spread globally by international air travel and other transport systems, especially in situations of high connectivity between remote regions and large urban centers.

Table I
Examples of connections among human-related environmental disturbance, animal populations and infectious diseases.

Zoonotic spillover is a phenomenon characterized by the transfer of pathogens between different species (usually non-human animals to humans), which may result in new infectious diseases if biological and demographic conditions are conducive to the adaptation of the pathogen in the new species population. Spillover events are among the initial steps towards the emergence of new human infectious diseases, outbreaks, and epidemics (Plowright et al. 2017PLOWRIGHT RK, PARRISH CR, MCCALLUM H, HUDSON PJ, KO AI, GRAHAM AL & LLOYD-SMITH JO. 2017. Pathways to zoonotic spillover. Nat Rev Microbiol 15: 502-510., Ellwanger et al. 2019ELLWANGER JH, KAMINSKI VL & CHIES JAB. 2019. Emerging infectious disease prevention: Where should we invest our resources and efforts? J Infect Public Health 12: 313-316.). Most of the pathogens (~60%) that affect humans are derived from microbial strains that previously circulated only in non-human animals (Jones et al. 2008JONES KE, PATEL NG, LEVY MA, STOREYGARD A, BALK D, GITTLEMAN JL & DASZAK P. 2008. Global trends in emerging infectious diseases. Nature 451: 990-993.), such as HIV (Keele et al. 2006KEELE BF ET AL. 2006. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313: 523-526.), influenza A viruses (Krammer et al. 2018KRAMMER F ET AL. 2018. Influenza. Nat Rev Dis Primers 4: 3.), Zika virus (Wikan & Smith 2016WIKAN N & SMITH DR. 2016. Zika virus: History of a newly emerging arbovirus. Lancet Infect Dis 16: e119-e126.), Ebola virus (Leroy et al. 2005LEROY EM, KUMULUNGUI B, POURRUT X, ROUQUET P, HASSANIN A, YABA P, DÉLICAT A, PAWESKA JT, GONZALEZ JP & SWANEPOEL R. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438: 575-576., Saéz et al. 2015SAÉZ AM ET AL. 2015. Investigating the zoonotic origin of the West African Ebola epidemic. EMBO Mol Med 7: 17-23.), rubella virus (Bennett et al. 2020BENNETT AJ ET AL. 2020. Relatives of rubella virus in diverse mammals. Nature 586: 424-428.), Echinococcus multilocularis, Trypanosoma cruzi (Thompson 2013THOMPSON RC. 2013. Parasite zoonoses and wildlife: One Health, spillover and human activity. Int J Parasitol 43: 1079-1088.), hepatitis B virus (Rasche et al. 2016RASCHE A, SOUZA BFCD & DREXLER JF. 2016. Bat hepadnaviruses and the origins of primate hepatitis B viruses. Curr Opin Virol 16: 86-94.), MERS-CoV, SARS-CoV (Cui et al. 2019CUI J, LI F & SHI ZL. 2019. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 17: 181-192.) and SARS-CoV-2 (Andersen et al. 2020ANDERSEN KG, RAMBAUT A, LIPKIN WI, HOLMES EC & GARRY RF. 2020. The proximal origin of SARS-CoV-2. Nat Med 26: 450-452.), among many others (Montgomery & Macdonald 2020MONTGOMERY RA & MACDONALD DW. 2020. COVID-19, health, conservation, and shared wellbeing: details matter. Trends Ecol Evol 35: 748-750.). Considering adenoviruses, phylogenetic analyses indicate that at least 16 B-type human adenoviruses (HAdV) had their original reservoir in great apes, some of them causing severe human disease. Also, it was proposed that the HAdV-B76 strain, which is associated with a human fatality in 1965, arose from recombination of a virus that infected humans, chimpanzees, and bonobos (Hoppe et al. 2015HOPPE E ET AL. 2015. Multiple cross-species transmission events of human adenoviruses (HAdV) during hominine evolution. Mol Biol Evol 32: 2072-2084., Dehghan et al. 2019DEHGHAN S, SETO J, LIU EB, ISMAIL AM, MADUPU R, HEIM A, JONES MS, DYER DW, CHODOSH J & SETO D. 2019. A zoonotic adenoviral human pathogen emerged through genomic recombination among human and nonhuman simian hosts. J Virol 93: e00564-19., Kremer 2021KREMER EJ. 2021. What is the risk of a deadly adenovirus pandemic? PLoS Pathog 17: e1009814.).

In this article, the expression ‘zoonotic spillover’ will be used to refer to the introduction of a pathogen into the human population from a different animal species. However, it is essential to emphasize that spillover is a complex phenomenon. There are different pathways of spillover events. For example, a pathogen can be transmitted from one species (source host) to another (recipient host) directly, without an intermediate species. Alternatively, some spillover events involve an intermediate species (intermediary host) that acts as a ‘bridge’ for the transmission of the pathogen between the source host and the recipient host. The intermediary host can be a vertebrate species or an invertebrate animal (e.g., mosquito, tick). More than one intermediate host may be involved in the spillover event. Also, the spillover can involve the environment. In this case, the recipient host is infected by the pathogen that has been released into the environment by the source or intermediate host (Borremans et al. 2019BORREMANS B, FAUST C, MANLOVE KR, SOKOLOW SH & LLOYD-SMITH JO. 2019. Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory. Philos Trans R Soc Lond B Biol Sci 374: 20180344., Ellwanger & Chies 2021ELLWANGER JH & CHIES JAB. 2021. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 44: e20200355.).

The association between anthropogenic activity and emerging infectious diseases has been increasingly recognized by the scientific community and by the general population since the beginning of the COVID-19 pandemic, with some positive impact on public concern and awareness about nature and environmental issues (Rousseau & Deschacht 2020ROUSSEAU S & DESCHACHT N. 2020. Public awareness of nature and the environment during the COVID-19 crisis. Environ Resour Econ (Dordr) 12: 1-11., Severo et al. 2021SEVERO EA, DE GUIMARÃES JCF & DELLARMELIN ML. 2021. Impact of the COVID-19 pandemic on environmental awareness, sustainable consumption and social responsibility: Evidence from generations in Brazil and Portugal. J Clean Prod 286: 124947.). A search on the PubMed database using in association the terms “environmental change” and “pandemic” resulted in 1974 documents published in 2021, a huge increase compared to the 64 documents published in 2019 (https://pubmed.ncbi.nlm.nih.gov/; search performed on February 2, 2022). However, the connections and ecological mechanisms linking environmental disturbance and increased risk of zoonotic spillover events are not always explored in scientific publications. Synthesizing the sequence of basic events involved in the emergence of new human pathogens is important to guide the understanding, identification, and description of key aspects of human activities that can be changed to prevent new outbreaks, epidemics, and pandemics. This knowledge is critical for researchers from different fields. Thus, the main aim of this review is to synthesize the principal connections between environmental disturbances and increased risk of spillover events. In this article, ‘environmental disturbance’ refers to disturbance, damage or imbalance caused by human activity on natural landscapes, urban and rural areas, animal populations, or ecosystems.

Considering the multiple dimensions surrounding the association between anthropogenic activity and infectious diseases, this article was written with the collaboration of authors from multiple fields, a strategy aligned with the One Health perspective. In the first part of this article, we briefly discussed the relationship between biodiversity and spillover risk. Subsequently, the connections between environmental disturbances and spillover events are reviewed. Considering the authors’ expertise on tropical ecosystems in the Brazilian context, this review also brings a discussion concerning anthropogenic activities in the Amazon region and their potential impacts on spillover risk and spread of emerging infectious diseases in this region. This article therefore differs from the literature on emerging diseases because it brings together basic information on anthropogenic activities that facilitate zoonotic spillover events in different contexts and countries, and it provides an analysis focused on a specific highly biodiverse biome - the Amazon Forest.

BIODIVERSITY AND SPILLOVER RISK

Biodiversity can be associated with an increased risk of infectious diseases in some situations. For example, this can occur by adding new infectious agents or carriers to the environment (biodiversity as a ‘source’ of pathogens), or through the incorporation of new (host) species into a given environment, or by increasing food sources for disease vectors and thus contributing to their proliferation (Keesing et al. 2006KEESING F, HOLT RD & OSTFELD RS. 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485-498.). A good discussion regarding the complex influences of biodiversity on infectious diseases can be found in Rohr et al. (2020)ROHR JR, CIVITELLO DJ, HALLIDAY FW, HUDSON PJ, LAFFERTY KD, WOOD CL & MORDECAI EA. 2020. Towards common ground in the biodiversity-disease debate. Nat Ecol Evol 4: 24-33.. Although on some occasions biodiverse environments can be associated with increased risk of infectious diseases, biodiversity per se is not the cause of emerging infectious diseases. On the contrary, biodiversity usually confers protection to human health.

High-biodiversity ecosystems ‘dilute’ the density of reservoir hosts and competent vectors, minimizing the contact between reservoir hosts and vectors and reducing the prevalence or load of pathogens in these hosts and vectors, thus decreasing the risk of zoonotic infections. Greater richness and diversity of predators and competitors can also contribute to the control of species that are both adapted to human-modified environments and have the potential to transmit zoonotic pathogens (Schmidt & Ostfeld 2001SCHMIDT KA & OSTFELD RS. 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82: 609-619., Keesing et al. 2006KEESING F, HOLT RD & OSTFELD RS. 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485-498., Ostfeld 2009OSTFELD RS. 2009. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect 15: 40-43., Pongsiri et al. 2009PONGSIRI MJ, ROMAN J, EZENWA VO, GOLDBERG TL, KOREN HS, NEWBOLD SC, OSTFELD RS, PATTANAYAK SK & SALKELD DJ. 2009. Biodiversity loss affects global disease ecology. BioScience 59: 945-954., Civitello et al. 2015CIVITELLO DJ ET AL. 2015. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc Natl Acad Sci USA 112: 8667-8671., Kilpatrick et al. 2017KILPATRICK AM, SALKELD DJ, TITCOMB G & HAHN MB. 2017. Conservation of biodiversity as a strategy for improving human health and well-being. Philos Trans R Soc Lond B Biol Sci 372: 20160131.). The phenomenon in which high species diversity reduces the risk of infectious diseases is called the ‘dilution effect’ (Keesing et al. 2006KEESING F, HOLT RD & OSTFELD RS. 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485-498.).

A good example of the dilution effect can be found in Lyme disease, which is caused by the Borrelia burgdorferi infection and is transmitted by ticks in the genus Ixodes. Different mammals are natural hosts of B. burgdorferi in nature, including the white-footed mouse (Peromyscus leucopus), a highly competent reservoir. The disease affects human populations living in the USA, Canada, and European nations, among other countries. In the presence of a great diversity of reservoir hosts in nature (white-footed mouse plus other hosts), ticks feed on the blood of different hosts with varied competence for Borrelia transmission (many with a low reservoir competence), thus ‘diluting’ the number of infected ticks and consequently the risk of Lyme disease (LoGiudice et al. 2003LOGIUDICE K, OSTFELD RS, SCHMIDT KA & KEESING F. 2003. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA 100: 567-571., Ozdenerol 2015OZDENEROL E. 2015. GIS and remote sensing use in the exploration of Lyme disease epidemiology. Int J Environ Res Public Health 12: 15182-15203., Keesing & Ostfeld 2021KEESING F & OSTFELD RS. 2021. Dilution effects in disease ecology. Ecol Lett 24: 2490-2505.). In brief, high host diversity including poor competent hosts dilutes the infection risk exerted by the few highly competent hosts. On the other hand, the risk of disease increases as the diversity of Borrelia hosts declines and the density of competent reservoir hosts increases in a particular area (LoGiudice et al. 2003LOGIUDICE K, OSTFELD RS, SCHMIDT KA & KEESING F. 2003. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci USA 100: 567-571., Keesing & Ostfeld 2021KEESING F & OSTFELD RS. 2021. Dilution effects in disease ecology. Ecol Lett 24: 2490-2505.).

