SCIENCE ADVANCES | REVIEW

EPIDEMIOLOGY Copyright © 2022

The Authors, some
The infectious disease trap of animal agriculture rights reserved;
exclusive licensee
American Association
Matthew N. Hayek for the Advancement
of Science. No claim to
Infectious diseases originating from animals (zoonotic diseases) have emerged following deforestation from agricul- original U.S. Government
ture. Agriculture can reduce its land use through intensification, i.e., improving resource use efficiency. However, Works. Distributed
intensive management often confines animals and their wastes, which also fosters disease emergence. Therefore, under a Creative
rising demand for animal-sourced foods creates a “trap” of zoonotic disease risks: extensive land use on one hand Commons Attribution
or intensive animal management on the other. Not all intensification poses disease risks; some methods avoid License 4.0 (CC BY).
confinement and improve animal health. However, these “win-win” improvements alone cannot satisfy rising
meat demand, particularly for chicken and pork. Intensive poultry and pig production entails greater antibiotic
use, confinement, and animal populations than beef production. Shifting from beef to chicken consumption mit-
igates climate emissions, but this common strategy neglects zoonotic disease risks. Preventing zoonotic diseases
requires international coordination to reduce the high demand for animal-sourced foods, improve forest conser-
vation governance, and selectively intensify the lowest-producing ruminant animal systems without confinement.

INTRODUCTION: FOOD PRODUCTION DRIVES can reduce greenhouse gas (GHG) emissions and deforestation
ZOONOSIS EMERGENCE

Downloaded from https://www.science.org on March 22, 2024

(15–17), thereby also reducing zoonotic disease risks.
Despite global advances in prosperity, nutrition, and medical care, However, the intensification of animal agricultural production,
infectious diseases are rising in prevalence (1, 2). In the past four in its most common forms, entails the concentration and confine-
decades, emerging infectious diseases have increased at more than ment of animal bodies and their wastes, trading off deforestation for
four times the rate of prior decades (3), most of which have nonhu- other multiple well-documented and potentially cascading risks for
man animal (zoonotic) origins. zoonotic disease emergence. This creates a paradox for intensifica-
Since 1940, an estimated 50% of zoonotic disease emergence has tion that remains unaddressed in the scientific literature: Intensi-
been associated with agriculture (1–3). This estimate, however, is fied animal production, while decreasing marginal land use change
necessarily conservative because only direct agricultural drivers are and GHG emissions, can often increase other zoonotic disease risks.
considered in the epidemiological literature, i.e., within the farm gate. The risks of zoonotic disease emergence from intensive animal ag-
Food systems have environmental impacts before and after the farm riculture could therefore undermine the “sustainable” nature of sus-
gate (4), such as land clearing, food processing, and waste disposal. tainable intensification.
Food systems therefore affect zoonotic disease emergence indirectly. This review examines the zoonotic disease paradox inherent to the
The true contributions of food systems to recently emerged zoonotic sustainable intensification of animal agriculture, exploring whether
diseases remain poorly characterized. food systems can circumvent a “trap” of zoonotic disease risks as
The increase in zoonosis emergence has been partially attributed they further develop. The review first aims to characterize interac-
to ongoing deforestation, particularly in the tropics (2, 5, 6). The tions between intensification and deforestation while examining
largest driver of deforestation is pasture expansion for ruminants ways that they both contribute to zoonotic disease risk. On the basis
(e.g., cattle) with another substantial fraction of forest and savanna of these interactions, this review provides recommendations to re-
clearing for producing feed crops like soy, predominantly fed to duce the likelihood of zoonotic disease emergence, including (i) se-
monogastrics (e.g., pigs and chickens) for domestic and export lectively intensifying the least productive regions, namely, LMICs,
markets (7), with ongoing debate as to the precise proportions (8). without resorting to confinement and other common high-risk in-
Land clearing is expected to continue through 2050 due to further tensive management techniques; (ii) strengthening and improving
increased meat and dairy demand (9–12). Deforestation and con- conservation regulations with effective community governance; and
version to human-dominated systems drive the loss, turnover, and (iii) curbing the high and rising demand for animal-sourced food
homogenization of biodiversity and expose adjacent human com- products. These three strategies are most likely to succeed if imple-
munities to wildlife harboring microbes that can become zoonotic mented in tandem and via regional and international coordination
pathogens with pandemic potential (5). to avoid leakage and rebound effects.
To meet the rising global demand for animal-sourced foods, the
most commonly recommended development strategy in the envi-
ronmental literature is “sustainable intensification,” which refers to INTENSIFICATION—RISKS, OPPORTUNITIES, AND LIMITS
increasing production while managing inputs more judiciously FOR STEMMING ZOONOTIC DISEASE
(13, 14). Experts recommend this strategy for virtually all low- and A number of intensive animal production methods have been im-
middle-income countries (LMICs). By improving resource use effi- plicated in zoonotic disease emergence in the literature (Table 1). The
ciency, sustainable intensification strategies for animal agriculture intensification of animal agriculture through confinement and
industrialization has directly led to the emergence of viruses including
Nipah and H5N1 influenza (“swine flu”) (18) and antibiotic-­r esistant
Department of Environmental Studies, New York University, 285 Mercer St., New York, infectious bacteria including methicillin-resistant Staphylococcus
NY 10012, USA. Email: [email protected] aureus and Escherichia coli (19, 20).

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 1 of 8

SCIENCE ADVANCES | REVIEW

leading to spillover into humans (26). These intensive systems are

Table 1. Intensive animal management strategies, by qualitative risk predominant in developed, industrialized countries but are rapidly
categories and farmed animal types. proliferating in developing regions (27), with encouragement and
Elevated risks
Evidence of zoonotic disease financing from international development organizations including
emergence the World Bank (28).
All farmed animal species Relatively more extensive systems include pastoralism, extensive
Indoor production and confinement (83–85) grazing, and mixed crop-livestock grazing. Extensive systems are
Genetic homogenization (86, 87)
used almost exclusively in developing regions, namely, through the
tropics and semitropics, and among predominantly ruminant live-
Subtherapeutic and growth-
promoting antibiotic use
(19, 20, 25, 74, 88–90) stock (e.g., cows, buffalo, sheep, and goats).
Intensification methods sit on a spectrum, with poles of landless,
Long-distance transportation (91, 92)
industrialized production on the high end and highly extensive pas-
Physiological stress from crowding, toralist grazing on the lowest. The most extensive and inefficient
confinement, and conflicts (e.g., systems have the potential to be improved using “win-win” forms of
(22, 23, 26, 93)
gestation crates, veal crates, and
battery cages) intensification that do not entail a fully industrialized or landless
kind of confined intensification (Table 1), but rather a kind of
Temporary/seasonal and transient
(83, 94) “meeting in the middle” for the lowest, least productive systems to
human labor
improve their performance (15). Thus, intensifying low-production
Concentrated animal wastes (88, 95)
ruminant systems in a selective manner could confer a neutral or
Evidence of reduced land and decreased risk of zoonosis emergence while improving meat and
Neutral or reduced risks
resource needs

