Preventing the next
pandemic
Alice C. Hughes
Xishuangbanna Tropical Botanical Garden,
Chinese Academy of Sciences

Zoonoses and risks• 111 recent epidemic disease outbreaks have
zoonotic origins (i.e. HIV-AIDS, Ebola, MERS and
SARS)• 60% of human emerging disease events are causedby zoonotic pathogens, with most (72%)
originating in wildlife.
• Most human pathogens are zoonotic (80% ofviruses)• (50% of bacteria, 40% of fungi, 70% of protozoa
and 95% of helminths)

Route of spillover
1. Direct: Bites, scratches, fluids (i.e. Rabies)
2. Indirect: Contamination (i.e. Marburg)
3. Vector-borne: Bites (i.e. Lyme, Plague)
4. Foodborne/Waterborne: Contamination (i.e.
Hendra, Ebola)A brief
history ofPandemics• Though by nomeans thelargestpandemic
COVID hasalready caused
major global
fatalities

Zoonoses and fatality• Seven coronaviruses (CoVs) are currently known toinfect humans (Andersen et al 2020), four of which
are regularly found in populations in which theycause only mild symptoms (Corman et al 2018)• However, the betacoronaviruses, SARS-CoV-1,
MERS and SARS-CoV-2 are more often fatal• Over 200 novel coronaviruses have been identified
in bats and approximately 35% of the bat virome
sequenced is composed of coronaviruses (Banerjee
et al. 2019)

Interface between humans andexposure• Not all wildlife! –much comes from livestock• Understanding the possibilities for spillover anddrivers behind spillover risk are essential• Here we will discuss why some species are better
reservoirs, the interfaces that cause risk, and how
landscape governance impacts on probable risks

Wildlife reservoirs• Some species can act as reservoir hosts of viruses,
whilst many species have the capacity to act as
reservoirs this is more common in some taxa thanothers• Broadly we can think of such hosts in three maincategories
1. Species which are in close contact with humans
and can spread pathogens (i.e. pets)
2. Species which are good at spreading between
individuals (rodents, civets)
3. Species with immune systems adapted to act as
reservoirs

Immune based adaptations• Special immune adaptations; bats
• Though bats are largely grouped due powered flightthey are deeply divergent• The costs associated with flight have driven selection on
almost every process in bats from the cellular level up• As a consequence bats live upto 10x longer than
expected and provide ideal models to understand thecauses of aging in inferior mammals• Much more work is needed on almost every aspect ofbat ecology, as they remain understudied and highly
cryptic

Where in the world are bats?

Bats Distribution

Cryptic diversity
Ada Chornelia

R. chasenii
R. stheno remain R. affinisR. lepidus
malayanus• R.Onaverage inthis region 50%
of bat species
to be described• Many species are cryptic; and this may be
accelerated by call structure providing a rapidmechanism to generate a pre-mating barrier• Within groups with a particular call structure overR. paradoxolophus
R. luctus
R. siamensis
pearsonii
R. robinsoni
80%of someR.families
may
be undescribed• Better methodologies which measure features moreassociated with how they use space are needed tobetter delineate species without genetic approaches

Endangered ecosystems and species
Rhinolophus pusillus
Rhinolophus trifoliatus
Rhinolophus luctus
Upto 12Rhinolophus affinis• Karst projectnew cryptic
R.affinis clade2-subclade1: China,XTBG,Thailand
bat species

Rhinolophus acuminatus
Rhinolophus pearsonii
R. pearsonii (2 clade)
4 subclade in 2nd clade

R. pusillus clade1 (Malaysia, Thailand)

R. paradoxolophus clade1(China, Vietnam)
R. paradoxolophus clade2 (Laos)
R. rex(Yunnan, China)

Rhinolophus stheno

R.malayanus(2 clade)
3 subclade in 2nd clade
Xtbg malayanus in one clade

Rhinolophus lepidus

Rhinolophus paradoxolophus

R.affinis clade1 (Indonesia)

Rhinolophus malayanus

R. pusillus clade2(Thailand, Laos)

R. pusillus clade1 (Vietnam)-subclade2: Vietnam,Thailand,Malaysia-subclade3: Yunnan

R.stheno (2 clade)
Clade1 (Laos)
Clade2(XTBG,Vietnam,Laos)