The impact of host diversity on the disease risk was observed in other models beyond Lyme diseases. The risk of human infection by West Nile virus and Hantavirus decreases as the diversity of their hosts (wild birds and rodents, respectively) increases. The opposite correlation can also occur, with the risk of human infection increasing as host diversity decreases (Mills 2006MILLS JN. 2006. Biodiversity loss and emerging infectious disease: An example from the rodent-borne hemorrhagic fevers. Biodiversity 7: 9-17., Allan et al. 2009ALLAN BF ET AL. 2009. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158: 699-708., Ostfeld 2009OSTFELD RS. 2009. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect 15: 40-43.). These two additional examples highlight the dilution effect, indicating how biodiversity can ‘dilute’ the risk of zoonotic spillover events, protecting human health.

The dilution effect is strongly related to the number and relative abundance of taxa, namely taxonomic diversity (Naeem et al. 2012NAEEM S, DUFFY JE & ZAVALETA E. 2012. The functions of biological diversity in an age of extinction. Science 336: 1401-1406.), which is the kind of “biodiversity” discussed above. However, it is essential to consider that other forms of biodiversity exist, with varied impacts on disease risk. According to Naeem et al. (2012)NAEEM S, DUFFY JE & ZAVALETA E. 2012. The functions of biological diversity in an age of extinction. Science 336: 1401-1406., biodiversity can be classified on the basis of several dimensions, including taxonomic, phylogenetic, genetic, functional, spatial or temporal, interaction, and landscape diversities. These other dimensions of biodiversity can also affect spillover events and the spread of pathogens. For example, genetic diversity has contributed to the emergence of new pathogens or variants, as observed in the SARS-CoV-2 and HIV pandemics, facilitating the transmission and spread of the viruses to different countries (Faria et al. 2014FARIA NR ET AL. 2014. The early spread and epidemic ignition of HIV-1 in human populations. Science 346: 56-61., Andersen et al. 2020ANDERSEN KG, RAMBAUT A, LIPKIN WI, HOLMES EC & GARRY RF. 2020. The proximal origin of SARS-CoV-2. Nat Med 26: 450-452.). Also, interaction diversity (e.g., competition, predation, parasitism) has an important influence on the risk of emergence and spread of zoonotic diseases (Vourc’h et al. 2012VOURC’H G, PLANTARD O & MORAND S. How does biodiversity influence the ecology of infectious disease? In: MORAND S ET AL. (Eds). New Frontiers of Molecular Epidemiology of Infectious Diseases. Springer Science and Business Media B.V. 2012.) because it modulates the contact between species, host immunity, transmission of pathogens and food webs.

It is also fundamental to stress that the dilution effect does not apply to all types of zoonotic diseases, being more closely related to diseases borne by vectors such as arthropods and rodents, as indicated by the examples mentioned above. Furthermore, the dilution effect may be scale dependent. The protective role of biodiversity on disease risk observed at the local scale may not be observed when the effect of biodiversity is analyzed at the global scale. Also, the ecological history of each disease is different and, in some cases, is either weakly dependent on the degree or dimension of biodiversity or its effect is only indirect (Rohr et al. 2020ROHR JR, CIVITELLO DJ, HALLIDAY FW, HUDSON PJ, LAFFERTY KD, WOOD CL & MORDECAI EA. 2020. Towards common ground in the biodiversity-disease debate. Nat Ecol Evol 4: 24-33.). Some diseases of zoonotic origin, but that are currently highly specialized on the human host (e.g., measles, tuberculosis, pneumonia), have a weak relation with measures of biodiversity (Rohr et al. 2020ROHR JR, CIVITELLO DJ, HALLIDAY FW, HUDSON PJ, LAFFERTY KD, WOOD CL & MORDECAI EA. 2020. Towards common ground in the biodiversity-disease debate. Nat Ecol Evol 4: 24-33.).

Other factors (e.g., demography, social issues) also increase the complexity of the relation between biodiversity and zoonotic risk. Globally, countries with high biodiversity are often precisely those where the burden of zoonotic diseases can be observed most intensely. For example, Brazil is classically affected by multiple types of zoonotic vector-borne diseases (Magalhaes et al. 2020MAGALHAES T, CHALEGRE KDM, BRAGA C & FOY BD. 2020. The endless challenges of arboviral diseases in Brazil. Trop Med Infect Dis 5: 75.), despite being one of the most biodiverse countries in the world. Inadequate sanitary conditions and precarious public health systems, which are frequently observed in tropical developing countries, can override the dilution effect associated with high biodiversity, facilitating the emergence and spread of diseases in these countries (Ellwanger et al. 2021ELLWANGER JH, VEIGA ABG, KAMINSKI VL, VALVERDE-VILLEGAS JM, FREITAS AWQ & CHIES JAB. 2021. Control and prevention of infectious diseases from a One Health perspective. Genet Mol Biol 44: e20200256.). In brief, the connections between biodiversity and zoonotic spillover are multiple and complex. Although some generalizations are possible, such as the dilution effect and the connections that will be discussed later in this article, each pathogen and spillover event must be analyzed according to its natural history and the context of its occurrence.

ALIGNMENT OF CONDITIONS CONDUCIVE TO ZOONOTIC SPILLOVER

Role of animal groups

An increased risk of spillover events is usually associated with particular animal orders, including Chiroptera and Rodentia, which are composed of species with supposed high ‘zoonotic potential’. Also, anthropogenic modifications in landscapes favoring human contact with rodents and bats are usually associated with increased risk of zoonotic infection. However, some criticism concerning these aspects is needed. Some animal species can indeed host a high load or diversity of zoonotic pathogens due to intrinsic biological characteristics (e.g., immune system factors, genetic proximity to humans) or due to ecological characteristics, such as the sharing of a habitat with humans or livestock. However, a greater load and variety of pathogens in certain reservoir hosts can be circumstantial and is not necessarily an intrinsic characteristic of a specific animal group. Bats and rodents are often considered highly competent in transmitting pathogens to humans because they harbor a great diversity of zoonotic pathogens, reproduce quickly and often inhabit human-related environments. Chiroptera and Rodentia are the most numerous orders of placental animals, which can increase the opportunity for the emergence of potential zoonotic agents from these animals (Luis et al. 2013LUIS AD ET AL. 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc Biol Sci 280: 20122753., Han et al. 2016HAN BA, KRAMER AM & DRAKE JM. 2016. Global patterns of zoonotic disease in mammals. Trends Parasitol 32: 565-577.). Canidae and Felidae are families in the order Carnivora that also pose risks to the human population in terms of zoonotic spillover because their members (e.g., dogs, foxes, cats) host different zoonotic pathogens and frequently circulate in human-dominated areas (Han et al. 2021HAN BA, CASTELLANOS AA, SCHMIDT JP, FISCHHOFF IR & DRAKE JM. 2021. The ecology of zoonotic parasites in the Carnivora. Trends Parasitol 37: 1096-1110.).

Stray dogs and cats find favorable conditions to proliferate in areas where urbanization has taken place in a disorderly way, and these animals are transmitters of zoonotic diseases in urban centers, especially due to soil contamination with the eggs and oocysts of parasites (Toxocara, Trichuris, Toxoplasma, Cystoisospora and Taenia genera, among others) released into the environment through animal feces. This is a particularly important problem for children because they come into greater contact with the soil in public squares and parks; this affects populations in China, South America, highly developed European nations, and elsewhere (Szwabe & Błaszkowska 2017SZWABE K & BLASZKOWSKA J. 2017. Stray dogs and cats as potential sources of soil contamination with zoonotic parasites. Ann Agric Environ Med 24: 39-43., Montoya et al. 2018MONTOYA A ET AL. 2018. Implications of zoonotic and vector-borne parasites to free-roaming cats in central Spain. Vet Parasitol 251: 125-130., Fu et al. 2019FU Y ET AL. 2019. Prevalence and potential zoonotic risk of hookworms from stray dogs and cats in Guangdong, China. Vet Parasitol Reg Stud Reports 17: 100316., SaldanhaElias et al. 2019SALDANHA-ELIAS AM, SILVA MA, SILVA VO, AMORIM SLA, COUTINHO AR, SANTOS HA, GIUNCHETTI RC, VITOR RWA & GEIGER SM. 2019. Prevalence of endoparasites in urban stray dogs from Brazil diagnosed with Leishmania, with potential for human zoonoses. Acta Parasitol 64: 352-359.). Moreover, leishmaniasis is a major zoonotic disease in several Latin American countries. This disease is caused by Leishmania parasites, which have dogs as common reservoirs. The disease is transmitted by phlebotomine sandflies that proliferate in areas with a lack of environmental sanitation and an abundance of domestic animals, thus affecting people living in urban and peri-urban areas (Teodoro et al. 1999TEODORO U, BALDUÍNO J, THOMAZ-SOCCOL V, BARBOSA OC, FERREIRA MEMC, LOZOVEI AL, VERZIGNASSI TG & ROBERTO ACBS. 1999. Environmental sanitation and peri-domiciliar organisation as auxiliary practices for the control of phlebotomines in Paraná state, southern Brazil. Braz Arch Biol Technol 42: 307-314., Marcondes & Day 2019MARCONDES M & DAY MJ. 2019. Current status and management of canine leishmaniasis in Latin America. Res Vet Sci 123: 261-272.). These cases exemplify the role of the order Carnivora as an additional source of zoonotic pathogens.

Mammals in the order Rodentia were initially classified as the animal group with the highest number of zoonotic hosts, with ~11% of species having zoonotic potential. Highly competent rodent reservoirs show a fast life history profile, reaching sexual maturity and producing offspring at higher rates earlier in life as compared to non-reservoir rodents. Also, highly competent rodent reservoirs usually thrive in areas with high human population densities (Han et al. 2015HAN BA, SCHMIDT JP, BOWDEN SE & DRAKE JM. 2015. Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci USA 112: 7039-7044., 2016). Similar to rodents, bats are usually considered to be of special zoonotic concern because they have high longevity, the colonies are numerous, and the share of viruses between different bat species is increased due to sympatry (Luis et al. 2013LUIS AD ET AL. 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc Biol Sci 280: 20122753.). Bats have immune systems with unique adaptations that allow these animals to harbor many viruses without themselves becoming sick, which contributes to making these animals of special concern regarding zoonotic risk (Hayman 2019HAYMAN DTS. 2019. Bat tolerance to viral infections. Nature Microbiol 4: 728-729., Subudhi et al. 2019SUBUDHI S, RAPIN N & MISRA V. 2019. Immune system modulation and viral persistence in bats: Understanding viral spillover. Viruses 11: 192.).

