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Science Adj1190

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Science Adj1190

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INSIGHTS

PERSPECTIVES

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CONSERVATION

Global influenza threatens conservation


How avian influenza virus will continue to spread and circulate among wildlife is unclear

By Jonathan Runstadler disruption to ecosystem health adversely af- tion in Northern Europe and the Americas. .
fects human well-being, overcoming a risk The virus is a high concern for species

T
he highly pathogenic avian influenza such as HPAIV requires a paradigm for in- of conservation interest, such as Caspian
virus (HPAIV) known as H5 HPAI is fectious disease that prioritizes the health, terns or the common loon (4). Infections
now in Europe, Asia, Africa, North sustainability, and preservation of natural in avian hosts and marine mammals in Ant-
America, South America, and Ant- ecosystems and resources. arctica are sparking fears of ecological di-
arctica, infecting domestic and wild Although it remains a threat to domestic saster among seasonal breeding penguins.
avian and mammalian populations. fowl, the H5 HPAI clade 2.3.4.4b continues Restoration of the California condor, which
Certainly, much attention has been focused to dominate the global spread of HPAIV, required decades of effort and resources, is
on its spread to humans, and the risk of which is indicative of a virus that is both now under threat and the feasibility of field
its transmission between people remains a more transmissible and virulent to many vaccination is being explored in the west-
major public health concern. Less discussed wild hosts. Last year, the Convention on the ern United States In addition, the deaths of
is the virus spilling over to wildlife that is Conservation of Migratory Species of Wild thousands of birds in seabird colonies such
endangered or threatened (1, 2). Second- Animals and the Food and Agriculture Or- as the northern gannet and roseate tern are
ary and indirect effects of this spread are ganization of the United Nations convened now a concern in the United Kingdom. .
unpredictable given knowledge gaps in the a scientific task force on avian influenza and The reasons for such rapid global spread
ecology and evolution of influenza in natu- wild birds (2) and reported outbreaks across of HPAIV are poorly understood but are
PHOTO: MICHAEL DURHAM/MINDEN

ral populations (3). The lack of effective the globe in diverse avian taxa, from raptors likely related to the high capacity for mu-
control measures may result in high fatali- to seabirds, including several endangered tation in this RNA virus, coupled with ad-
ties to many wildlife species and the de- bird populations. HPAIV has infected over aptation and the relative fitness of current
struction of major ecosystems. Given that 500 species of wild birds so far, which is, circulating strains. These factors collec-
over space and time, unprecedented. Many tively allow persistence in, and transmis-
outbreaks of the 2.3.4.4b clade since 2020 sion between, new and accidental hosts.
Department of Infectious Disease and Global Health,
Cummings School of Veterinary Medicine, Tufts University, indicate that the virus is now causing year- High rates of carriage in mobile species
North Grafton, MA, USA. Email: [email protected] round, rather than seasonal, waves of infec- such as gulls, which can migrate for thou-

618 8 NOVEMBER 2024 • VOL 386 ISSUE 6722 science.org SCIENCE


Rapid and global spread of the highly pathogenic quently defined as a “fitter” virus than earlier large changes in species composition, par-
avian influenza virus threatens conservation efforts circulating clades. However, what constitutes ticularly of keystone predators, through in-
for species such as the California condor. virus fitness beyond genome replicative is not fectious disease outbreaks open the door for
clear. Is 2.3.4.4b more fit because the virus invasive species. This could disrupt preda-
sands of kilometers and cross open oceans, itself has improved its ability to infect cells tor-prey relationships or deplete biodiversity,
may also promote the spread and evolution across a wide variety of hosts or because its which has implications for economic, aes-
of the 2.3.4.4b lineage (5, 6). Widespread re- primary wild reservoir has shifted to provide thetic, and functional aspects of ecosystem
assortment of genomic RNA segments and enhanced ecological interfaces with multiple services. Such concern is high for fragile eco-
continued viral drift have been documented new species? The role of the environment, of systems such as the Antarctic ice shelf and its
as the virus spreads across the North and changes in viral function, and of interaction susceptible penguin populations.
South American continents (4, 7). with host factors that influence susceptibil- What can be done in the face of such
Concurrently, spillover of viral infection ity to infection are all possibilities in what is uncertainty? Vastly improved surveillance
has been observed in mammalian hosts likely a complex explanation involving mo- and monitoring of wildlife populations to
(8–10). Most of these infections have been lecular, cellular, organismal, and ecological understand infection patterns, virus ecol-
reported in carnivorous predatory or scaven- contributors to clade 2.3.4.4b’s explosive cir- ogy, virus evolution, and host immunity
ger hosts, such as the red fox and wild cat culation in the past 2 years. are sorely needed. Worldwide, surveillance
species. However, the range of affected spe- How HPAIV will continue to spread and efforts are spotty, unreliable, and largely
cies is broad, extending to marine mammals, circulate also is obscure. The mechanisms only targeted for specific opportunistic
and multiple mass mortality events within supporting shifts in the epidemiological species. Comprehensive multiyear moni-
South American seal and sea lion popula- patterns of its transmission, from seasonal toring could provide the foundation for
tions suggest that host-to-host transmission outbreaks to endemic circulation, are un- better gauging impacts on wildlife, as well