R. pusillus clade1(Yunnan, Vietnam)

Rhinolophus marshalli
Rhinolophus siamensis

Noseleaf traits
can be used to
distinguishspecies over
96% of samples

R. siamensis clade1(XTBG, Vietnam, Laos,Myanmar,Vietnam)
R. siamensis clade2(XTBG, Yunnan)

Rhinolophus marshalli
Rhinolophus borneensis
Rhinolophus chasenii
Rhinolophus thomasi
R. thomasi clade1(XTBG, Yunnan)
R. thomasi clade2 (subclade1,2,3)(Laos,China,Vietnam, Yunnan)

Bat immunity & Longevity• Being a bat is stressful!
• Babies born at 25% of mothers weight• Longest gestation for their bodysize• Metabolism which can accelerate to 16x• Long migrations in some species• Many species hibernate

Distance
travelled

Species100-2754275-5009500-7504

750-100051000-1250

3

1250-1500

1

1500-1750

2

1750-2000

3

What makes bats extraordinary?
• Unique senses (i.e. wing mechanoreceptors andacoustic feedback map onto visual cortex)• Incredible longevity• Disease resistance• Highly sophisticated ecolocation
Comparative
metabolomics of aging
in a long-lived bat:
Insights into thephysiology of extreme
longevity, Hope C.
BallShiva levariHealy, K., Guillerme, T., Finlay, S., Kane, A., Kelly, S. B.,
ShariatiLisa
McClean,D., ... &Noelle
Cooper, N. (2014). Ecology and mode-of-life
explainlifespan variationin birds and mammals. Proceedings of
CooperMichel
Alianithe Royal Society B: Biological Sciences, 281(1784), 20140298.

Getting old….
• 2 old mammals…….
• Crumbling bones• Loss of sight• Loss of hearing• Sensitive to illness…..bats can’t afford to get old

Transcriptomic analysis shows genes are upregulated to repair, and may additionally decrease senescence

Longevity synthesis• Whereas other mammals show slow degradationbats utilize multiple pathways to prevent and repair
damage and maintain full function• Bones remain as strong due to increasing release of
Collagen• Different species use different mechanisms, so theseprocesses evolved multiple times

Huang, Z., Whelan, C. V., Foley, N. M., Jebb, D., Touzalin, F., Petit, E. J., ... & Teeling, E. C. (2019). Longitudinal comparative transcriptomics
reveals unique mechanisms underlying extended healthspan in bats. Nature ecology & evolution, 3(7), 1110-1120.

Bats as reservoirs• Bats adaptations high stress life confers bothlongevity and viral resistance• However the end of the evolutionary arms race is a“cold-war” or co-existence meaning that bats canlargely host viruses without showing symptoms andthe virus will largely be dormant within bat cells• Understanding drivers of increased spillover will beessential to attempting to reducing the risk ofspillover into other groupsOther credible reservoirs• Pangolins-Little known, seems capable of hosting, butlittle strong or conclusive evidence, so likely to exist at
low levels in population• Carnivores; civets, raccoon-dogs etc, capacity for
hosting similar viruses. Such viruses may accumulate inliver (and elsewhere) and spread very well in
unhygienic conditions; generally viverrids andmustelids would be good reservoirs• These species act as good intermediaries because they
are often housed in poor conditions, can be laundered,and co-occupy spaces with bats as well as humans

Consuming wildlife-and the risks• Wildlife consumption in Asia has transitioned fromsubsistence to luxury-this is not the case in parts of theworld (i.e. Africa) where wildmeat may still be afundamental part of the diet
• Wildlife is easy to buy across much of Asia, fromluxury high value items to novel but lower price items(i.e squirrels)• Hunting is still very common across rural areas acrossAsia, including bats and other high risk wildlife• In terms of species extinction it is still the major threat
for island bat species, and many species used in
medicineOther regional zoonotic outbreaks• Hendra• Nipah• Plague• ………All of these have caused fatalities in Asia (orAustralasia)• These generally occur though the routes detailed
belowCaptive wildlife• Fur farms• Pets• Medicine• Ornamental• Fashion industry• Food• Many species are actually harvested from the wildcommercially and for personal use; the use of wildlife isworth billions annually; but captive wildlife andranching has particularly high zoonotic risk