However, it is necessary to consider some points regarding the role of the orders Rodentia and Chiroptera (especially bats) as disproportionate zoonotic reservoirs. Limited inflammatory responses, high population densities and gregarious social behaviors observed in some bat species may indeed facilitate pathogen transmission among bats, especially viruses, contributing to the zoonotic potential of this group (Brook & Dobson 2015BROOK CE & DOBSON AP. 2015. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol 23: 172-180., Streicker & Gilbert 2020STREICKER DG & GILBERT AT. 2020. Contextualizing bats as viral reservoirs. Science 370: 172-173.). On the other hand, the lack of knowledge about the immunity of other animal groups, including their ability to harbor pathogens asymptomatically, may currently be biasing the conclusion that bats or rodents are especially competent in harboring and transmitting zoonotic pathogens. There is also high immunological variation among bat species, making generalizations about the ability of bats to transmit zoonosis a complicated task. Beyond bats and rodents, other animal groups can be of great importance for the transmission of zoonotic pathogens to humans, although they have been less considered and sampled in studies involving zoonotic diseases (Streicker & Gilbert 2020STREICKER DG & GILBERT AT. 2020. Contextualizing bats as viral reservoirs. Science 370: 172-173.). A recent study by Mollentze & Streicker (2020)MOLLENTZE N & STREICKER DG. 2020. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc Natl Acad Sci USA 117: 9423-9430. reported that the viral zoonotic risk was homogenous among mammalian and avian species when reservoir hosts of 415 RNA and DNA viruses were considered, this being the largest dataset to date. Bats and rodents were considered unexceptional zoonotic hosts, with the proportion of zoonotic viruses varying minimally across the taxonomic orders of the reservoirs that were analyzed (Mollentze & Streicker 2020MOLLENTZE N & STREICKER DG. 2020. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc Natl Acad Sci USA 117: 9423-9430.).

Still concerning bats, human activity has effects beyond those expected from human-triggered changes in the sizes and population structures of these animals. Bats are highly sensitive to anthropogenic activity, which generates physiological stress in these animals. These physiological changes impact infection severity and pathogen shedding in bats, affecting their associated viral populations and risk of spillover events. For example, Plowright et al. (2008)PLOWRIGHT RK, FIELD HE, SMITH C, DIVLJAN A, PALMER C, TABOR G, DASZAK P & FOLEY JE. 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc Biol Sci 275: 861-869. observed that reproduction and nutritional stress in little red flying foxes (Pteropus scapulatus) increases the risk of Hendra virus infection in these animals, potentially increasing the risk of human infection when these conditions occur. Pregnant and lactating female bats showed higher Hendra virus infection rates, and animals under nutritional stress showed higher infection prevalence, a result potentially derived from factors such as poor immune defense or greater contact with other animals while sharing food (Plowright et al. 2008PLOWRIGHT RK, FIELD HE, SMITH C, DIVLJAN A, PALMER C, TABOR G, DASZAK P & FOLEY JE. 2008. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc Biol Sci 275: 861-869.). Furthermore, recent data have shown that the ecological conditions of the flying fox hosts of Hendra virus influence the timing, magnitude, and cumulative intensity of virus shedding, thus affecting the spillover risk (Becker et al. 2021BECKER DJ, EBY P, MADDEN W, PEEL AJ & PLOWRIGHT RK. 2021. Ecological conditions experienced by bat reservoir hosts predict the intensity of Hendra virus excretion over space and time. Available at: https://doi.org/10.1101/2021.08.19.457011. Accessed on February 1st, 2022.
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). Based on these findings, changes in bat immunity derived from human-associated environmental disturbances (e.g., habitat loss, food shortages) can be considered a mechanism by which human activity can increase the risk of spillover events and zoonotic diseases, since these immunological changes can increase infection severity, viral shedding and infection rate in reservoir host populations. Moreover, this information indicates that the zoonotic risk attributed to a given host is circumstantial and not necessarily intrinsic to a specific animal group, with human-related interference on these hosts influencing the circumstantial zoonotic risk.

Host-associated factors, pathogen characteristics and the environmental context

Several host-associated factors can increase or reduce the risks of spillover events, including pathogen load in the source or intermediate host, immunity or nutritional status of recipient host, similarity of pathogen receptors in the different hosts, and genetic/evolutionary distance between species. Spillover risk is also modulated by ecological conditions (e.g., habitat sharing by different species, changing patterns disease in reservoir populations, changing reservoir species behavior) and environmental factors (e.g., landscape characteristics, environmental sanitary conditions, abiotic factors: temperature, humidity, rainfall). Adding more complexity to spillover risk, characteristics of the pathogens (e.g., virulence, transmissibility, viral family, host range) and human behavior (e.g., interaction with other species, invasion of habitats) also affect the spillover risk. The dose and route of human exposure to pathogens also determine the chances of a pathogen crossing the species barrier. After a pathogen successfully reaches a new host, other factors will affect the outcome of the spillover. Not all spillover events result in an epidemic outbreak, and many spillover events go unnoticed, without medical or epidemiological importance. An outbreak or epidemic only occurs when the pathogen, after crossing the barriers between species, finds favorable conditions for its dissemination in the new population. These conditions are usually population agglomeration, unplanned urbanization, and a large number of susceptible hosts (Plowright et al. 2017PLOWRIGHT RK, PARRISH CR, MCCALLUM H, HUDSON PJ, KO AI, GRAHAM AL & LLOYD-SMITH JO. 2017. Pathways to zoonotic spillover. Nat Rev Microbiol 15: 502-510., Becker et al. 2019BECKER DJ, WASHBURNE AD, FAUST CL, PULLIAM JRC, MORDECAI EA, LLOYD-SMITH JO & PLOWRIGHT RK. 2019. Dynamic and integrative approaches to understanding pathogen spillover. Philos Trans R Soc Lond B Biol Sci 374: 20190014., Borremans et al. 2019BORREMANS B, FAUST C, MANLOVE KR, SOKOLOW SH & LLOYD-SMITH JO. 2019. Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory. Philos Trans R Soc Lond B Biol Sci 374: 20180344., Ellwanger & Chies 2021ELLWANGER JH & CHIES JAB. 2021. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 44: e20200355., Grange et al. 2021GRANGE ZL ET AL. 2021. Ranking the risk of animal-to-human spillover for newly discovered viruses. Proc Natl Acad Sci USA 118: e2002324118., Nandi & Allen 2021NANDI A & ALLEN LJS. 2021. Probability of a zoonotic spillover with seasonal variation. Infect Dis Model 6: 514-531.).

The human immunological status at the time of contact with a new zoonotic pathogen influences the outcome of a spillover event. Immunosuppressed individuals can be infected by viruses, fungi, parasites, and bacteria much more easily than individuals with fully competent immune systems (Raychaudhuri et al. 2009RAYCHAUDHURI SP, NGUYEN CT, RAYCHAUDHURI SK & GERSHWIN ME. 2009. Incidence and nature of infectious disease in patients treated with anti-TNF agents. Autoimmun Rev 9: 67-81., Vanichanan et al. 2018VANICHANAN J, UDOMKARNJANANUN S, AVIHINGSANON Y & JUTIVORAKOOL K. 2018. Common viral infections in kidney transplant recipients. Kidney Res Clin Pract 37: 323-337.). Both the maintenance of a pandemic status and the raising of new pathogenic variants are conditions affected by the human immunological status, as can be seen in the current COVID-19 pandemic dynamics. Similarly, HLA alleles and variants in immune-system genes (e.g., single nucleotide polymorphisms in Toll-like receptor, cytokine and chemokine receptor genes, complement system) can either increase or decrease the risk of infection by different pathogens in human populations, in addition to affecting the progression of infection and the host’s pathogen load, and, consequently, disease spread in the population (Burgner et al. 2006BURGNER D, JAMIESON SE & BLACKWELL JM. 2006. Genetic susceptibility to infectious diseases: big is beautiful, but will bigger be even better? Lancet Infect Dis 6: 653-663., Chang et al. 2008CHANG LY ET AL. 2008. HLA-A33 is associated with susceptibility to enterovirus 71 infection. Pediatrics 122: 1271-1276., Pine et al. 2009PINE SO, MCELRATH MJ & BOCHUD PY. 2009. Polymorphisms in toll-like receptor 4 and toll-like receptor 9 influence viral load in a seroincident cohort of HIV-1-infected individuals. AIDS 23: 2387-2395., Ferguson et al. 2011FERGUSON R, RAMANAKUMAR AV, RICHARDSON H, TELLIER PP, COUTLÉE F, FRANCO EL & ROGER M. 2011. Human leukocyte antigen (HLA)-E and HLA-G polymorphisms in human papillomavirus infection susceptibility and persistence. Hum Immunol 72: 337-341., Adriani et al. 2013ADRIANI KS, BROUWER MC, GELDHOFF M, BAAS F, ZWINDERMAN AH, PAUL MORGAN B, HARRIS CL, VAN DER ENDE A & VAN DE BEEK D. 2013. Common polymorphisms in the complement system and susceptiblity to bacterial meningitis. J Infect 66: 255-262., van den Broek et al. 2020VAN DEN BROEK B, VAN DER FLIER M, DE GROOT R, DE JONGE MI & LANGEREIS JD. 2020. Common genetic variants in the complement system and their potential link with disease susceptibility and outcome of invasive bacterial infection. J Innate Immun 12: 131-141., de Vries et al. 2020DE VRIES RD, DE JONG A, VERBURGH RJ, SAUERHERING L, VAN NIEROP GP, VAN BINNENDIJK RS, OSTERHAUS ADME, MAISNER A, KOOPMANS MPG & DE SWART RL. 2020. Human paramyxovirus infections induce T cells that cross-react with zoonotic henipaviruses. mBio 11: e00972-20., Sánchez-Luquez et al. 2021SÁNCHEZ-LUQUEZ K ET AL. 2021. Impact of TLR7 and TLR9 polymorphisms on susceptibility to placental infections and pregnancy complications. J Reprod Immunol 146: 103342.), indicating the importance of host genetics as a determinant of spillover risk and outcome. Therefore, this information makes it clear that when a new pathogen reaches a human being due to favorable ecological conditions (e.g., contact between species sharing the same habitat, land-use changes), the outcome of the spillover event will also be conditioned to a series of other biological factors.

CONNECTIONS BETWEEN ENVIRONMENTAL DISTURBANCES AND ZOONOTIC SPILLOVER

Human behavior and demography

Human behavior and demographic changes are critical modulators of risk and outcome of spillover events. Keeping animals in captivity for decorative or entertainment purposes, the frequent and close contact with wild species, as well as human entry into wild environments, facilitate spillover events because they put humans in close contact with different species. For example, tourist activities involving cave exploration in Africa facilitated Marburg infection cases in past years. Caves are usually visited by numerous animals, including fruit bats (Rousettus aegyptiacus) that act as Marburg reservoir hosts; caves are places where animal deficate and associated pathogens are found in abundance (Johnson et al. 1996JOHNSON ED, JOHNSON BK, SILVERSTEIN D, TUKEI P, GEISBERT TW, SANCHEZ AN & JAHRLING PB. 1996. Characterization of a new Marburg virus isolated from a 1987 fatal case in Kenya. Arch Virol Suppl 11: 101-114., CDC 2009CDC - CENTERS FOR DISEASE CONTROL AND PREVENTION. 2009. Imported case of Marburg hemorrhagic fever - Colorado, 2008. MMWR Morb Mortal Wkly Rep 58: 1377-1381., Amman et al. 2012AMMAN BR ET AL. 2012. Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog 8: e1002877.). Also related to human behavior, the use of wild or exotic animals as pets can facilitate the introduction of new pathogens into the human population (Chomel et al. 2007CHOMEL BB, BELOTTO A & MESLIN FX. 2007. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 13: 6-11.), in addition to being a conservation problem affecting wild species.