Downloaded from https://www.science.org on March 22, 2024

dairy productivity in the most marginal contexts.
All farmed animal species However, there are limitations to this form of intensification.
Improving veterinary care and
(15)
First, the number of animals raised in extensive systems is already
reducing mortality decreasing while being supplanted by highly industrialized/landless
Improving animal husbandry systems throughout developing regions (11, 21). Therefore, there
management (e.g., lower (15, 96) are regional and global limitations to how much additional food
reproductive age) “semi-intensive” systems can provide. Second, shifts downward
Integrating crop and livestock from more highly intensive forms would compromise food produc-
(97–99)
production tion or lead to net agricultural expansion. For instance, eliminating
Ruminant species only feedlot beef cattle systems in the United States by shifting to inten-
Optimizing grazing densities (100, 101) sive grazing would require 64 to 270% greater land use (29), while
Improving forage quality (15, 102) eliminating confined indoor broiler chicken systems by shifting to
minimal pasture would require 43.8 to 60.1% greater land use (30).
Amending and restoring
(15, 102–104) Industrialized systems are often more productive and resource effi-
degraded pastures
cient than semi-intensive methods. Shifting away from industrial-
ized systems therefore entails a GHG and land use penalty or
“sustainability gap” (30). Last, production systems for monogastric
animals, which produce two-thirds of meat globally, lack common
Intensified animal agriculture is often, but not always, character- semi-intensive commercial methods (21). Global production and
ized by a shift toward “landless” or “industrialized” systems (as de- consumption of beef, pork, and chicken are expected to rise by 39,
fined by the United Nations Food and Agriculture Organization). 55, and 58%, respectively, by 2050, with the majority of additional
These systems typically restrict animal movement and are oriented production expected to be achieved through intensification systems
toward rapid weight gain and productivity (21). Monogastric ani- (industrial, in the case of monogastrics) (11). Therefore, additional
mals like pigs and chickens are raised indoors in sheds, each animal food system strategies beyond intensification are needed to safely
with less than twice the space that their bodies occupy, with little or feed a rising and more affluent global population.
no room to express natural behaviors (22, 23). Many beef cattle
spend the latter part of their lives being “finished” or rapidly fat-
tened to reach their final market weights on enriched feeds in feed- INTERACTIONS BETWEEN INTENSIFICATION
lots, with stocking densities for cattle on outdoor feedlots of less AND DEFORESTATION
than 4 m2 per steer/heifer (24). These environments entail physio- Intensification tends to reduce deforestation directly
logical and mental stress, close proximity to each other and wastes, Intensification, which aims to make agricultural production more
and the routine administration of subtherapeutic (infection-­ efficient, is commonly understood to decrease the pressure for de-
preventing) and growth-promoting antibiotics (Table 1). Zoonotic forestation within the environmental literature (13, 31, 32). How-
diseases from aquatic animals are relatively less common and are ever, in many developing tropical regions, both intensification and
predominantly caused by bacteria rather than viruses (25). However, deforestation are occurring simultaneously because they share under-
aquatic animal bacteria are expected to become more prominent lying drivers (i.e., confounding causes): rising populations, incomes,
and potentially infectious among humans as finfish aquaculture and demand for animal-sourced foods (Fig. 1). Because the two are
continues to grow to produce a larger share of aquatic foods globally, visibly correlated, the epidemiological literature on zoonotic disease
and with it are confinement, stress, and antibiotic use, potentially often erroneously links intensification directly to deforestation. A

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 2 of 8

SCIENCE ADVANCES | REVIEW

Meat for stemming zoonotic disease” section) and for mitigating and
demand reversing deforestation (see the previous section). Direct forest
+ + conservation policies and incentives are widely recommended in
environmental and epidemiological literature, e.g., (6, 18, 33). How-
The zoonosis trap ever, known trade-offs and pratfalls exist. First, forest and wildlife
− habitat conservation policies that are not appropriately designed
Intensification Deforestation
and enforced with the involvement of local cultures have backfired
(36, 48–50). Second, conservation may lead to “leakage” effects: Global-
ization allows production to relocate, along with its deforestation,
+ − to countries where conservation policies are insufficiently adopted
Forest or enforced (51, 52). Last, effective forest conservation policies in
conservation
the short term can boost intensification but lead to further defor-
estation in the long term and across wider regions (Fig. 1) (39). These
Fig. 1. Higher incomes are associated with high meat demand that must be
met through intensification or deforestation (or both). Intensification can trigger
effects can vary over space and time, changing with local livelihoods
higher meat demand through lower prices, because meat demand is elastic with and culture, price elasticities for agricultural goods, and how con-
respect to its cost. Intensification and deforestation are highlighted in orange, as both nected production regions are to global markets (37).
have caused recent zoonotic disease emergence and are predicted to continue Conservation policies should be culturally sensitive, rigorously
doing so. Intensification is colored by a gradient to indicate that intensification strat- enforced, and have long-term community buy-in. However, a well-­
egies lie on a gradient of helpful/neutral to harmful with respect to zoonosis risks. crafted conservation policy is still insufficient to spare land from
agricultural pressures; additional land for rising populations and diets