Fur-farms• Every year, around 100 million animals are raised and killed
for their fur• Minks -72 million in 2015
• China (2014 stats): 60 million mink, 13 million foxes, 14
million raccoon dogs bred and killed on fur farms• European Union: 42.6 million mink, 2.7 million foxes; 155,000
raccoon dogs; 206,000 chinchilla killed for fur in the EU• Rabbits are also killed for fur (and, in some cases, their meat)in large but unknown numbers (likely hundreds of millions) inEurope and China• In 2015, more than 4 million animals were killed for their pelts
in North America

Biosafety• Rural poverty alleviation schemes in some countries
have focused on breeding these species for meat and fur• As a consequence many wild animals can be mixed inwith captive wildlife, both through wild capture or open
conditions• In rural areas there is also potential for feed
contamination• Unhygienic conditions means urine and feces can flow
between cages; providing ideal conditions for viralspread• Transport also provides ideal conditions for spilloverAdditional issues with farmed
wildlife• Weak legislation and poor health• Wild caught individuals bring in parasites which canspread and spread diseases• Bigger interface for wildlife to be exposed to otherwildlife (sharing caves/roostsites, eating or hunting
other wildlife, exposure to urine etc)
• Poorer regulations with how animals are kept, orveterinary procedures• Issues like otterfarms• According to data released by the Chinese Academy ofEngineering, the wildlife trade in China is valued at $74
billion, employing more than 14 million people, withthe fur industry accounting for 74%

Livestock• Whilst often neglected livestock is a major routecause of many zoonosis• This varies from large industrial scale farms (whichin Asia typically have poorer biosafety, welfare andfewer healthchecks than in the West) to very small
scale operations• Growth hormones and steroids often used toincrease growth rates can weaken immune systems
and may increase viral risk

Livestock• Major outbreaks of Avian flu and Swine flu haveoccurred even this year
• Swine flu “with pandemic potential” has been
increasing over the last decade in Asia, especiallyChina, including new and more virulent strains• Increasing amounts of livestock (especially
Chickens and pigs) are being bred in Asia, with over
½ the worlds pigs in China

Livestock• Multiple routes of transmission• Workers in pig farms often carry swine flu and havesuffered (sometimes fatally)• Smaller operations (i.e those seen in more
mountainous areas) may bring people into very
close contact with livestock-driving huge spilloverrisk• Where wildlife and domestic animals share spaces itenhances spillover risk

Is Asia at a higher risk?
• Asia has well over half the worlds population• With increasing population, industrialization andconsumption of meat it is putting natural resources
under increasing pressure• The interface between livestock and wildlife is also
considerable providing risks of spillover via directcontact, parasites or fluids• However rate of change within Asia is also a majorriskIs Asia at a higher risk?

Life in a changing world
ChangesLightsNight 2016
lights
2013-2016
1992
Growth
1992-2013

1992
2016
% Lights Expansion
Coverage
Yellow-Red: Light 1992, Turquoise: expansion since 1992

Deforestation• Tropical deforestation resulted in a debt of more than 140 forestspecific vertebrates (Rosa et al., 16)• The extinction debt would increase 20th-century extinctions invertebrates by 120%
• Clearance for agriculture accounts for appx 80% deforestation from1980-2000 (Gibbs et al., 10)• Agriculture is the main driver in Asia, whereas political stability &GDP are correlates in SS Africa (Lebois et al., 17)Austin et al., 17

This paper has been cited 108
times despite being invalid
across the tropics-and for ALL
global assessments
There is NO Place for bad
science

Global roads….

Rail_km

%_Pas
1
7
14
30
50

0.1
0.6
1.3
3.0
6.8

1
7
14
30

0.0
1.1
3.0
6.7

50

13.5

Road_km

KM_Rail

No_KBAs
1
7
14
30
50

KM_Road

440
477
580
830
1218
No_KBAs

1
7
14
30

937
1164
1458
1957

%_KBAs
14.9
19.9
27.5
40.2
60.6
%_KBAs

0.2
1.9
4.0
8.6

Number of fragments indifferent size classes
100%

100%
90%

90%
80%

80%

70%

70%

60%
60%

35000

35000
12500

12500

12500

50%
50%

12500
3500
3500
750

40%
40%

750
350
150
350
50
150

30%
30%
20%
20%
10%
10%
0%

0%

1
50

Asia-under threat• Rapid rates of development are quickly destroying
native habitat, which has major implications fordisease risk
• Loss of forests means species are forced to moveinto agricultural areas to obtain enough food• This forces increased interactions between wildlife
and domestic animals, and wildlife and humans• Thus this increases the potential of encounterswhere spillover could occur