Human migratory flows can also change the epidemiology of infectious diseases through the introduction of known and unknown pathogens into new areas, by overburdening health systems, or by exposing non-vaccinated migrants to new pathogens and precarious health conditions. These problems are particularly important in cases of forced migration due to war, political instability and climate change. This indicates that the global political instability associated with the disparity in terms of access to healthcare directly or indirectly affects populations worldwide concerning control and prevention of infectious diseases (Gushulak & MacPherson 2004GUSHULAK BD & MACPHERSON DW. 2004. Globalization of infectious diseases: the impact of migration. Clin Infect Dis 38: 1742-1748., Castelli & Sulis 2017CASTELLI F & SULIS G. 2017. Migration and infectious diseases. Clin Microbiol Infect 23: 283-289., Berry et al. 2020BERRY IM, RUTVISUTTINUNT W, SIPPY R, BELTRAN-AYALA E, FIGUEROA K, RYAN S, SRIKANTH A, STEWART-IBARRA AM, ENDY T & JARMAN RG. 2020. The origins of dengue and chikungunya viruses in Ecuador following increased migration from Venezuela and Colombia. BMC Evol Biol 20: 31., Ibáñez et al. 2021IBÁÑEZ AM, ROZO SV & URBINA MJ. 2021. Forced migration and the spread of infectious diseases. J Health Econ 79: 102491.). Recent measles outbreaks in Brazil and Colombia due to Venezuelan migration demonstrated failures in the vaccination and access to health services by Venezuelans (Hotez et al. 2020HOTEZ PJ, NUZHATH T & COLWELL B. 2020. Combating vaccine hesitancy and other 21st century social determinants in the global fight against measles. Curr Opin Virol 41: 1-7.). The number of ‘climate refugees’ will increase as climate change intensifies, contributing to both the exposure of migrants to new reservoir hosts and related pathogens, and to the change in the profile of infectious diseases in many countries (McMichael 2015MCMICHAEL C. 2015. Climate change-related migration and infectious disease. Virulence 6: 548-553.). However, we stress that the effect of migratory flows on infectious disease burden on migrants and refugees is greater than the effect on the population of the country that receives the immigrants, especially in Europe (Castelli & Sulis 2017CASTELLI F & SULIS G. 2017. Migration and infectious diseases. Clin Microbiol Infect 23: 283-289.).

Exploitation of wildlife

Hunting, wildlife trafficking, animal trade in ‘wet markets,’ and ‘bushmeat’ consumption are classic driving forces of spillover events, since these practices put humans in close contact with pathogens in the meat, blood and other biofluids from a wide range of animal species (Karesh et al. 2005KARESH WB, COOK RA, BENNETT EL & NEWCOMB J. 2005. Wildlife trade and global disease emergence. Emerg Infect Dis 11: 1000-1002., Smith et al. 2012SMITH KM ET AL. 2012. Zoonotic viruses associated with illegally imported wildlife products. PLoS One 7: e29505., Johnson et al. 2020JOHNSON CK, HITCHENS PL, PANDIT PS, RUSHMORE J, EVANS TS, YOUNG CCW & DOYLE MM. 2020. Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proc Biol Sci 287: 20192736., Magouras et al. 2020MAGOURAS I, BROOKES VJ, JORI F, MARTIN A, PFEIFFER DU & DÜRR S. 2020. Emerging zoonotic diseases: Should we rethink the animal-human interface? Front Vet Sci 7: 582743., Zhang & Holmes 2020ZHANG YZ & HOLMES EC. 2020. A Genomic perspective on the origin and emergence of SARS-CoV-2. Cell 181: 223-227.). The expression ‘wet markets’ refers to places where different live animal species are sold in close contact, sometimes sharing a same cage. Some wet markets sell endangered species (Zhang & Holmes 2020ZHANG YZ & HOLMES EC. 2020. A Genomic perspective on the origin and emergence of SARS-CoV-2. Cell 181: 223-227., Peros et al. 2021PEROS CS, DASGUPTA R, KUMAR P & JOHNSON BA. 2021. Bushmeat, wet markets, and the risks of pandemics: Exploring the nexus through systematic review of scientific disclosures. Environ Sci Policy 124: 1-11.). Wet markets are frequently associated with bushmeat. The expression ‘bushmeat’ refers to the meat of hunted wild animals sold in popular or wet markets (Pangau-Adam et al. 2012PANGAU-ADAM M, NOSKE R & MUEHLENBERG M. 2012. Wildmeat or Bushmeat? Subsistence hunting and commercial harvesting in Papua (West New Guinea), Indonesia. Hum Ecol 40: 611-621.), in some situations in the absence of adequate sanitary standards according to regulatory agencies (Naguib et al. 2021NAGUIB MM, LI R, LING J, GRACE D, NGUYEN-VIET H & LINDAHL JF. 2021. Live and wet markets: food access versus the risk of disease emergence. Trends Microbiol 29: 573-581., Peros et al. 2021PEROS CS, DASGUPTA R, KUMAR P & JOHNSON BA. 2021. Bushmeat, wet markets, and the risks of pandemics: Exploring the nexus through systematic review of scientific disclosures. Environ Sci Policy 124: 1-11., Saylors et al. 2021SAYLORS KE ET AL. 2021. Market characteristics and zoonotic disease risk perception in Cameroon bushmeat markets. Soc Sci Med 268: 113358., WHO 2021WHO - World Health Organization, OiE - World Organisation for Animal Health, UN Environment Programme. 2021. Reducing public health risks associated with the sale of live wild animals of mammalian species in traditional food markets. Available at: https://www.who.int/publications/i/item/WHO-2019-nCoV-Food-safety-traditional-markets-2021.1. Access on January 30, 2022.
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). Sanitary requirements may vary depending on the sanitary regulations of each country, and traditional food markets can be considered safe when operating in accordance with health regulations (WHO 2021).

Different from ‘bushmeat’ (hunted meat for income purposes), ‘wild meat’ refers to the meat of wild animals killed for consumption by hunters and their families. As bushmeat products usually come from systematic hunting activities, including frequent handling of animal carcasses, blood and viscera without sanitary control or inspection, bushmeat is associated with increased spillover risk (Wolfe et al. 2005WOLFE ND, DASZAK P, KILPATRICK AM & BURKE DS. 2005. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerg Infect Dis 11: 1822-1827., Pangau-Adam et al. 2012PANGAU-ADAM M, NOSKE R & MUEHLENBERG M. 2012. Wildmeat or Bushmeat? Subsistence hunting and commercial harvesting in Papua (West New Guinea), Indonesia. Hum Ecol 40: 611-621., Peros et al. 2021PEROS CS, DASGUPTA R, KUMAR P & JOHNSON BA. 2021. Bushmeat, wet markets, and the risks of pandemics: Exploring the nexus through systematic review of scientific disclosures. Environ Sci Policy 124: 1-11.). For these reasons, wet markets and bushmeat consumption are recognized as important drivers of zoonotic spillover, unlike markets or fairs where meat products are sold under sanitary inspection, which reduces the risk of transmission of pathogens to humans (Wolfe et al. 2005WOLFE ND, DASZAK P, KILPATRICK AM & BURKE DS. 2005. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerg Infect Dis 11: 1822-1827., Karesh & Noble 2009KARESH WB & NOBLE E. 2009. The bushmeat trade: increased opportunities for transmission of zoonotic disease. Mt Sinai J Med 76: 429-434., Zhang & Holmes 2020ZHANG YZ & HOLMES EC. 2020. A Genomic perspective on the origin and emergence of SARS-CoV-2. Cell 181: 223-227., Naguib et al. 2021NAGUIB MM, LI R, LING J, GRACE D, NGUYEN-VIET H & LINDAHL JF. 2021. Live and wet markets: food access versus the risk of disease emergence. Trends Microbiol 29: 573-581., Peros et al. 2021PEROS CS, DASGUPTA R, KUMAR P & JOHNSON BA. 2021. Bushmeat, wet markets, and the risks of pandemics: Exploring the nexus through systematic review of scientific disclosures. Environ Sci Policy 124: 1-11.). In these places, spillover risk also exists [as indicated by human outbreaks of food-borne diseases in high-income nations like the UK (Public Health England 2018PUBLIC HEALTH ENGLAND. 2018. Zoonoses Report UK 2017. Available at: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/918089/UK_Zoonoses_report_2017.pdf. Accessed on October 26, 2021.
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)], but the risk is lower due to sanitary control.

Land-use changes and exploitation of Indigenous lands

Other human-mediated activities also facilitate spillover events, including deforestation, industrial livestock, monoculture farming, and mining, among other types of human alterations on land. These changes are commonly unified in the expression ‘land-use changes.’ Land-use changes lead to host exposure to a new array of pathogens (Murray & Daszak 2013MURRAY KA & DASZAK P. 2013. Human ecology in pathogenic landscapes: two hypotheses on how land use change drives viral emergence. Curr Opin Virol 3: 79-83.). The construction of roads in wild landscapes (e.g., Amazon rainforest), besides causing damage to ecosystems (Ferrante & Fearnside 2020aFERRANTE L & FEARNSIDE PM. 2020a. The Amazon’s road to deforestation. Science 369: 634.), increases the contact of humans with forest-associated animal species and the risk of spillover. Although the human presence can scare away some animal species, when humans invade forest environments to build roads or to perform mining and logging activities, among other reasons, the contact with animal species increases, especially contact with mosquitoes and other blood-sucking insects that benefit from the human presence that provides an additional food source. This closer and more frequent interaction between humans and anthropophilic insects favors spillover events mediated by invertebrate intermediate hosts (Ellwanger et al. 2020ELLWANGER JH ET AL. 2020. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc 92: e20191375.).

Extensive land-use changes and associated spillover risk are also a major issue for Indigenous populations. Due to limited contact with non-indigenous populations, indigenous peoples have weak or no natural/protective immunity to pathogens that emerged outside Indigenous areas. Such populations also have limited access to vaccines and healthcare facilities. These factors exacerbate the burden related to emerging pathogens in Indigenous populations. This is a problem observed in several situations and in various parts of the world, from the colonization of the Americas and Africa by Europeans to the ongoing COVID-19 pandemic in Brazil, among other situations (Valeggia & Snodgrass 2015VALEGGIA CR & SNODGRASS JJ. 2015. Health of Indigenous peoples. Annu Rev Anthropol 44: 117-135., Ferrante & Fearnside 2020bFERRANTE L & FEARNSIDE PM. 2020b. Protect Indigenous peoples from COVID-19. Science 368: 251.). Of particular concern is a proposed law in Brazil (PL191/2020) opening Indigenous lands to mining, logging, agriculture and other activities by non-indigenous people (Villén-Pérez et al. 2021VILLÉN-PÉREZ S, ANAYA-VALENZUELA L, CRUZ DC & FEARNSIDE PM. 2021. Mining threatens isolated indigenous peoples in the Brazilian Amazon. Glob Environ Change 72: 102398.). The risk is clear in a project that is already moving ahead to grow corn (maize) to feed pigs in an Indigenous area in association with a food and biofuel company (Ferrante et al. 2021FERRANTE L, BARBOSA RI, DUCZMAL L & FEARNSIDE PM. 2021. Brazil’s planned exploitation of Amazonian indigenous lands for commercial agriculture increases risk of new pandemics. Reg Environ Change 21: 81.). Land-use activities in the Indigenous areas expose both Indigenous peoples and workers to a new range of potential exotic pathogens.