Downloaded from https://www.science.org on March 22, 2024

number of recent high-profile synthesis reports on zoonoses discuss richer in animal-sourced foods must come at the expense of clear-
intensification and deforestation synonymously and interchange- ing native habitats somewhere (11, 53).
ably (6, 33, 34), sometimes directly implicating intensification as
causing the ongoing deforestation, although the environmental lit-
erature predominantly concludes the opposite. Intensification can MEAT DEMAND AT THE NEXUS OF ENVIRONMENTAL CHANGES
lead directly to reduced deforestation in agriculture-forest fron- The largest increases in meat demand and production are occurring
tiers (35, 36). in developing, tropical regions (16). Meat consumption exceeds the
dietary requirements in high-income countries and among increas-
Intensification can indirectly trigger more deforestation ingly urban and middle-class populations of most middle-income
Intensification reduces the marginal resource requirements of animal-­ countries (54–56). As demand rises along with affluence in the
sourced food production; it thus can potentially reduce pressures coming decades in LMICs and high-income countries continue to
for deforestation, a finding that is widely accepted and uncontro- sustain high levels of consumption and exports, additional land
versial. However, after achieving higher efficiency, intensification can clearing and GHG emissions will occur even with ambitious levels
lower the costs of production and sale prices of final goods, induc- of intensification (9, 12).
ing higher demand and production (Fig. 1). This greater demand
can then incentivize additional deforestation (37), negating some or Shifting to plant-rich diets mitigates environmental
all of the original efficiency improvements. This trade-off is known as and zoonotic disease risks
Jevons’ paradox (36, 38, 39) or “rebound effects,” more commonly. Decreasing meat consumption has cobenefits for environmental pro-
The occurrence and magnitude of rebound effects in animal-­ tection and zoonotic disease risks. Global dietary changes are theoret-
sourced food production are difficult and controversial to identify ically sufficient to reverse ongoing deforestation trends, providing 5
because of confounding factors (40–42), leading to ongoing debates to 11 GtCO2 per year of natural carbon removal across 5 to 12 million
(similarly reflected in the “land sparing versus land sharing” debate km2, sequestering approximately a decade worth of anthropogenic
regarding agricultural efficiency). However, some trends and investi- emissions by 2050 in natural vegetation (9, 57–59), which would also
gations are illuminating. In Sweden and the United States, an in- conserve and restore a substantial fraction of lost biodiversity (53, 60).
creased consumption of chicken over the past two decades, due to Shifts to plant-rich diets in high-income countries alone would remove
lower prices, resulted in greater aggregate GHG emissions despite approximately 3 million km2 from agricultural production, including
marginal efficiency gains over the same period (43, 44). In South 1 million km2 of natively forested areas (9, 56).
America, beef intensification has triggered further deforestation To address the emerging zoonotic disease risks of animal agricul-
due to lower production costs (35, 37, 45). Sustainable intensifica- ture, a multipillared approach is required (Fig. 2). This approach in-
tion can thus spur greater environmental impacts, undermining its cludes reducing demand for animal-sourced foods, semi-intensification
sustainable aims (46, 47). Intensification is necessary but insuffi- (see the “Intensification—Risks, opportunities, and limits for stem-
cient to reduce pressures for agriculture expansion and land clear- ming zoonotic disease” section and Table 1), and direct forest con-
ing. Escaping this “damned if we do, damned if we don’t” trap of servation (see the “Effective forest conservation occurs in tandem
intensification (Fig. 1) requires a more multipronged approach. with other strategies” section). Under business-as-usual condi-
tions of rising demand for animal-sourced food, increased land
Effective forest conservation occurs in tandem with clearing is inevitable (57, 61). Reducing demand can therefore avoid
other strategies leakage and rebound effects from focusing exclusively on supply-­
Intensification alone is an insufficient strategy for reducing zoonotic side protections like semi-intensification and forest conservation
disease risk (see the “Intensification—Risks, opportunities, and limits (Figs. 1 and 2).

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 3 of 8

SCIENCE ADVANCES | REVIEW

behavioral, and organizational sciences to change the underlying

motivations and choice environments that drive consumer deci-
Shifts to sions (64, 67). Small successes should also be better communicated to
Semi- decision-makers and ambitiously scaled to large populations with
Inexpensive land plant-rich
intensification clearing—Low
help from community-based advocacy and organizing (68).
incentives to
improve marginal
diets
Rebound effects/ production Fewer cobenefits for
Jevons’ paradox—
Lower costs beget more Ecosystem
emerging economies Differentiating risks across food animals
(low- & lower-middle
consumption &
production
preservation/ income) Shifting production and consumption from beef to poultry is a com-
restoration,
zoonotic disease mon recommendation in the literature. Such shifts would accomplish
Leakage—
Production is
prevention Remaining
demand must be most of the GHG emission mitigation as reducing or eliminating all
displaced
met with
confined/industrial meat (69–71). These recommendations have shaped national cli-
elsewhere production
mate policies: Ethiopia stated plans to shift 30% of their beef pro-
duction to poultry in their 2021 Nationally Determined Contribution
Forest to the United Nations Framework Convention on Climate Change
conservation (72). However, such shifts could maintain or even increase zoonotic
Lack of support for low-
disease risks.
income producers and
animals’ health
Beef has higher land use and is associated with more tropical
deforestation than any other commodity (73). However, monogas-
tric animals, including pigs and chickens, require higher antibiotic
Fig. 2. A three-pillar approach for preventing zoonotic disease emergence and use and higher animal populations to produce the same quantity of

Downloaded from https://www.science.org on March 22, 2024

reducing environmental impacts from animal agriculture (center). Within indi- meat as ruminants such as cattle (Fig. 3). Pigs and chickens are fed
vidual circles and the intersections between the two, limitations of adopting only more than three times the antibiotics than cattle in intensive sys-
one or two strategies are described. tems (74) due to close confinement of animals and their wastes. It
takes three pigs or 170 chickens to produce the meat of one steer.
Intensive methods of monogastric animal production entail more
The zoonotic disease risks of rising animal-sourced food pro- marked confinement, including hen laying and pig gestation sys-
duction and consumption have been underscored by a number of re- tems wherein animals are confined without enough space to spread
cent major environmental epidemiology synthesis reports (6, 33, 62). their wings or turn around. Now, there are more than 33 billion
These reports imply or outright state that high future demand chickens on Earth, representing more than 70% of global avian bio-
for animal-sourced foods is an immutable consequence of rising in- mass (75). Shifts from beef to even greater chicken consumption
comes, treating this trend as fait accompli rather than a decision would entail greater confinement and subtherapeutic antibiotic use
point for policy interventions. This fatalism contradicts behav- for a larger number of animals, elevating multiple risks for zoonotic
ioral science research on reducing the consumption of meat and disease emergence.
other products with harmful public health impacts (e.g., tobacco The precise zoonotic disease risks of individual foods and whole
and sugar). dietary patterns have not previously been quantified. Statistical
To meaningfully flatten the rising curve of animal-sourced foods, analyses are challenging because any predictive metrics would en-
demand-side interventions should be implemented, tested, and tail creating robust models from only a few (but highly costly) zoo-
scaled ambitiously (63). Even gentle changes to dining options and notic disease spillover events and outbreaks that have emerged from
presentation can create large effects (64). Effective interventions agricultural production, often from diverse pathogens and with
range from these subtle “nudges” to more blatant rewards and in- sometimes ambiguous origins. The lack of quantitative disease anal-
centives, as well as stringent regulations and restrictions (16, 55). yses remains a hurdle to assessing the full costs, benefits, and trade-
This spectrum has been described using the Nuffield intervention offs of food system transitions. Despite this, plant-rich diets entail
ladder, with lower rungs of “soft” methods or “carrots” (e.g., guid- cost-saving cobenefits (76, 77), including environmental outcomes,
ance, suggestions, education, and nudging) to higher rungs of in- human nutrition, and animal welfare, which have been quantified
creasingly forceful “hard” interventions or “sticks” at the top (e.g., robustly in previous work (78–80).
taxes and bans) (65).
Countries lack healthy and sustainable food consumption policies
that are comprehensive and synergistic; most countries only have INTERNATIONAL COORDINATION FOR PRIMARY PREVENTION
education policies (e.g., dietary recommendations), with higher rungs OF PANDEMICS
on the Nuffield ladder—including guiding choices through chang- The coronavirus disease 2019 pandemic has increased the vigilance
ing incentives and defaults or disincentivizing options—completely of the global community in identifying and monitoring the poten-
missing (66). Promising local policies and corporate initiatives, mean- tial sources of the next zoonotic disease outbreak. Well-trodden
while, are aiming to guide consumers toward more sustainable op- prevention strategies include suppressing disease in vulnerable ani-
tions using methods of monitoring, goal setting, and verification in mals, monitoring transmission and spillover events of pathogens
combination with multiple soft behavioral interventions to motivate with pandemic potential, and stopping detected outbreaks in do-
change (67). mesticated animals through culling (81). These decade-long pursuits
More targeted dietary change interventions are needed; recom- have only tackled pathogens of concern after some initial emer-
mendations for dietary change policies across most scientific litera- gence or spillover. They do not address root causes of transmission,
ture are general and vague (16, 55). Policies can leverage social, mutation, spillover, and proliferation of emerging infectious zoonotic