Asia-under threat• Hunting, roost loss, habitat loss causes stress• Stress leads to immunosuppression; so animals are
more likely to encounter, suffer and pass on
pathogens• By modifying ecosystems we are exponentially
increasing the risk of spillover• By then bringing that wildlife into captivity andconsumption we are further exacerbating the risk
• These will cause further pandemics-as we can see incases like Ebola

Bats as a casestudy• Bats are frequently a scapegoat for issues with disease
and fruit predation• Mauritius culled over 20,000 P. niger (20% global
population)• Culls have also been used to combat crop damage
elsewhere (i.e. Australia)• Culling programs have failed to reduce rabies
prevalence in vampire bats (Streicker et al. 2012); andfailed attempt to cull Rousettus aegyptiacus in Uganda
resulted in a rise in the prevalence of Marburg virus(Amman et al. 2014). Yet these happen globally

Threats• Bat hunting for consumption as bushmeat andmedicine affects at least 167 species of bats (13 %global bat species)• Half (92/183) extant Pteropodidae species are
hunted• Pteropodids that are hunted are six times more
likely to be Red Listed as threatened: 66 % species(CR, EN, VU, NT), compared to 11 % of species inthe ‘Least Concern’ (LC) category

Threats

RegionTotal#%hunted1146

On Red Not on list Total
Listhunted
97
70
167

249

0

8

8

3.2

South and Southeast Asia 365

43

20

63

17.3

SE
South

333
114

36
8

20
5

56
13

16.8
11.4

Sub-Saharan Africa

249

25

26

51

20.5

West and Central Asia

94

1

0

1

11

14.6

106
0
0providing
00• On many islands
despiteessential
East Asia
3
4item of7 bushmeat
5.4
services bats130are a major
and inEurope
42
0
0
0
0
some
islands
their
teeth
are
the
preferredcurrency
Meso America
177
0
0
0
0
North(i.eAfricaon Malaku)
41
3
1
4
9.8
North
America
49 has 0the highest
00• Southeast
Asia
level
of0hunting forNorth Asia
43
0
0
0
0
Pteropids in 173
terms ofproportionof species
Oceania
25
15
40
23.1
Caribbean islands

South America

https://link.springer.com/chapter/10.1007/978-3-319-25220-9_12

Threats-Mass mortality events
100%

90%

80%

70%

60%

50%

40%

30%

20%

10%

0%
AfricaAsia
Intentional

Australia
BioticAbiotic

Contaminants

EuropeAccidental

Islands
Wind

Viral

N America
White-nose

Unexplained

How are these impacting on behavior, and risk (i.e. contaminants)?

S America

Using bats as indicators• Parasite load and health-higher density,
more transfer• Greater incidence of fighting if
overcrowded• Multiple factors both influence health andpotential risk
• Habitat loss increases novel communities,
and shared parasites and pathogens

Our impacts-our outcomes• Southeast Asia is a hotspot of biodiversity• Yet it is a hotspot of threat-the highest rates ofdeforestation globally, highest rates of mining in
the tropics, and a 5.7% annual loss of karst• Destroying habitat increases interactions andspillover opportunity, and increased stressincreases ability to contract and carry viruses• Unless we protect habitat we will see increased andcontinued emergence of threats• Consumption of wildlife and farming of wild
species is inherently high risk
• Biosafety needs to be improved through allcomponents of meat production and efforts made toprevent wildlife-livestock interactions

Our future-our choices• Covid is a consequence of unsustainable resource use• The difference between Covid and the 100s of otherNovel Zoonoses is that it spreads well, can be spread
asymptomatically-and we now move more
• The difference between now and the 2012 casesconnections• This will not be the last pandemic unless we learnmaintain healthy habitats and populations, reduce
interactions and spillover• Sustainability and tracking systems to identify and stopspread, and reduce use of high risk species is key toreducing furture pandemics

Thank you!
Questions?