Similarly, human contact with other animal species is facilitated by habitat fragmentation (Wilkinson et al. 2018WILKINSON DA, MARSHALL JC, FRENCH NP & HAYMAN DTS. 2018. Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence. J R Soc Interface 15: 20180403.). For example, the transmission of zoonotic parasitic diseases such as leishmaniasis and Chagas disease is facilitated in areas with fragmented vegetation due to the increased human contact with the vectors of Leishmania and Trypanosoma parasites (phlebotomine sandflies and triatomine bugs, respectively), and changes in the composition and infectious status of wild hosts (Vaz et al. 2007VAZ VC, D’ANDREA PS & JANSEN AM. 2007. Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi. Parasitology 134: 1785-1793., Roque et al. 2008ROQUE AL, XAVIER SC, DA ROCHA MG, DUARTE AC, D’ANDREA OS & JANSEN AM. 2008. Trypanosoma cruzi transmission cycle among wild and domestic mammals in three areas of orally transmitted Chagas disease outbreaks. Am J Trop Med Hyg 79: 742-749., Curi et al. 2014CURI NHA, PASCHOAL AMO, MASSARA RL, MARCELINO AP, RIBEIRO AA, PASSAMANI M, DEMÉTRIO GR & CHIARELLO AG. 2014. Factors associated with the seroprevalence of leishmaniasis in dogs living around Atlantic Forest fragments. PLoS One 9: e104003., Zaidi et al. 2017ZAIDI F, FATIMA SH, JAN T, FATIMA M, ALI A, KHISROON M, ADNAN M & RASHEED SB. 2017. Environmental risk modelling and potential sand fly vectors of cutaneous leishmaniasis in Chitral district: a leishmanial focal point of mount Tirich Mir, Pakistan. Trop Med Int Health 22: 1130-1140., Cardozo et al. 2021CARDOZO M, FIAD FG, CROCCO LB & GORLA DE. 2021. Effect of habitat fragmentation on rural house invasion by sylvatic triatomines: A multiple landscape-scale approach. PLoS Negl Trop Dis 15: e0009579.). In a general sense, the maintenance of habitat core/solidity reduces the habitat perimeter, diminishing the human contact with other species and, consequently, the spillover risk. On the other hand, habitat fragmentation increases the habitat perimeter and contact zones where pathogen transmissions may occur between non-human animals and humans (Wilkinson et al. 2018WILKINSON DA, MARSHALL JC, FRENCH NP & HAYMAN DTS. 2018. Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence. J R Soc Interface 15: 20180403., Borremans et al. 2019BORREMANS B, FAUST C, MANLOVE KR, SOKOLOW SH & LLOYD-SMITH JO. 2019. Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory. Philos Trans R Soc Lond B Biol Sci 374: 20180344., Bloomfield et al. 2020BLOOMFIELD LSP, MCINTOSH TL & LAMBIN EF. 2020. Habitat fragmentation, livelihood behaviors, and contact between people and nonhuman primates in Africa. Landscape Ecol 35: 985-1000.). Specifically, there are examples showing that habitat fragmentation in Africa was associated with increased human contact with non-human primates, bats, and potentially the zoonotic pathogens found in these animals (Rulli et al. 2017RULLI MC, SANTINI M, HAYMAN DTS & D’ODORICO P. 2017. The nexus between forest fragmentation in Africa and Ebola virus disease outbreaks. Sci Rep 7: 41613., Bloomfield et al. 2020BLOOMFIELD LSP, MCINTOSH TL & LAMBIN EF. 2020. Habitat fragmentation, livelihood behaviors, and contact between people and nonhuman primates in Africa. Landscape Ecol 35: 985-1000.). A recent study reported that the risk of SARS-related coronavirus outbreaks in China is higher in areas with forest fragmentation and concentrations of livestock and humans (Rulli et al. 2021RULLI MC, D’ODORICO P, GALLI N & HAYMAN DTS. 2021. Land-use change and the livestock revolution increase the risk of zoonotic coronavirus transmission from rhinolophid bats. Nature Food 2: 409-416.). Habitat fragmentation is strongly associated with loss of ecosystem functions, reduced landscape connectivity, and biodiversity loss (Haddad et al. 2015HADDAD NM ET AL. 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1: e1500052.), which impairs the dilution effect and increases the risk of zoonotic diseases through this additional mechanism (Allan et al. 2003ALLAN BF, KEESING F & OSTFELD RS. 2003. Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17: 267-272., Keesing et al. 2006KEESING F, HOLT RD & OSTFELD RS. 2006. Effects of species diversity on disease risk. Ecol Lett 9: 485-498.). These factors act in synergy with the proliferation of species adapted to human-modified environments and an increase in the load of pathogens hosted by these species, thus creating favorable conditions for the transmission of relatively new zoonotic pathogens to humans.

Livestock industry and antimicrobial resistance

The large scale of the livestock industry for the production of meat and other animal products leads to the confinement of a large number of animals in small areas, usually with frequent contact with humans and other species. As previously described, environments with low species richness can limit the dilution effect, favoring the spread of pathogens. In addition, the movement of livestock within and between countries with little or no sanitary inspection poses a threat to the dissemination of infectious diseases if these animals carry pathogens with zoonotic potential, such as Rift Valley fever virus, as seen in East-African countries that export livestock (Anyamba et al. 2001ANYAMBA A, LINTHICUM KJ & TUCKER CJ. 2001. Climate-disease connections: Rift Valley Fever in Kenya. Cad Saude Publica 17: 133-140., Martin et al. 2008MARTIN V, CHEVALIER V, CECCATO P, ANYAMBA A, DE SIMONE L, LUBROTH J, DE LA ROCQUE S & DOMENECH J. 2008. The impact of climate change on the epidemiology and control of Rift Valley fever. Rev Sci Tech 27: 413-426., Taylor et al. 2016TAYLOR D, HAGENLOCHER M, JONES AE, KIENBERGER S, LEEDALE J & MORSE AP. 2016. Environmental change and Rift Valley fever in eastern Africa: projecting beyond HEALTHY FUTURES. Geospat Health 11: 387.).

Animals from livestock production also act as intermediate hosts for the adaptation of pathogens from wildlife before they are introduced into the human population. For example, swine (e.g., domestic pigs) are considered to be ‘mixing vessels’ where strains of influenza A viruses from wild birds can undergo genetic recombination or reassortment with other viruses present in pigs, originating new influenza strains that will then be transmitted to the human population. This occurs because pigs have cell receptors recognized by avian and human influenza viruses, in addition to sharing the environment with different species of birds and humans (Ma et al. 2008MA W, KAHN RE & RICHT JA. 2008. The pig as a mixing vessel for influenza viruses: Human and veterinary implications. J Mol Genet Med 3: 158-166., Ellwanger & Chies 2021ELLWANGER JH & CHIES JAB. 2021. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 44: e20200355.). The role of pigs as mixing vessels for the reassortment of influenza viruses has already been shown by various studies, confirming that pigs can act as intermediate hosts for the adaptation of animal influenza viruses before being introduced into the human population (Zhou et al. 1999ZHOU NN, SENNE DA, LANDGRAF JS, SWENSON SL, ERICKSON G, ROSSOW K, LIU L, YOON KJ, KRAUSS S & WEBSTER RG. 1999. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73: 8851-8856., Urbaniak et al. 2017URBANIAK K, MARKOWSKA-DANIEL I, KOWALCZYK A, KWIT K, POMORSKA-MÓL M, FRĄCEK B & PEJSAK Z. 2017. Reassortment process after co-infection of pigs with avian H1N1 and swine H3N2 influenza viruses. BMC Vet Res 13: 215., Zell et al. 2020ZELL R, GROTH M, KRUMBHOLZ A, LANGE J, PHILIPPS A & DÜRRWALD R. 2020. Novel reassortant swine H3N2 influenza A viruses in Germany. Sci Rep 10: 14296.). In a study performed in Egypt, Gomaa et al. (2018)GOMAA MR, KANDEIL A, EL-SHESHENY R, SHEHATA MM, MCKENZIE PP, WEBBY RJ, ALI MA & KAYALI G. 2018. Evidence of infection with avian, human, and swine influenza viruses in pigs in Cairo, Egypt. Arch Virol 163: 359-364. found evidence of infection with avian (H9N2, H5N1), human (pandemic H1N1), and swine influenza viruses in pigs. Ganti et al. (2021)GANTI K, BAGGA A, DASILVA J, SHEPARD SS, BARNES JR, SHRINER S, KOELLE K & LOWEN AC. 2021. Avian influenza A viruses reassort and diversify differently in mallards and mammals. Viruses 13: 509. recently showed that mallard ducks also have the potential to act as mixing vessels for the reassortment of influenza A viruses.

Animals from livestock production (e.g., cattle, swine, poultry) also pose a zoonotic risk to human populations considering diseases caused by parasites, especially when these animals are raised in inadequate facilities and with poor hygiene conditions. Infection by Fasciola hepatica, Schistosoma japonicum, Trichinella spiralis, among other parasitic infections, can affect humans due to problems in the practices of breeding, confinement and sanitary inspection of livestock animals and derived products (Gortázar et al. 2007GORTÁZAR C, FERROGLIO E, HÖFLE U, FRÖLICH K & VICENTE J. 2007. Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53: 241-256., Rist et al. 2015RIST CL, GARCHITORENA A, NGONGHALA CN, GILLESPIE TR & BONDS MH. 2015. The burden of livestock parasites on the poor. Trends Parasitol. 31: 527-530.). Livestock can act as bridges (intermediate hosts) for the transmission of parasites from wild hosts to humans (Gortázar et al. 2007GORTÁZAR C, FERROGLIO E, HÖFLE U, FRÖLICH K & VICENTE J. 2007. Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53: 241-256., Wiethoelter et al. 2015WIETHOELTER AK, BELTRÁN-ALCRUDO D, KOCK R & MOR SM. 2015. Global trends in infectious diseases at the wildlife-livestock interface. Proc Natl Acad Sci USA. 112: 9662-9667.).

Finally, it is possible that the introduction (spillover) of SARS-related viruses (SARS-CoV, MERS-CoV) to the human population from bats, source hosts for both SARS-related viruses, has the participation of intermediate hosts, specifically palm civets for SARS-CoV and camels for MERS-CoV. However, the direct bat-human transmission of these viruses cannot be ruled out (Letko et al. 2020LETKO M, SEIFERT SN, OLIVAL KJ, PLOWRIGHT RK & MUNSTER VJ. 2020. Bat-borne virus diversity, spillover and emergence. Nat Rev Microbiol 18: 461-471.). Some farmed species such as minks, red foxes, and raccoon dogs, potentially acted as intermediary hosts in the SARS-CoV-2 spillover into the human population, but this represents an open question (Koopmans et al. 2021KOOPMANS M ET AL. 2021. Origins of SARS-CoV-2: window is closing for key scientific studies. Nature 596: 482-485., Lytras et al. 2021LYTRAS S, XIA W, HUGHES J, JIANG X & ROBERTSON DL. 2021. The animal origin of SARS-CoV-2. Science 373: 968-970.). The large number of animals observed in industrial livestock production and the frequent contact with other animal species create numerous opportunities for the adaptation of new pathogens before reaching the human population.