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 4 of 8

SCIENCE ADVANCES | REVIEW

Requirements for 1 metric ton of meat production in OECD countries

A Native forest area cleared C Number of animals

3.93 ha

Hectares (10,000 m2)

0.78 ha
0.44 ha

Cattle Pigs Chickens

= 1 animal 592 chickens

B Antibiotics
172 g
148 g
Grams

Downloaded from https://www.science.org on March 22, 2024

45 g
11.3 pigs
3.5 cattle

Cattle Pigs Chickens

Fig. 3. Requirements to produce 1 metric ton of meat (dressed carcass weight), averaged among all OECD countries and weighted by production quantity, base
year 2010. (A) Hectares required for the production of animal feed (crops, pastures, and forages) in natively forested areas, calculated by the author from geospatial
potential vegetation data and agricultural production data in (9) and sources therein. (B) Grams of antibiotics used, derived from (74). (C) Number of animals required for
slaughter, from United Nations FAOSTAT (105). OECD, Organization for Economic Co-operation and Development.

pathogens. The high and increasing demand for animal-­sourced foods 2. J. R. Rohr, C. B. Barrett, D. J. Civitello, M. E. Craft, B. Delius, G. A. DeLeo, P. J. Hudson,
is one such root cause. N. Jouanard, K. H. Nguyen, R. S. Ostfeld, J. V. Remais, G. Riveau, S. H. Sokolow, D. Tilman,
Emerging human infectious diseases and the links to global food production. Nat. Sustain.
Strategies that prevent infectious diseases at their root sources
2, 445–456 (2019).
are called primary prevention (6, 18, 33). This work outlines three 3. K. E. Jones, N. G. Patel, M. A. Levy, A. Storeygard, D. Balk, J. L. Gittleman, P. Daszak, Global
pillars for primary prevention that, when combined, constitute trends in emerging infectious diseases. Nature 451, 990–993 (2008).
stronger protection against zoonotic diseases from animal agricul- 4. F. N. Tubiello, C. Rosenzweig, G. Conchedda, K. Karl, J. Gütschow, P. Xueyao,
ture than any one pillar in isolation (Fig 2). National governments G. Obli-Laryea, N. Wanner, S. Y. Qiu, J. De Barros, A. Flammini, E. Mencos-Contreras,
L. Souza, R. Quadrelli, H. H. Heiðarsdóttir, P. Benoit, M. Hayek, D. Sandalow, Greenhouse
should coordinate their support for a wide range of policies and gas emissions from food systems: Building the evidence base. Environ. Res. Lett. 16,
activities that support these pillars, including expanding veterinary 065007 (2021).
and extension services for improved animal care in LMICs (18), 5. R. Gibb, D. W. Redding, K. Q. Chin, C. A. Donnelly, T. M. Blackburn, T. Newbold, K. E. Jones,
phasing out and banning subtherapeutic and growth-promoting anti­ Zoonotic host diversity increases in human-dominated ecosystems. Nature 584,
398–402 (2020).
biotic uses (82), forming multilateral commitments among countries
6. Workshop Report on Biodiversity and Pandemics of the Intergovernmental Platform on
importing and exporting tropical commodities linked to defor- Biodiversity and Ecosystem Services (IPBES), Bonn, Germany, 27 to 31 July 2020.
estation (73), ambitiously scaling community-based approaches to 7. F. Pendrill, U. M. Persson, J. Godar, T. Kastner, Deforestation displaced: Trade in forest-risk
popularizing plant-rich diets (68), supporting open and public al- commodities and the prospects for a global forest transition. Environ. Res. Lett. 14, 055003
ternative protein research (77), and facilitating sustainable and just (2019).
8. E. Barona, N. Ramankutty, G. Hyman, O. T. Coomes, The role of pasture and soybean
transitions for producers. Commitments should also set quantifi- in deforestation of the Brazilian Amazon. Environ. Res. Lett. 5, 024002 (2010).
able science-based goals and fund ongoing research to monitor and 9. M. N. Hayek, H. Harwatt, W. J. Ripple, N. D. Mueller, The carbon opportunity cost of
accelerate progress. Together, the three pillars of primary preven- animal-sourced food production on land. Nat. Sustain. 4, 21–24 (2021).
tion can guide and empower decision-makers to escape the zoonotic 10. N. Alexandratos, J. Bruinsma, “World agriculture towards 2030/2050: The 2012 revision,”
disease trap of business-as-usual animal agriculture. ESA Working paper, FAO, Rome, June 2012.
11. FAO, “The future of food and agriculture—Alternative pathways to 2050” (Rome, 2018);
www.fao.org/3/I8429EN/i8429en.pdf.
12. D. Tilman, M. Clark, Global diets link environmental sustainability and human health.
REFERENCES AND NOTES Nature 515, 518–522 (2014).
1. E. H. Loh, C. Zambrana-Torrelio, K. J. Olival, T. L. Bogich, C. K. Johnson, J. A. K. Mazet, 13. H. C. J. Godfray, J. R. Beddington, I. R. Crute, L. Haddad, D. Lawrence, J. F. Muir, J. Pretty,
W. Karesh, P. Daszak, Targeting transmission pathways for emerging zoonotic disease S. Robinson, S. M. Thomas, C. Toulmin, Food security: The challenge of feeding 9 billion
surveillance and control. Vector Borne Zoonotic Dis. 15, 432–437 (2015). people. Science 327, 812–818 (2010).