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may play an important role in epidemic known. The current year-round presence of as on human hosts (13). Framing this ap-
spread in these hosts. Furthermore, indica- influenza virus in areas of Northern Europe proach through a “one health” lens that
tions of neuroinvasive pathology (infection of and the Americas has produced unexpected considers the interconnected nature of
the central nervous system) in wildlife spe- geography and timing of wildlife outbreaks. animal, environmental, and human health
cies are particularly concerning for conserva- For example, marine mammals are assumed may increase the urgency for more com-
tion (10–12). This can cause conditions such to have been infected by HPAIV spillover prehensive surveillance efforts.
as paralysis and disorientation that affect from seabird hosts with which they have di- There has been a long-running debate
survival. Although some influenza strains are rect and close contact. In the northeastern in conservation about whether to interfere
occasionally associated with clinical signs of United States, however, epidemic mortality with wildlife well-being through human
neuroinvasive pathology, it is unusual to see of gray and harbor seal populations in the action or let nature take its course in the
such widespread neuropathology in diverse summer of 2022 did not reoccur in 2023 or face of a threat. But what if the course of
avian and mammalian species, including 2024 to date despite the continued regional nature has been directed by human activi-
seabirds like the gannet and scavengers such virus appearance in avian populations such ties, however indirect? Do we have a moral
as raccoons. It is likely that neuroinvasion is as gulls and geese or ducks. By contrast, and ethical responsibility to intercede?
contributing to the unprecedented high wild- massive outbreaks that caused the deaths of Recognizing and taking responsibility
life mortality being reported (>10,000 avian thousands of marine mammals, including for humanity’s role in disease impacts on
and >400 mammalian cases to the US De- multiple species, occurred in the Southern wildlife through consideration of the inter-
partment of Agriculture). Hemisphere in Chile and Peru and extended faces and connections between human, ani-
The ability of wildlife to recover from to Antarctica. The impact of prior infec- mal, and environmental health should be a
HPAIV infection may depend on several fac- tion with other influenza virus strains, or shared goal. j
tors relating to the host species’ natural his- of strains circulating at the same time as a
REFERENCES AND NOT ES
tory, which are not well understood in most HPAIV, on the susceptibility of a host spe-
1. O. Duriez et al., Curr. Biol. 33, 3766 (2023).
cases. In species with substantial parental cies to 2.3.4.4b (or further evolved versions) 2. E. Office, J. Disaster Res. 2, 115 (2007).
investment and long-lived adults (such as is also unknown. 3. S. R. Hopkins et al., Lancet Planet. Health 6, e694
seals), high adult mortality may mean that it Infectious disease in wildlife has histori- (2022).
4. J. A. Harvey, J. M. Mullinax, M. C. Runge, D. J. Prosser,
will take years for a species to recover from cally been approached as a problem modeled Biol. Conserv. 282, 110041 (2023).
an epidemic. By contrast, for species that by epidemiological principles of contact dis- 5. D. J. Prosser, C. S. Teitelbaum, S. Yin, N. J. Hill, X. Xiao,
invest relatively less in offspring and expe- ease transmission. However, a more complex Nat. Microbiol. 8, 2223 (2023).
6. J. Loeb, Vet. Rec. 193, 340 (2023).
rience reproductive booms in response to ecological sphere is needed that includes the 7. S. Youk et al., Virology 587, 109860 (2023).
resource availability (such as many rodent effects of climate change, habitat destruction, 8. J. Loeb, Vet. Rec. 192, 143 (2023).
species), recovery may be relatively rapid. resource depletion, and host species physi- 9. I. V. Chestakova et al., Emerg. Microbes Infect. 12,
2270068 (2023).
Despite new data on the spread and genetic ology and behavior. Thus, the trajectory of 10. E. J. Elsmo et al., Emerg. Infect. Dis. 29, 2451 (2023).
diversification of the 2.3.4.4b lineage, this HPAIV cannot be reliably derived from cur- 11. L. Bauer, F. F. W. Benavides, E. J. B. Veldhuis Kroeze, E. de
panzootic virus has highlighted substantial rent scientific understanding, and therefore Wit, D. van Riel, Trends Neurosci. 46, 953 (2023).
12. B. D. Cronk et al., Emerg. Microbes Infect. 12, 2249554
gaps in understanding infectious disease in preparing guidance for groups working on
(2023).
wildlife populations and the inability of hu- species conservation is challenging. A ma- 13. A. Barbachano-Guerrero, D. R. Perez, S. L. Sawyer, eLife
mans to anticipate or mitigate downstream jor problem is uncertainty about short- and 12, e86051 (2023).
effects. The notion that clade 2.3.4.4b will long-term ecological impacts of epidemic and
ACKNOWL EDGMENTS
continue to circulate and evolve in wildlife recurring HPAIV infection. Furthermore, the
J.R. acknowledges support from the US National Institutes
species is somewhat speculative because it emergence and global spread of HPAIV may of Health Centers of Excellence for Influenza Research and
is based on several assumptions that remain be a sign of large-scale changes in ecosystem Response program.
untested and poorly understood. For exam- function caused by human activity. In turn,
ple, the currently circulating lineage is fre- and in a potential positive feedback loop, 10.1126/science.adj1190

SCIENCE science.org 8 NOVEMBER 2024 • VOL 386 ISSUE 6722 619

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