The intensive use of antimicrobial drugs in the livestock industry creates ideal conditions for the selection of microorganisms resistant to multiple drugs and for the emergence of new pathogenic microbial strains, reinforcing opportunities for spillover events (Ye et al. 2016YE X, FAN Y, WANG X, LIU W, YU H, ZHOU J, CHEN S & YAO Z. 2016. Livestock-associated methicillin and multidrug resistant S. aureus in humans is associated with occupational pig contact, not pet contact. Sci Rep 6: 19184., He et al. 2020HE Y, YUAN Q, MATHIEU J, STADLER L, SENEHI N, SUN R & ALVAREZ PJJ. 2020. Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. NPJ Clean Water 3: 4., Magouras et al. 2020MAGOURAS I, BROOKES VJ, JORI F, MARTIN A, PFEIFFER DU & DÜRR S. 2020. Emerging zoonotic diseases: Should we rethink the animal-human interface? Front Vet Sci 7: 582743.). Drug-resistant pathogens were responsible for ~20% of all emerging infectious-disease events reported since 1940, a phenomenon stemming from the pervasive use of antimicrobial drugs (Jones et al. 2008JONES KE, PATEL NG, LEVY MA, STOREYGARD A, BALK D, GITTLEMAN JL & DASZAK P. 2008. Global trends in emerging infectious diseases. Nature 451: 990-993.). Inappropriate intensive use of antimicrobials in human medicine (e.g., azithromycin as a supposed COVID-19 treatment) will contribute to the emergence of multiresistant strains (Afshinnekoo et al. 2021AFSHINNEKOO E ET AL. 2021. COVID-19 drug practices risk antimicrobial resistance evolution. Lancet Microbe 2: e135-e136.). The role of drug resistance in the emergence of outbreaks and epidemics is expected to gain greater attention in the coming decades, along with anthropogenic pressures on the environment and animal species.

Fires and other drivers of unusual movement pattern of animals

Fires, deforestation, and habitat loss induce wild animals to assume unusual movement patterns and alternative spatial distributions because these animals need to leave their natural habitats to obtain food, water and shelter, or to escape fire, among other reasons (Johnson et al. 1992JOHNSON AR, WIENS JA, MILNE BT & CRIST TO. 1992. Animal movements and population dynamics in heterogeneous landscapes. Landscape Ecol 7: 63-75., Hadley & Betts 2009HADLEY AS & BETTS MG. 2009. Tropical deforestation alters hummingbird movement patterns. Biol Lett 5: 207-210., Niebuhr et al. 2015NIEBUHR BBS, WOSNIACK ME, SANTOS MC, RAPOSO EP, VISWANATHAN GM, DA LUZ MGE & PIE MR. 2015. Survival in patchy landscapes: the interplay between dispersal, habitat loss and fragmentation. Sci Rep 5: 11898., Nimmo et al. 2019NIMMO DG ET AL. 2019. Animal movements in fire-prone landscapes. Biol Rev Camb Philos Soc 94: 981-998., Ramos et al. 2020RAMOS DL, PIZO MA, RIBEIRO MC, CRUZ RS, MORALES JM & OVASKAINEN O. 2020. Forest and connectivity loss drive changes in movement behavior of bird species. Ecography 43: 1-12.). In response to such events, animals often supply their needs in forest-city borders and in urban and peri-urban areas (e.g., migration of non-human primates from wild areas to cities), especially when urban settings are established in areas previously occupied by forests. For instance, in the Brazilian cities of Rio de Janeiro and Porto Alegre, non-human primates share forest fragments with the human population (Cunha et al. 2006CUNHA AA, VIEIRA MV & GRELLE CEV. 2006. Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic forest fragment: The capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca forest, Rio de Janeiro. Urban Ecosyst 9: 351-359., Corrêa et al. 2018CORRÊA FM, CHAVES ÓM, PRINTES RC & ROMANOWSKI HP. 2018. Surviving in the urban-rural interface: Feeding and ranging behavior of brown howlers (Alouatta guariba clamitans) in an urban fragment in southern Brazil. Am J Primatol 80: e22865.). Also in Brazil, non-human primates (howler monkeys) and forest-dwelling mosquitoes found in city-forest interfaces (as a consequence of urbanization, habitat loss and forest fragmentation) can act as bridges between the sylvatic and urban cycles of yellow fever, as well as bridges for the spillover of new human pathogens from wildlife (Cardoso et al. 2010CARDOSO JC ET AL. 2010. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, southern Brazil, 2008. Emerg Infect Dis 16: 1918-1924., Almeida et al. 2012ALMEIDA MAB, DOS SANTOS E, CARDOSO JC, DA FONSECA DF, NOLL CA, SILVEIRA VR, MAEDA AY, DE SOUZA RP, KANAMURA C & BRASIL RA. 2012. Yellow fever outbreak affecting Alouatta populations in southern Brazil (Rio Grande do Sul State), 2008-2009. Am J Primatol 74: 68-76., Couto-Lima et al. 2017COUTO-LIMA D, MADEC Y, BERSOT MI, CAMPOS SS, MOTTA MA, SANTOS FBD, VAZEILLE M, VASCONCELOS PFDC, LOURENÇO-DE-OLIVEIRA R & FAILLOUX AB. 2017. Potential risk of re-emergence of urban transmission of Yellow Fever virus in Brazil facilitated by competent Aedes populations. Sci Rep 7: 4848.).

In addition to inducing animals to explore new environments due to habitat loss, fires can favor the occurrence of arboviral diseases. In Brazil, studies have associated fires with outbreaks of Dengue, Zika, Chikungunya and Yellow fever, especially in areas where fires have an anthropogenic origin and are associated with the expansion of agriculture and livestock production (Torres et al. 2019TORRES RG, MOREIRA VM, MOREIRA PF & NEVES RA. 2019. Análise da distribuição espacial dos casos de febre amarela no estado de Goiás, 2007 – 2017. RBMC 5: 35-41., Moreno et al. 2021MORENO GS, SANTANA LON, NUVOLONI FM & LOPES EFN. 2021. Incêndios, queimadas e arboviroses: relações emergentes na pré e pós pandemia. Revista Científica ANAP Brasil 14: 1-14.). The increase in fire outbreaks recently observed in Brazil and other countries (Pivello et al. 2021PIVELLO VR ET AL. 2021. Understanding Brazil’s catastrophic fires: Causes, consequences and policy needed to prevent future tragedies. Perspect Ecol Conserv 19: 233-255.) will potentially increase the risk of spillover events involving arboviruses.

Animal trafficking and the domestication of wild animals also contribute to changes in the geographical distribution of animal species and pathogens with zoonotic potential. These processes can put human populations into contact with new pathogens from exotic animals that have been artificially moved to new areas and environments. For example, zoonotic Salmonella outbreaks were associated to animal trafficking and exotic pets (e.g., Amazon parrots) (Marietto-Gonçalves et al. 2010MARIETTO-GONÇALVES GA, DE ALMEIDA SM, DE LIMA ET, OKAMOTO AS, PINCZOWSKI P & FILHO RLA. 2010. Isolation of Salmonella enterica serovar enteritidis in blue-fronted Amazon parrot (Amazona aestiva). Avian Dis 54: 151-155., Saidenberg et al. 2021SAIDENBERG ABS ET AL. 2021. Salmonella Newport outbreak in Brazilian parrots: confiscated birds from the illegal pet trade as possible zoonotic sources. Environ Microbiol Rep 13: 702-707.). Also, Kovalev & Mazurina (2022)KOVALEV SY & MAZURINA EA. 2022. Omsk hemorrhagic fever virus is a tick-borne encephalitis virus adapted to muskrat through host-jumping. J Med Virol 94: 2510-2518. recently evaluated Omsk hemorrhagic fever, an endemic disease from Western Siberia and associated with muskrats (Ondatra zibethicus). Since the Omsk hemorrhagic fever virus (OHFV) is closely related to the tick-borne encephalitis virus (TBEV), considering genetic and ecological characteristics, the authors suggested that the OHFV originated directly from the TBEV (Far Eastern subtype) in a spillover event involving the transmission of the virus from Ixodes persulcatus ticks to muskrats after the human introduction of O. zibethicus to Western Siberia in the second half of the 1930s. The introduction of O. zibethicus in this new region was motivated by the potential use of muskrat’s valuable fur (Kovalev & Mazurina 2022KOVALEV SY & MAZURINA EA. 2022. Omsk hemorrhagic fever virus is a tick-borne encephalitis virus adapted to muskrat through host-jumping. J Med Virol 94: 2510-2518.).

Unusual animal movement patterns are also of epidemiological concern when they involve domestic animals with competence for the transmission of zoonoses, potentially increasing the risks of zoonotic spillover or creating conditions for these animals to act as bridges to pathogen hosts. Dogs that circulate between urban and forest areas can facilitate the spillover and spillback (human-to-animal transmission) of many pathogens, increasing the infectious-disease risk for both human and animal populations (Martinez et al. 2013MARTINEZ E, CESÁRIO C, DE OLIVEIRA E SILVA I & BOERE V. 2013. Domestic dogs in rural area of fragmented Atlantic Forest: potential threats to wild animals. Cienc Rural 43: 1998-2003., Ellwanger & Chies 2019ELLWANGER JH & CHIES JAB. 2019. The triad “dogs, conservation and zoonotic diseases” - An old and still neglected problem in Brazil. Perspect Ecol Conserv 17: 157-161.).