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 5 of 8

SCIENCE ADVANCES | REVIEW

14. P. K. Thornton, M. Herrero, Potential for reduced methane and carbon dioxide emissions 38. E. F. Lambin, P. Meyfroidt, Global land use change, economic globalization, and the
from livestock and pasture management in the tropics. Proc. Natl. Acad. Sci. U.S.A. 107, looming land scarcity. Proc. Natl. Acad. Sci. U.S.A. 108, 3465–3472 (2011).
19667–19672 (2010). 39. P. Meyfroidt, R. R. Chowdhury, A. de Bremond, E. C. Ellis, K.-H. Erb, T. Filatova, R. D. Garrett,
15. P. J. Gerber, H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, J. M. Grove, A. Heinimann, T. Kuemmerle, C. A. Kull, E. F. Lambin, Y. Landon,
G. Tempio, Tackling Climate Change Through Livestock – A Global Assessment of Emissions Y. le Polain de Waroux, P. Messerli, D. Müller, J. Ø. Nielsen, G. D. Peterson,
and Mitigation Opportunities (Food and Agriculture Organization of the United Nations, V. Rodriguez García, M. Schlüter, B. L. Turner II, P. H. Verburg, Middle-range theories
2013). of land system change. Glob. Environ. Chang. 53, 52–67 (2018).
16. IPCC, “Climate change and land: An IPCC special report on climate change, 40. B. T. Phalan, What have we learned from the land sparing-sharing model? MDPI Sustain.
desertification, land degradation, sustainable land management, food security, and 10, 1760 (2018).
greenhouse gas fluxes in terrestrial ecosystems” (Head of TSU (Operations) IT/Web 41. P. Meyfroidt, T. K. Rudel, E. F. Lambin, Forest transitions, trade, and the global displacement
Manager Senior Administrat, 2019); www.ipcc.ch. of land use. Proc. Natl. Acad. Sci. U.S.A. 107, 20917–20922 (2010).
17. J. A. Foley, N. Ramankutty, K. A. Brauman, E. S. Cassidy, J. S. Gerber, M. Johnston, 42. J. R. Stevenson, N. Villoria, D. Byerlee, T. Kelley, M. Maredia, Green Revolution research
N. D. Mueller, C. O’Connell, D. K. Ray, P. C. West, C. Balzer, E. M. Bennett, S. R. Carpenter, saved an estimated 18 to 27 million hectares from being brought into agricultural
J. Hill, C. Monfreda, S. Polasky, J. Rockström, J. Sheehan, S. Siebert, D. Tilman, D. P. M. Zaks, production. Proc. Natl. Acad. Sci. U.S.A. 110, 8363–8368 (2013).
Solutions for a cultivated planet. Nature 478, 337–342 (2011). 43. T. Garnett, E. Röös, D. Little, “Lean, green, mean, obscene…? What is efficiency and is it
18. A. S. Bernstein, A. W. Ando, T. Loch-Temzelides, M. M. Vale, B. V. Li, H. Li, J. Busch, sustainable? Animal production and consumption reconsidered” (Food Climate Research
C. A. Chapman, M. Kinnaird, K. Nowak, M. C. Castro, C. Zambrana-Torrelio, J. A. Ahumada, Network, 2015); https://core.ac.uk/download/pdf/77611459.pdf.
L. Xiao, P. Roehrdanz, L. Kaufman, L. Hannah, P. Daszak, S. L. Pimm, A. P. Dobson, The 44. C. Cederberg, U. Sonesson, M. Henriksson, V. Sund, J. Davis, Greenhouse Gas Emissions
costs and benefits of primary prevention of zoonotic pandemics. Sci. Adv. 8, eabl4183 from Swedish Consumption of Meat, Milk and Eggs 1990 and 2005 (The Swedish Institute
(2022). for Food and Biotechnology, 2009).
19. H. L. Snyder, S. E. Niebuhr, J. S. Dickson, Transfer of methicillin-resistant Staphylococcus 45. F. Müller-Hansen, J. Heitzig, J. F. Donges, M. F. Cardoso, E. L. Dalla-Nora, P. Andrade,
aureus from retail pork products onto food contact surfaces and the potential J. Kurths, K. Thonicke, Can intensification of cattle ranching reduce deforestation
for consumer exposure. J. Food Prot. 76, 2087–2092 (2013). in the Amazon? Insights from an agent-based social-ecological model. Ecol. Econ. 159,
20. C. R. Bergeron, C. Prussing, P. Boerlin, D. Daignault, L. Dutil, R. J. Reid-Smith, G. G. Zhanel, 198–211 (2019).

Downloaded from https://www.science.org on March 22, 2024

A. R. Manges, Chicken as reservoir for extraintestinal pathogenic Escherichia coli 46. J. Loos, D. J. Abson, M. J. Chappell, J. Hanspach, F. Mikulcak, M. Tichit, J. Fischer, Putting
in humans, Canada. Emerg. Infect. Dis. 18, 415–421 (2012). meaning back into “sustainable intensification”. Front. Ecol. Environ. 12, 356–361 (2014).
21. T. Robinson, P. Thorton, G. Franceschini, R. Kruska, F. Chiozza, A. Notenbaert, G. Cecchi, 47. L. V. Rasmussen, B. Coolsaet, A. Martin, O. Mertz, U. Pascual, E. Corbera, N. Dawson,
M. Herrero, M. Epprecht, S. Fritz, L. You, G. Conchedda, L. See, “Global Livestock J. A. Fisher, P. Franks, C. M. Ryan, Social-ecological outcomes of agricultural intensification.
Production Systems” (FAO, 2011); www.fao.org/3/i2414e/i2414e00.htm. Nat. Sustain. 1, 275–282 (2018).
22. K. Proudfoot, G. Habing, Social stress as a cause of diseases in farm animals: Current 48. S. T. Garnett, N. D. Burgess, J. E. Fa, Á. Fernández-Llamazares, Z. Molnár, C. J. Robinson,
knowledge and future directions. Vet. J. 206, 15–21 (2015). J. E. M. Watson, K. K. Zander, B. Austin, E. S. Brondizio, N. F. Collier, T. Duncan, E. Ellis,
23. M. H. Rostagno, Can stress in farm animals increase food safety risk? Foodborne Pathog. Dis. H. Geyle, M. V. Jackson, H. Jonas, P. Malmer, B. McGowan, A. Sivongxay, I. Leiper, A spatial
6, 767–776 (2009). overview of the global importance of Indigenous lands for conservation. Nat. Sustain. 1,
24. M. S. Honeyman, D. L. Maxwell, W. D. Busby, “Effects of stocking density on steer 369–374 (2018).
performance and carcass characteristics in bedded hoop barns” (Iowa State University 49. E. A. Ellis, L. Porter-Bolland, Is community-based forest management more effective than
Animal Industry Report, vol. 9, 2012);https://doi.org/10.31274/ans_air-180814-138. protected areas?: A comparison of land use/land cover change in two neighboring study
25. D. T. Gauthier, Bacterial zoonoses of fishes: A review and appraisal of evidence areas of the Central Yucatan Peninsula, Mexico. For. Ecol. Manage. 256, 1971–1983
for linkages between fish and human infections. Vet. J. 203, 27–35 (2015). (2008).
26. P. T. J. Johnson, A. R. Townsend, C. C. Cleveland, P. M. Glibert, R. W. Howarth, 50. É. Edelblutte, R. Krithivasan, M. N. Hayek, Animal agency in wildlife conservation and
V. J. Mckenzie, E. Rejmankova, M. H. Ward, Linking environmental nutrient enrichment management. Conserv. Biol. 9, e13853 (2022).
and disease emergence in humans and wildlife. Ecol. Appl. 20, 16–29 (2010). 51. R. D. Garrett, L. L. Rausch, Green for gold: Social and ecological tradeoffs influencing
27. Y. Lam, J. P. Fry, K. E. Nachman, Applying an environmental public health lens the sustainability of the Brazilian soy industry. J. Peasant Stud. 43, 461–493 (2016).
to the industrialization of food animal production in ten low- and middle-income 52. Y. le Polain de Waroux, R. D. Garrett, R. Heilmayr, E. F. Lambin, Land-use policies
countries. Global. Health. 15, 40 (2019). and corporate investments in agriculture in the Gran Chaco and Chiquitano. Proc. Natl.
28. A. Wasley, A. Heal, “Revealed: Development banks funding industrial livestock farms Acad. Sci. U.S.A. 113, 4021–4026 (2016).
around the world,” The Guardian, 2 July 2020; www.theguardian.com/environment/2020/ 53. D. Leclère, M. Obersteiner, M. Barrett, S. H. M. Butchart, A. Chaudhary, A. De Palma,
jul/02/revealed-development-banks-funding-industrial-livestock-farms-around-the-world. F. A. J. DeClerck, M. Di Marco, J. C. Doelman, M. Dürauer, R. Freeman, M. Harfoot,
29. M. N. Hayek, R. D. Garrett, Nationwide shift to grass-fed beef requires larger cattle T. Hasegawa, S. Hellweg, J. P. Hilbers, S. L. L. Hill, F. Humpenöder, N. Jennings, T. Krisztin,
population. Environ. Res. Lett. 13, 084005 (2018). G. M. Mace, H. Ohashi, A. Popp, A. Purvis, A. M. Schipper, A. Tabeau, H. Valin, H. van Meijl,
30. I. Chan, B. Franks, M. N. Hayek, The “sustainability gap” of US broiler chicken production: W.-J. van Zeist, P. Visconti, R. Alkemade, R. Almond, G. Bunting, N. D. Burgess, S. E. Cornell,
Trade-offs between welfare, land-use, and consumption. R. Soc. Open Sci. 9, 210478 F. Di Fulvio, S. Ferrier, S. Fritz, S. Fujimori, M. Grooten, T. Harwood, P. Havlík, M. Herrero,
(2022). A. J. Hoskins, M. Jung, T. Kram, H. Lotze-Campen, T. Matsui, C. Meyer, D. Nel, T. Newbold,
31. P. Smith, Delivering food security without increasing pressure on land. Glob. Food Sec. 2, G. Schmidt-Traub, E. Stehfest, B. B. N. Strassburg, D. P. van Vuuren, C. Ware, J. E. M. Watson,
18–23 (2013). W. Wu, L. Young, Bending the curve of terrestrial biodiversity needs an integrated
32. D. Tilman, C. Balzer, J. Hill, B. L. Befort, Global food demand and the sustainable strategy. Nature 585, 551–556 (2020).
intensification of agriculture. Proc. Natl. Acad. Sci. U.S.A. 108, 20260–20264 (2011). 54. C. Rosenzweig, C. Mbow, L. G. Barioni, T. G. Benton, M. Herrero, M. Krishnapillai,
33. UNEP, ILRI, “Preventing the next pandemic—Zoonotic diseases and how to break the E. T. Liwenga, P. Pradhan, M. G. Rivera-Ferre, T. Sapkota, F. N. Tubiello, Y. Xu,
chain of transmission” (Nairobi, Kenya, 2020); www.unenvironment.org/resources/report/ E. Mencos Contreras, J. Portugal-Pereira, Climate change responses benefit from a global
preventing-future-zoonotic-disease-outbreaks-protecting-environment-animals-and. food system approach. Nat. Food. 1, 94–97 (2020).
34. B. A. Jones, D. Grace, R. Kock, S. Alonso, J. Rushton, M. Y. Said, D. McKeever, F. Mutua, 55. W. Willett, J. Rockström, B. Loken, M. Springmann, T. Lang, S. Vermeulen, T. Garnett,
J. Young, J. McDermott, D. U. Pfeiffer, Zoonosis emergence linked to agricultural D. Tilman, F. DeClerck, A. Wood, M. Jonell, M. Clark, L. Gordon, J. Fanzo, C. Hawkes,
intensification and environmental change. Proc. Natl. Acad. Sci. U.S.A. 110, 8399–8404 (2013). R. Zurayk, J. A. Rivera, W. De Vries, L. Sibanda, A. Afshin, A. Chaudhary, M. Herrero,
35. R. D. Garrett, I. Koh, E. F. Lambin, Y. le Polain de Waroux, J. H. Kastens, J. C. Brown, R. Agustina, F. Branca, A. Lartey, S. Fan, B. Crona, E. Fox, V. Bignet, M. Troell, T. Lindahl,
Intensification in agriculture-forest frontiers: Land use responses to development S. Singh, S. E. Cornell, K. S. Reddy, S. Narain, S. Nishtar, C. J. L. Murray, Food in the
and conservation policies in Brazil. Glob. Environ. Chang. 53, 233–243 (2018). Anthropocene: The EAT–Lancet Commission on healthy diets from sustainable food
36. M. G. Ceddia, N. O. Bardsley, S. Gomez-Y-Paloma, S. Sedlacek, Governance, agricultural systems. Lancet 6736, 3–49 (2019).
intensification, and land sparing in tropical South America. Proc. Natl. Acad. Sci. U.S.A. 56. Z. Sun, L. Scherer, A. Tukker, S. A. Spawn-Lee, M. Bruckner, H. K. Gibbs, P. Behrens, Dietary
111, 7242–7247 (2014). change in high-income nations alone can lead to substantial double climate dividend.
37. U. Kreidenweis, F. Humpenöder, L. Kehoe, T. Kuemmerle, B. L. Bodirsky, H. Lotze-Campen, Nat. Food. 3, 29–37 (2022).
A. Popp, Pasture intensification is insufficient to relieve pressure on conservation priority 57. K.-H. Erb, C. Lauk, T. Kastner, A. Mayer, M. C. Theurl, H. Haberl, Exploring the biophysical
areas in open agricultural markets. Glob. Chang. Biol. 24, 3199–3213 (2018). option space for feeding the world without deforestation. Nat. Commun. 7, 11382 (2016).