Biotic and abiotic environmental changes

Studies performed with mosquitoes are critical to comprehend how human disturbance of the environment can lead to an increased risk of spillover events mediated by vectors (as intermediary hosts). Environments with high biodiversity tend to have a greater variety and abundance of predators of disease vectors. These predators include bats, birds, amphibians and larvivorous fishes that feed on mosquitoes at different stages of development. Reduction of the diversity of predators due to anthropic action can benefit the survival and proliferation of mosquitoes. Also, abiotic factors (e.g., sunlight, wind patterns, temperature, moisture, and the pH of water in breeding sites) are altered in degraded landscapes and can affect vector distribution and proliferation (Burkett-Cadena & Vittor 2018BURKETT-CADENA ND & VITTOR AY. 2018. Deforestation and vector-borne disease: Forest conversion favors important mosquito vectors of human pathogens. Basic Appl Ecol 26: 101-110., Almeida et al. 2019ALMEIDA MAB, DOS SANTOS E, CARDOSO JC, DA SILVA LG, RABELO RM & BICCA-MARQUES JC. 2019. Predicting yellow fever through species distribution modeling of virus, vector, and monkeys. Ecohealth 16: 95-108., Franklinos et al. 2019FRANKLINOS LHV, JONES KE, REDDING DW & ABUBAKAR I. 2019. The effect of global change on mosquito-borne disease. Lancet Infect Dis 19: e302-e312.). For example, lower temperatures in the forest can slow the larval development of mosquitoes while the opposite can occur when forests are cleared, resulting in warmer temperatures, greater light intensities, and increased availability of nutrients in water pools, thus benefitting the larvae of some mosquito species (Burkett-Cadena & Vittor 2018BURKETT-CADENA ND & VITTOR AY. 2018. Deforestation and vector-borne disease: Forest conversion favors important mosquito vectors of human pathogens. Basic Appl Ecol 26: 101-110., Franklinos et al. 2019FRANKLINOS LHV, JONES KE, REDDING DW & ABUBAKAR I. 2019. The effect of global change on mosquito-borne disease. Lancet Infect Dis 19: e302-e312.). Consequently, these ecological and abiotic changes benefit mosquito populations and increase the risk of spillover events mediated by vectors (Burkett-Cadena & Vittor 2018BURKETT-CADENA ND & VITTOR AY. 2018. Deforestation and vector-borne disease: Forest conversion favors important mosquito vectors of human pathogens. Basic Appl Ecol 26: 101-110., Ellwanger & Chies 2018ELLWANGER JH & CHIES JAB. 2018. Wind: a neglected factor in the spread of infectious diseases. Lancet Planet Health 2: e475., Almeida et al. 2019ALMEIDA MAB, DOS SANTOS E, CARDOSO JC, DA SILVA LG, RABELO RM & BICCA-MARQUES JC. 2019. Predicting yellow fever through species distribution modeling of virus, vector, and monkeys. Ecohealth 16: 95-108., Franklinos et al. 2019FRANKLINOS LHV, JONES KE, REDDING DW & ABUBAKAR I. 2019. The effect of global change on mosquito-borne disease. Lancet Infect Dis 19: e302-e312.). From a global perspective, it is very likely that climate change in the coming decades, including a 1.0–3.5ºC increase of global temperature and more frequent climatic anomalies (e.g., El Niño, droughts, floods), will lead to an increased burden of vector-borne diseases and more zoonotic spillover events mediated by arthropod vectors (Githeko et al. 2000GITHEKO AK, LINDSAY SW, CONFALONIERI UE & PATZ JA. 2000. Climate change and vector-borne diseases: A regional analysis. Bull World Health Organ 78: 1136-1147., Watts et al. 2019WATTS N ET AL. 2019. The 2019 report of The Lancet Countdown on health and climate change: ensuring that the health of a child born today is not defined by a changing climate. Lancet 394: 1836-1878., Wilke et al. 2019bWILKE ABB, BEIER JC & BENELLI G. 2019b. Complexity of the relationship between global warming and urbanization - an obscure future for predicting increases in vector-borne infectious diseases. Curr Opin Insect Sci 35: 1-9.).

Finally, it is essential to consider that disease cycles are often complex, being influenced by factors that go beyond the abiotic sphere, such as biological aspects of vertebrate hosts (immunity, genetics, and other characteristics, as discussed previously), arthropod resistance to insecticides, and stresses on communities of vectors (Guedes et al. 2017GUEDES RNC, WALSE SS & THRONE JE. 2017. Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21: 47-53., Pavlidi et al. 2018PAVLIDI N, VONTAS J & VAN LEEUWEN T. 2018. The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors. Curr Opin Insect Sci 27: 97-102.). Therefore, the impact of climate change on vector-borne and other zoonotic diseases will be affected by these other factors, making it difficult to accurately predict the intensity of impacts and distribution of pathogens and diseases in a changing world. Considering these uncertainties, the precautionary principle must be considered (Mahrenholz 2008MAHRENHOLZ P. 2008. Climate change and adaptation needs. Parasitol Res 103(Suppl 1): S139-S146.) and anthropogenic changes in the environment must be controlled in order to reduce zoonotic risks to the human population.

ANTHROPOGENIC ACTIVITIES IN THE AMAZON REGION AND THEIR POTENTIAL IMPACTS ON SPILLOVER EVENTS

The Amazon Forest is one of the most biodiverse regions in the world, with 70% of the Amazon basin located within Brazil (Kirby et al. 2006KIRBY KR, LAURANCE WF, ALBERNAZ AK, SCHROTH G, FEARNSIDE PM, BERGEN S, VENTICINQUE EM & COSTA C. 2006. The future of deforestation in the Brazilian Amazon. Futures 38: 432-453.). Due to its high biodiversity combined with a diversity of anthropogenic activities in the region, the Amazon Forest is a hotspot for the emergence of new pathogens (Val 2020VAL AL. 2020. Biodiversity - the hidden risks. An Acad Bras Cienc 92: e20200699.). Indeed, there are numerous potential new pathogens in the Amazon Forest that could pose a risk to human populations. However, it is the intense human activity in the region that is the main driver of potential spillover events in the Amazon Forest, not the biodiversity per se.

Degradation of tropical forests, including the Amazon Forest, is strongly derived from economic activities linked to the exploitation of minerals, oil, and timber, in addition to industrial livestock and monoculture production. Globalization and economic connections between developed and developing countries mean that the triggers of environmental degradation in any given part of the world can be derived from demands of distant countries or even other continents. For instance, land-use changes in the Amazon Forest, including the increasing deforestation rate in the region (see Figure 1, panel a, for more data), are partially triggered by the demand for beef and agricultural commodities by China and European countries (Fearnside et al. 2013FEARNSIDE PM, FIGUEIREDO AMR & BONJOUR SCM. 2013. Amazonian forest loss and the long reach of China’s influence. Environ Dev Sustain 15: 325-338., Fuchs et al. 2019FUCHS R, ALEXANDER P, BROWN C, COSSAR F, HENRY RC & ROUNSEVELL M. 2019. Why the US-China trade war spells disaster for the Amazon. Nature 567: 451-454., Pendrill et al. 2019PENDRILL F, PERSSON UM, GODAR J, KASTNER T, MORAN D, SCHMIDT S & WOOD R. 2019. Agricultural and forestry trade drives large share of tropical deforestation emissions. Glob Environ Change 56: 1-10.), by the bovine leather industry in Europe (Mammadova et al. 2020MAMMADOVA A, MASIERO M & PETTENELLA D. 2020. Embedded deforestation: the case study of the Brazilian-Italian bovine leather trade. Forests 11: 472.), among other economic drivers. These human activities in the Amazon region facilitate the risk of zoonotic spillover events and the spread of infectious diseases in multiple ways (Figure 1, panel b).

Figure 1
Deforestation rate in Brazilian Amazon Forest (Legal Amazon) between 1988 and 2021 and connections between anthropogenic pressures on Amazon Forest and spillover risk. Panel a: between 2004 and 2012, deforestation in the Amazon underwent a significant reduction, partly as a result of the strengthening of policies for controlling illegal activities. From 2014 onwards there have been increases in deforestation rates, with alarming results in 2019, 2020 and 2021, reflecting the weakening of the regulation of illegal activities in the region. Tipping point: the point at which the Amazon Forest stops properly providing its environmental services (e.g., hydrological cycle, maintenance of carbon stocks), losing many rainforest characteristics and enters into a self-perpetuating decline. Data (deforestation rate by year collected on February 1st, 2022) obtained from TerraBrasilis - Programa de Cálculo do Desflorestamento da Amazônia (PRODES), Instituto Nacional de Pesquisas Espaciais (INPE); data under CC BY-SA 4.0 license (INPE 2022INPE - INSTITUTO NACIONAL DE PESQUISAS ESPACIAIS. 2022. TerraBrasilis, Programa de Cálculo do Desflorestamento da Amazônia (PRODES). Taxas de desmatamento - Amazônia Legal - Estados. Available at: http://terrabrasilis.dpi.inpe.br/app/dashboard/deforestation/biomes/legal_amazon/rates [data under Attribution-ShareAlike 4.0 International (CC BY-SA 4.0) license]. Accessed on February 1st, 2022.
http://terrabrasilis.dpi.inpe.br/app/das...
). The graph was plotted using GraphPad Prism. Additional information was obtained from Aguiar et al. (2016)AGUIAR AP ET AL. 2016. Land use change emission scenarios: Anticipating a forest transition process in the Brazilian Amazon. Glob Chang Biol 22: 1821-1840., Lovejoy & Nobre (2018)LOVEJOY TE & NOBRE C. 2018. Amazon tipping point. Sci Adv 4: eaat2340., and Ferrante & Fearnside (2019)FERRANTE L & FEARNSIDE PM. 2019. Brazil’s new president and ‘ruralists’ threaten Amazonia’s environment, traditional peoples and the global climate. Environ Conserv 46: 261-263.. Panel b: deforestation and other anthropogenic pressures on Amazon Forest are closely connected activities. These pressures facilitate spillover events, the emergence of pathogens and the spread of infectious diseases, affecting populations living inside and outside the Amazon region.

A recent study performed in the Amazon rainforest showed that anthropogenic pressure on the natural landscape, specifically forest fragmentation, decreases mosquito diversity and increases the abundance of malaria vectors such as Anopheles (Nyssorhynchus) darlingi mosquitoes (Chaves et al. 2021CHAVES LSM, BERGO ES, CONN JE, LAPORTA GZ, PRIST PR & SALLUM MAM. 2021. Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest. PLoS One 16: e0245087.). Human occupation in forest areas causes loss and fragmentation of habitat. In association with this, there is an increase in the availability of human hosts and a blockage of water flow, thus facilitating the dispersion and proliferation of human-associated mosquito species with medical importance, like An. (Ny.) darlingi (Chaves et al. 2021CHAVES LSM, BERGO ES, CONN JE, LAPORTA GZ, PRIST PR & SALLUM MAM. 2021. Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest. PLoS One 16: e0245087.). These data reinforce the concept that diversity of species is important for the prevention of vector-borne diseases. Furthermore, the same study (Chaves et al. 2021CHAVES LSM, BERGO ES, CONN JE, LAPORTA GZ, PRIST PR & SALLUM MAM. 2021. Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest. PLoS One 16: e0245087.) demonstrates that anthropogenic actions favor the abundance of medically important mosquitoes not only in urban environments but also in tropical forests. In accordance with the information described above, Prist et al. (2022)PRIST PR ET AL. 2022. Roads and forest edges facilitate yellow fever virus dispersion. J Appl Ecol 59: 4-17. recently showed that the construction of roads and the associated increase in forest fragmentation and forest edges facilitate yellow fever virus dispersion. Road construction and associated environmental degradation have been a threat to the Amazon biome from the 1970s to the present (Barni et al. 2015BARNI PE, FEARNSIDE PM & GRAÇA PM. 2015. Simulating deforestation and carbon loss in Amazonia: impacts in Brazil’s Roraima state from reconstructing Highway BR-319 (Manaus-Porto Velho). Environ Manage 55: 259-278., Ferrante & Fearnside 2020aFERRANTE L & FEARNSIDE PM. 2020a. The Amazon’s road to deforestation. Science 369: 634.).

The construction of hydroelectric dams in tropical forest areas can result in population explosions of some mosquito species, as occurred in Brazil’s Tucuruí Dam for Mansonia species (Tadei et al. 1991TADEI WP, SCARPASSA VM & RODRIGUES IB. 1991. Evolução das populações de Anopheles e de Mansonia, na área de influência da Usina Hidrelétrica de Tucuruí (Pará). Ciência e Cultura 43: 639-640., Fearnside 1999FEARNSIDE PM. 1999. Social impacts of Brazil’s Tucuruí Dam. Environ Manage 24: 483-495.) and at the Samuel Dam for Culex species (Fearnside 2005FEARNSIDE PM. 2005. Brazil’s Samuel Dam: Lessons for hydroelectric development policy and the environment in Amazonia. Environ Manage 35: 1-19.). In the first years after dam construction, large areas of the reservoirs were covered by aquatic plants (macrophytes) that provide breeding grounds for Mansonia mosquitoes (Fearnside 2001FEARNSIDE PM. 2001. Environmental impacts of Brazil’s Tucuruí Dam: Unlearned lessons for hydroelectric development in Amazonia. Environ Manage 27: 377-396.). Potential spillover events involving mosquito-borne pathogens are therefore a major concern in the Amazon region.