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 6 of 8

SCIENCE ADVANCES | REVIEW

58. J. Poore, T. Nemecek, Reducing food’s environmental impacts through producers and 84. J. H. Leibler, J. Otte, D. Roland-Holst, D. U. Pfeiffer, R. Soares Magalhaes, J. Rushton,
consumers. Science 360, 987–992 (2018). J. P. Graham, E. K. Silbergeld, Industrial food animal production and global health
59. T. D. Searchinger, S. Wirsenius, T. Beringer, P. Dumas, Assessing the efficiency of changes risks: Exploring the ecosystems and economics of avian influenza. Ecohealth 6, 58–70
in land use for mitigating climate change. Nature 564, 249–253 (2018). (2009).
60. B. B. N. Strassburg, A. Iribarrem, H. L. Beyer, C. L. Cordeiro, R. Crouzeilles, C. C. Jakovac, 85. S. Srinivasan, L. Easterling, B. Rimal, X. M. Niu, A. J. K. Conlan, P. Dudas, V. Kapur,
A. B. Junqueira, E. Lacerda, A. E. Latawiec, A. Balmford, T. M. Brooks, S. H. M. Butchart, Prevalence of bovine tuberculosis in India: A systematic review and meta-analysis.
R. L. Chazdon, K.-H. Erb, P. Brancalion, G. Buchanan, D. Cooper, S. Díaz, P. F. Donald, Transbound. Emerg. Dis. 65, 1627–1640 (2018).
V. Kapos, D. Leclère, L. Miles, M. Obersteiner, C. Plutzar, C. A. de M Scaramuzza, 86. A. J. Springbett, K. MacKenzie, J. A. Woolliams, S. C. Bishop, The contribution of genetic
F. R. Scarano, P. Visconti, Global priority areas for ecosystem restoration. Nature 586, diversity to the spread of infectious diseases in livestock populations. Genetics 165,
724–729 (2020). 1465–1474 (2003).
61. M. N. Hayek, M. Longo, J. Wu, M. N. Smith, N. Restrepo-Coupe, R. Tapajós, R. da Silva, 87. R. Alders, J. A. Awuni, B. Bagnol, P. Farrell, N. De Haan, Impact of avian influenza on village
D. R. Fitzjarrald, P. B. Camargo, L. R. Hutyra, L. F. Alves, B. Daube, J. W. Munger, poultry production globally. Ecohealth 11, 63–72 (2014).
K. T. Wiedemann, S. R. Saleska, S. C. Wofsy, Carbon exchange in an Amazon forest: 88. J. C. Chee-Sanford, R. I. Aminov, I. J. Krapac, N. Garrigues-Jeanjean, R. I. Mackie,
From hours to years. Biogeosciences. 15, 4833–4848 (2018). Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater
62. UN Environment, UNEP Frontiers 2016 Report: Emerging Issues of Environmental Concern underlying two swine production facilities. Appl. Environ. Microbiol. 67, 1494–1502
(United Nations Environmental Programme, 2016). (2001).
63. H. Harwatt, W. J. Ripple, A. Chaudhary, M. G. Betts, M. N. Hayek, Scientists call for renewed 89. N. Kanwar, H. M. Scott, B. Norby, G. H. Loneragan, J. Vinasco, M. McGowan, J. L. Cottell,
Paris pledges to transform agriculture. Lancet Planet. Health 4, e9–e10 (2020). M. M. Chengappa, J. Bai, P. Boerlin, Effects of ceftiofur and chlortetracycline treatment
64. S. Attwood, P. Voorheis, C. Mercer, K. Davies, D. Vennard, Playbook for Guiding Diners strategies on antimicrobial susceptibility and on tet(A), tet(B), and blaCMY-2 resistance
Toward Plant-Rich Dishes in Food Service (World Resources Institute, 2019). genes among E. coli isolated from the feces of feedlot cattle. PLOS ONE 8, e80575
65. S. S. Morris, S. Barquera, A. Sutrisna, D. Izwardy, R. Kupka, Perspective: Interventions (2013).
to improve the diets of children and adolescents. Glob. Food Sec. 27, 100379 (2020). 90. A. D. McEachran, B. R. Blackwell, J. D. Hanson, K. J. Wooten, G. D. Mayer, S. B. Cox,
66. D. Mason-D’Croz, J. R. Bogard, T. B. Sulser, N. Cenacchi, S. Dunston, M. Herrero, K. Wiebe, P. N. Smith, Antibiotics, bacteria, and antibiotic resistance genes: Aerial transport
Gaps between fruit and vegetable production, demand, and recommended from cattle feed yards via particulate matter. Environ. Health Perspect. 123, 337–343