Hunting and commercialization of wild animals in the Amazon region is very intense, with a bushmeat market reaching up to 6.49 kg per person/year in the central Amazon (quantity varies by Amazon region) (van Vliet et al. 2014VAN VLIET N, QUICENO-MESA MP, CRUZ-ANTIA D, DE AQUINO LJN, MORENO J & NASI R. 2014. The uncovered volumes of bushmeat commercialized in the Amazonian trifrontier between Colombia, Peru & Brazil. Ethnobio Conserv 3: 7., El Bizri et al., 2020EL BIZRI HR ET AL. 2020. Urban wild meat consumption and trade in central Amazonia. Conserv Biol 34: 438-448.). These data suggest that spillover events derived from bushmeat practices are a recurrent possibility in the Amazon region, similar to what happens in other countries with high biodiversity (Ellwanger & Chies 2021ELLWANGER JH & CHIES JAB. 2021. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 44: e20200355.).

In addition to habitat fragmentation, construction of water reservoirs and bushmeat practices, logging, mining, and other exploitative (and often illegal) economic activities in the Amazon region trigger a number of ecological and demographic changes, including migratory flows, habitat loss, unplanned urbanization, prostitution, pollution, climate change, and extreme weather events (Ellwanger et al. 2020ELLWANGER JH ET AL. 2020. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc 92: e20191375.). As discussed earlier in this article, these conditions directly or indirectly favor the occurrence of spillover events and the spread of emerging pathogens. For this reason, deforestation in the Amazon Forest and other anthropogenic activities in the region create the “perfect storm” of infectious diseases in the Amazon region (reviewed in Ellwanger et al. 2020ELLWANGER JH ET AL. 2020. Beyond diversity loss and climate change: Impacts of Amazon deforestation on infectious diseases and public health. An Acad Bras Cienc 92: e20191375.).

The potential emergence of pathogens in the Amazon Forest may affect populations living in the region as well as people living outside the Amazon region. As exemplified by the COVID-19 pandemic, emerging pathogens can spread across the world very easily and quickly. Thus, conserving the Amazon Forest is critical not only to protect biodiversity and associated ecosystem services (e.g., water cycling, carbon stock maintenance); protecting the Amazon biome is a global public health measure (Fearnside 2008FEARNSIDE PM. 2008. Amazon forest maintenance as a source of environmental services. An Acad Bras Cienc 80: 101-114., Ellwanger et al., 2020).

Combating deforestation, mining and other types of land-use change is difficult to achieve, but this is not an impossible task. In Brazil, deforestation in the Amazon region declined greatly (~70%) between 2005 and 2012 (Figure 1, panel a), in part due to government policies (West et al. 2019WEST TAP, BÖRNER J & FEARNSIDE PM. 2019. Climatic benefits from the 2006–2017 avoided deforestation in Amazonian Brazil. Front For Global Change 2: 52., Dobson et al. 2020DOBSON AP ET AL. 2020. Ecology and economics for pandemic prevention. Science 369: 379-381., West & Fearnside 2021WEST TAP & FEARNSIDE PM. 2021. Brazil’s conservation reform and the reduction of deforestation in Amazonia. Land Use Pol 100: 105072.). These policies have ended under Brazil’s presidential administration that took office in January 2019 (Ferrante & Fearnside 2019FERRANTE L & FEARNSIDE PM. 2019. Brazil’s new president and ‘ruralists’ threaten Amazonia’s environment, traditional peoples and the global climate. Environ Conserv 46: 261-263., 2020b), but the potential for controlling deforestation through government policies remains an essential lesson. A recent study (Dobson et al. 2020DOBSON AP ET AL. 2020. Ecology and economics for pandemic prevention. Science 369: 379-381.) pointed out that the costs of mitigating a pandemic such as the COVID-19 are much greater (estimated at US$8.1 to US$15.8 trillion) than the amount that would have to be invested to prevent the main drivers of emerging infectious disease events, estimated at US$17.7 to US$26.9 billion per year. Of note, the prevention costs for 10 years would represent ~2% of the costs of the COVID-19 pandemic (Dobson et al. 2020DOBSON AP ET AL. 2020. Ecology and economics for pandemic prevention. Science 369: 379-381.). In other words, conservation actions protect the environment, limit the spread of infectious diseases, and are cheaper than bearing the burden of emerging infectious disease events. Also, in Brazil, the demarcation of Indigenous lands (Terras Indígenas) is an effective way of limiting the exploitation of natural resources and land-use changes while protecting traditional communities. The contribution of protected areas governed by local communities and Indigenous peoples in the field of biodiversity conservation is widely recognized (Corrigan et al. 2018CORRIGAN C, BINGHAM H, SHI Y, LEWIS E, CHAUVENET A & KINGSTON N. 2018. Quantifying the contribution to biodiversity conservation of protected areas governed by indigenous peoples and local communities. Biol Conserv 227: 403-412.). Considering that Brazil holds most of the territory of the Amazon Forest and has strong political and economic powers, the country needs to take the lead in the conservation of the region, contributing to the reduction of the risks of potential spillover events in the Amazon Forest.

CONCLUSION

This article synthesized the main connections between human-related environmental disturbances, ecological modifications, and increased risk of spillover events (Figure 2), primarily based on examples and models from different world regions. In brief, anthropogenic disturbances in the environment lead to changes in ecological niches, reduction of the dilution effect, increased contact between humans and other animals, changes in the incidence and load of pathogens in animal populations, and alterations in the abiotic factors of landscapes, among other ecological changes. These alterations can increase the risk of spillover events, facilitating new infectious disease outbreaks. In addition to our interpretation of the issues addressed in this paper, we emphasize that other models also explain the relationship between human activity, environmental disturbances, and emerging infectious diseases (e.g., Wolfe et al. 2007WOLFE ND, DUNAVAN CP & DIAMOND J. 2007. Origins of major human infectious diseases. Nature 447: 279-283., Parrish et al. 2008PARRISH CR, HOLMES EC, MORENS DM, PARK EC, BURKE DS, CALISHER CH, LAUGHLIN CA, SAIF LJ & DASZAK P. 2008. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72: 457-470., Karesh et al. 2012KARESH WB ET AL. 2012. Ecology of zoonoses: natural and unnatural histories. Lancet 380: 1936-1945., Morse et al. 2012MORSE SS, MAZET JA, WOOLHOUSE M, PARRISH CR, CARROLL D, KARESH WB, ZAMBRANA-TORRELIO C, LIPKIN WI & DASZAK P. 2012. Prediction and prevention of the next pandemic zoonosis. Lancet 380: 1956-1965., Murray & Daszak 2013MURRAY KA & DASZAK P. 2013. Human ecology in pathogenic landscapes: two hypotheses on how land use change drives viral emergence. Curr Opin Virol 3: 79-83., Faust et al. 2018FAUST CL, MCCALLUM HI, BLOOMFIELD LSP, GOTTDENKER NL, GILLESPIE TR, TORNEY CJ, DOBSON AP & PLOWRIGHT RK. 2018. Pathogen spillover during land conversion. Ecol Lett 21: 471-483., Glidden et al. 2021GLIDDEN CK ET AL. 2021. Human-mediated impacts on biodiversity and the consequences for zoonotic disease spillover. Curr Biol 31: R1342-R1361.). These interpretations are generally not mutually exclusive, and in most cases are complementary. Above all, it is important to keep in mind that generalist explanations for the emergence of infectious diseases will always be incomplete (Jones et al. 2013JONES BA ET AL. 2013. Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci USA 110: 8399-8404.). Each outbreak, epidemic, pandemic, or small-scale zoonotic event has its specific characteristics and triggers that are inherent to the place and context in which it occurred. Considering the specificities of each environment, our review brought a discussion specifically focused on the Amazon rainforest, showing that increasing anthropogenic damage in the region may also increase the risk of zoonotic spillover events and spread of infectious diseases, impacting the Amazon populations and potentially populations elsewhere (Figure 1). Finally, conservation efforts lead to benefits to different global spheres in an integrated manner, as they help to contain anthropic activities on the environment and to reduce the risk of zoonotic spillover events.

Figure 2
Connections between human-related environmental disturbances, ecological modifications and increased risk of zoonotic spillover events. Spillover barriers are factors that facilitate or hinder the transmission of pathogens between different species/populations. They can be biological (e.g., genetic proximity between hosts, immunological and genetic factors), demographic (e.g., overcrowding), ecological (e.g., habitat sharing), cultural (e.g., bushmeat practices), and associated with pathogens (e.g., virulence, survival in the environment). These barriers affect both spillover risk and the outcome of spillover events. More information concerning spillover barriers can be found in Plowright et al. (2017)PLOWRIGHT RK, PARRISH CR, MCCALLUM H, HUDSON PJ, KO AI, GRAHAM AL & LLOYD-SMITH JO. 2017. Pathways to zoonotic spillover. Nat Rev Microbiol 15: 502-510. and Ellwanger & Chies (2021)ELLWANGER JH & CHIES JAB. 2021. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 44: e20200355..

ACKNOWLEDGMENTS

We thank the agencies that funded the authors of this article. Joel Henrique Ellwanger receives a postdoctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Programa Nacional de Pós-Doutorado – PNPD/CAPES, Brazil). Philip Martin Fearnside receives a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (Bolsa de Produtividade em Pesquisa - Nível 1A, CNPq, Brazil). Marina Ziliotto receives a fellowship from CAPES (Brazil). Ana Beatriz Gorini da Veiga receives a research fellowship from CNPq (Bolsa de Produtividade em Pesquisa - Nível 2, CNPq, Brazil) and has research project funded by FAPERGS (Brazil). Gustavo Fioravanti Vieira receives a research fellowship from CNPq (Bolsa de Produtividade em Pesquisa - Nível 2, CNPq, Brazil). Evelise Bach receives a postdoctoral fellowship from CAPES (Brazil). Nícolas Felipe Drumm Müller receives a fellowship from CNPq (Brazil). Gabriel Lopes receives a postdoctoral fellowship from CAPES (Brazil). Bruna Kulmann-Leal receives a doctoral fellowship from CAPES (Brazil). Valéria de Lima Kaminski receives a postdoctoral fellowship from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil). Etiele de Senna Silveira receives a doctoral fellowship from CAPES (Brazil). Fernando Rosado Spilki receives a research fellowship from CNPq (Bolsa de Produtividade em Pesquisa - Nível 1B, CNPq, Brazil) and has research project funded by Financiadora de Inovação e Pesquisa do Ministério da Ciência, Tecnologia e Inovações (Finep-MCTI; Brazil). José Artur Bogo Chies receives a research fellowship from CNPq (Bolsa de Produtividade em Pesquisa - Nível 1A, CNPq, Brazil) and has research project funded by FAPERGS (Brazil) and CAPES (“Prevenção e combate a surtos, endemias, epidemias e pandemias” CAPES AUXPE 686/2020; Brazil).

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Publication Dates

  • Publication in this collection
    19 Sept 2022
  • Date of issue
    2022

History

  • Received
    24 Nov 2021
  • Accepted
    3 Mar 2022
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