Downloaded from https://www.science.org on March 22, 2024

consumption at global and national levels: An integrated modelling study. Lancet Planet. (2015).
Health 3, e318–e329 (2019). 91. N. Ramesh, S. W. Joseph, L. E. Carr, L. W. Douglass, F. W. Wheaton, Serial disinfection
67. R. Waite, D. Vennard, G. Pozzi, “Tracking progress toward the cool food pledge: Setting with heat and chlorine to reduce microorganism populations on poultry transport
climate targets, tracking metrics, using the cool food calculator, and related guidance for containers. J. Food Prot. 66, 793–797 (2003).
pledge signatories” (World Resources Institute, 2019);www.coolfoodpledge.org. 92. A. Di Nardo, N. J. Knowles, D. J. Paton, Combining livestock trade patterns with
68. P. Puska, J. Tuomilehto, J. T. Salonen, A. Nissinen, Ten years of the North Karelia project phylogenetics to help understand the spread of foot and mouth disease in sub-Saharan
of prevention of ischaemic heart disease. Cas. Lek. Cesk. 218, 66–71 (1985). Africa, the Middle East and Southeast Asia. Rev. Sci. Tech. 30, 63–85 (2011).
69. A. Shepon, G. Eshel, E. Noor, R. Milo, Energy and protein feed-to-food conversion 93. H. El-Lethey, B. Huber-Eicher, T. W. Jungi, Exploration of stress-induced
efficiencies in the US and potential food security gains from dietary changes. Environ. Res. Lett. immunosuppression in chickens reveals both stress-resistant and stress-susceptible
11, 105002 (2016). antigen responses. Vet. Immunol. Immunopathol. 95, 91–101 (2003).
70. D. Bryngelsson, F. Hedenus, D. J. A. Johansson, C. Azar, S. Wirsenius, How do dietary choices 94. C. Millman, R. Christley, D. Rigby, D. Dennis, S. J. O’Brien, N. Williams, “Catch 22”:
influence the energy-system cost of stabilizing the climate? Energies 10, 182 (2017). Biosecurity awareness, interpretation and practice amongst poultry catchers. Prev. Vet. Med.
71. DGAC, “Scientific Report of the 2015 Dietary Guidelines Advisory Committee: Advisory 141, 22–32 (2017).
Report to the Secretary of Health and Human Services and the Secretary of Agriculture” 95. Y. Zheng, S. Ge, J. Zhang, Q. Guo, M. H. Ng, F. Wang, N. Xia, Q. Jiang, Swine as a principal
(U.S. Department of Agriculture, Agricultural Research Service, 2015);http://health.gov/ reservoir of hepatitis E virus that infects humans in Eastern China. J Infect Dis 193,
dietaryguidelines/2015-scientific-report/. 1643–1649 (2006).
72. FDRE, “Updated nationally determined contribution” (Federal Democratic Republic of 96. A. N. Hristov, J. Oh, C. Lee, R. Meinen, F. Montes, T. Ott, J. Firkins, A. Rotz, C. Dell,
Ethiopia, 2021). A. Adesogan, W. Yang, J. Tricarico, E. Kebreab, G. Waghorn, J. Dijkstra, S. Oosting,
73. S. Henders, U. M. Persson, T. Kastner, Trading forests: Land-use change and carbon Mitigation of Greenhouse Gas Emissions in Livestock Production - A Review of Technical
emissions embodied in production and exports of forest-risk commodities. Environ. Res. Lett. Options for Non-CO2 Emissions (FAO, 2013);https://dialnet.unirioja.es/servlet/
10, 125012 (2015). libro?codigo=317825.
74. T. P. Van Boeckel, C. Brower, M. Gilbert, B. T. Grenfell, S. A. Levin, T. P. Robinson, A. Teillant, 97. R. D. Garrett, M. T. Niles, J. D. B. Gil, A. Gaudin, R. Chaplin-Kramer, A. Assmann,
R. Laxminarayan, Global trends in antimicrobial use in food animals. Proc. Natl. Acad. Sci. U.S.A. T. S. Assmann, K. Brewer, P. C. de Faccio Carvalho, O. Cortner, R. Dynes, K. Garbach,
112, 5649–5654 (2015). E. Kebreab, N. Mueller, C. Peterson, J. C. Reis, V. Snow, J. Valentim, Social and ecological
75. Y. M. Bar-On, R. Phillips, R. Milo, P. G. Falkowski, The biomass distribution on Earth. Proc. Natl. analysis of commercial integrated crop livestock systems: Current knowledge
Acad. Sci. U.S.A. 115, 6506–6511 (2018). and remaining uncertainty. Agr. Syst. 155, 136–146 (2017).
76. R. Espinosa, D. Tago, N. Treich, Infectious diseases and meat production. Environ. Resource 98. J. C. Salton, F. M. Mercante, M. Tomazi, J. A. Zanatta, G. Concenço, W. M. Silva, M. Retore,
Econ. 76, 1019–1044 (2020). Integrated crop-livestock system in tropical Brazil: Toward a sustainable production
77. J. Bernstein, J. Dutkiewicz, A public health ethics case for mitigating zoonotic disease risk system. Agric. Ecosyst. Environ. 190, 70–79 (2014).
in food production. Food Ethics. 6, 9 (2021). 99. G. Lemaire, A. Franzluebbers, P. C. de Faccio Carvalho, B. Dedieu, Integrated
78. M. Springmann, H. C. J. Godfray, M. Rayner, P. Scarborough, Analysis and valuation of the crop-livestock systems: Strategies to achieve synergy between agricultural production
health and climate change cobenefits of dietary change. Proc. Natl. Acad. Sci. U.S.A. 113, and environmental quality. Agric. Ecosyst. Environ. 190, 4–8 (2014).
4146–4151 (2016). 100. M. Bogaerts, L. Cirhigiri, I. Robinson, M. Rodkin, R. Hajjar, C. Costa Junior, P. Newton,
79. L. Scherer, P. Behrens, A. Tukker, Opportunity for a dietary win-win-win in nutrition, Climate change mitigation through intensified pasture management: Estimating
environment, and animal welfare. One Earth 1, 349–360 (2019). greenhouse gas emissions on cattle farms in the Brazilian Amazon. J. Clean. Prod. 162,
80. F. Biermann, T. Hickmann, C.-A. Sénit, M. Beisheim, S. Bernstein, P. Chasek, L. Grob, 1539–1550 (2017).
R. E. Kim, L. J. Kotzé, M. Nilsson, A. Ordóñez Llanos, C. Okereke, P. Pradhan, R. Raven, 101. J. Piipponen, M. Jalava, J. de Leeuw, A. Rizayeva, C. Godde, G. Cramer, M. Herrero,
Y. Sun, M. J. Vijge, D. van Vuuren, B. Wicke, Scientific evidence on the political impact M. Kummu, Global trends in grassland carrying capacity and relative stocking density
of the Sustainable Development Goals. Nat. Sustain. 5, 795–800 (2022). of livestock. Glob. Chang. Biol. 28, 3902–3919 (2022).
81. C. van Staden, COVID-19 and the crisis of national development. Nat. Hum. Behav. 4, 102. M. Herrero, B. Henderson, P. Havlík, P. K. Thornton, R. T. Conant, P. Smith, S. Wirsenius,
443–444 (2020). A. N. Hristov, P. Gerber, M. Gill, K. Butterbach-Bahl, H. Valin, T. Garnett, E. Stehfest,
82. T. P. Van Boeckel, E. E. Glennon, D. Chen, M. Gilbert, T. P. Robinson, B. T. Grenfell, Greenhouse gas mitigation potentials in the livestock sector. Nat. Clim. Chang. 6, 452–461
S. A. Levin, S. Bonhoeffer, R. Laxminarayan, Reducing antimicrobial use in food animals. (2016).
Science 357, 1350–1352 (2017). 103. D. F. Cusack, C. E. Kazanski, A. Hedgpeth, K. Chow, A. L. Cordeiro, J. Karpman, R. Ryals,
83. J. P. Graham, J. H. Leibler, L. B. Price, J. M. Otte, D. U. Pfeiffer, T. Tiensin, E. K. Silbergeld, Reducing climate impacts of beef production: A synthesis of life cycle assessments
The animal-human interface and infectious disease in industrial food animal production: across management systems and global regions. Glob. Chang. Biol. 27, 1721–1736
Rethinking biosecurity and biocontainment. Public Health Rep. 123, 282–299 (2008). (2021).

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 7 of 8

SCIENCE ADVANCES | REVIEW

104. A. Bragança, P. Newton, A. Cohn, J. Assunção, C. Camboim, D. de Faveri, B. Farinelli, revisions, performed the data analysis, and created and designed all figures contained
V. M. E. Perego, M. Tavares, J. Resende, S. de Medeiros, T. D. Searchinger, Extension therein. Competing interests: The author declares that he has no competing interests.
services can promote pasture restoration: Evidence from Brazil’s low carbon agriculture Data and materials availability: All data needed to evaluate the conclusions in the paper are
plan. Proc. Natl. Acad. Sci. U.S.A. 119, e2114913119 (2022). present in the paper, with the exception of data in Fig. 3, the online sources of which are cited
105. FAOSTAT, UN FAO, www.fao.org/faostat/en/#data/QCL [accessed 29 August 2022]. in the caption.

Acknowledgments: I thank B. Franks, J. Sebo, D. Jamieson, W. Alonso, and N. Mueller as well Submitted 26 June 2022
as the anonymous reviewers for helpful input regarding the contents and direction of this Accepted 15 September 2022
article. Funding: The authors acknowledge that they received no funding in support of this Published 2 November 2022
research. Author contributions: M.N.H. authored this report, including all drafts and 10.1126/sciadv.add6681

Downloaded from https://www.science.org on March 22, 2024

Hayek, Sci. Adv. 8, eadd6681 (2022) 2 November 2022 8 of 8