1 Pandemics and biodiversity: applying lessons learned to conservation in the post-COVID- 2 19 era 3 4 Authors: Jiajia Liu1, Zhijun Ma1, Shilu Zheng2, Xingfeng Si3, Marc W. Cadotte4* 5 6 Affiliations: 7 1Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, 8 Coastal Ecosystems Research Station of the Yangtze River Estuary, Institute of Biodiversity 9 Science, School of Life Sciences, Fudan University, Shanghai, 200438, China 10 11 2School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, 12 Crawley, WA 6009, Australia 13 14 3Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, School of 15 Ecological and Environmental Sciences, East China Normal University, Shanghai, 200241, 16 China 17 18 4Department of Biological Sciences, University of Toronto, Scarborough, Toronto, ON, Canada 19
20 *Correspondence to: Marc Cadotte, [email protected]. 21
1 22 Abstract: 23
24 The COVID-19 pandemic has greatly restricted human activities, and wild species are seemingly
25 thriving in human-dominated areas. However, we have little understanding of the consequences
26 for biodiversity from governmental policies and socioeconomic changes in response to COVID-
27 19, and their conservation significance. Understanding these impacts is a priority for setting
28 effective conservation management in a post-COVID-19 world. Here, we identify putative
29 positive and negative effects of the pandemic on biodiversity. We also highlight consequences
30 that need to be mitigated and others that provided insight into policies to promote biodiversity
31 conservation. To avoid further pandemics and protect human health, local governments should
32 consider biodiversity conservation as a core value and strengthen conservation efforts. In
33 addition, global wildlife trade ban and maintenance of the wildlife’s intact habitats are urgently
34 required. 35
36
37 Keywords: Biodiversity, deforestation, pandemic, poaching, SARS-CoV-2, wildlife trade. 38 39
2 40 The COVID-19 pandemic is threatening global public health and severely limiting human
41 activities worldwide, resulting in unexpected consequences for biodiversity, penguins roaming
42 the streets of eerily quiet South African towns, a puma wandering through Santiago, Chile, and
43 wild boars having their way in Spanish cities, just a few signs of the changing nature of wildlife
44 in the current upheaval (Sharma et al., 2020). Research into the SARS-CoV-2 virus, the cause of
45 COVID-19 disease, has necessarily focused on understanding and finding a cure for the virus
46 and the human health impacts of infection. However, scientists are only beginning to grapple
47 with the environmental and biodiversity consequences of the pandemic and seek opportunities to
48 quantify the effects of human activity on biodiversity (Rutz et al., 2020). The consequences of
49 COVID-19 for biodiversity are critically important to study and understand because it is essential
50 for environmental health and human well-being. The human economic activities and movement
51 have been impacted by COVID-19 shutdowns directly, and impact biodiversity under normal
52 conditions. Further, we need to better understand and communicate that biodiversity is closely
53 related to the emergence and transmission of infectious diseases (Keesing et al., 2010). 54
55 Recent studies have discussed short-term effects of reduced human mobility on biodiversity
56 conservation (Bates et al., 2020; Rutz et al., 2020), but lack a full understanding of long-term
57 impacts from governmental policies and societal changes in response to COVID-19. Here we
58 highlight the possible impacts, identify their conservation significance, and propose potential
59 biodiversity management strategies to prevent future pandemics. 60
61 Direct effect of COVID-19 on wild animals
62 The SARS-CoV-2 virus not only threatens human health and well-being , but also is a risk to
63 wild animals worldwide. Current research is showing that the SARS-CoV-2 virus can transmit
64 from humans to other mammals such as farmed minks (Enserink, 2020), ferrets, and cats (Shi et
65 al., 2020). Siberian tigers and African lions at the Bronx Zoo in New York City have tested
66 positive for the SARS-CoV-2 virus (Leroy et al., 2020). The rising evidence of COVID-19
67 transmission to and between animals indicates that the virus can be a potential risk for
68 susceptible species. Historically, human-to-animal disease transmissions have been widely
69 observed (Messenger et al., 2014). It is a profound threat to apes, which are our closest relatives,
70 because they are likely to be susceptible to infection (Gillespie and Leendertz, 2020). The risk of
3 71 human-to-ape transmission is unfortunately informed by past episodes. For example, wild
72 chimpanzees have been infected with two common human paramyxoviruses, resulting in an
73 unusually high number of sudden deaths of chimpanzees in Côte d'Ivoire from 1995 to 2006
74 (Köndgen et al., 2008). All the great apes are critically endangered, leading to national and non-
75 governmental organizations to limit access to wild ape populations to limit exposure to SARS-
76 CoV-2 (Gillespie and Leendertz, 2020). Until now, we still know little about the direct effect of
77 COVID-19 on wildlife populations. 78
79 Indirect effect of pandemic lockdowns on biodiversity
80 The most important and obvious biodiversity response to reduced human activities is the rapid
81 range expansion of wild animals into formerly human-dominated areas, as showcased by rapid
82 wildlife population increases after the nuclear accidents in Chernobyl (Deryabina et al., 2015)
83 and Fukushima (Lyons et al., 2020). Similarly, COVID-19 lockdowns in human-dominated areas
84 worldwide have resulted in reduced traffic volumes and have generally provided more room for
85 wild animals. As indicated by numerous examples highlighted in popular social media, wild
86 animals are realizing more space and time for their activities as a result of COVID-19, such as
87 lions lounging on empty roads in South Africa, endangered hawksbill sea turtles hatching in
88 greater numbers on empty beaches, and wild flowers flourishing near the street verges and road
89 junctions (Sharma et al., 2020). 90
91 A plethora of environmental consequences, such as noise pollution (McQuate, 2017) and air
92 pollution (Saha and Padhy, 2011), have significant negative effects on the survival of wild plant
93 and animal species. The COVID-19 lockdown has reduced the effect of many of these stressors
94 on wildlife. Government restrictions in response to the pandemic have greatly reduced air
95 pollution (Cadotte, 2020), water pollution (Saraswat and Saraswat, 2020), and noise pollution
96 (Gibney, 2020) around the world. Such environmental improvements will have far-reaching
97 benefits for the survival, growth and reproduction of wild species. For example, reductions of
98 underwater noises caused by ship traffic in North America following the 9/11 attack, are
99 associated with decreased chronic stress in North Atlantic right whale (Eubalaena glacialis)
100 (Rolland et al., 2012). This benefit for marine mammals must surely be occurring again with
101 reduced ship traffic during COVID-19 lockdowns (Rutz et al., 2020).
4 102
103 Even though COVID-19 responses have resulted in reduced air and noise pollution (Cadotte,
104 2020; Gibney, 2020), other pollution pathways have likely increased and have more direct
105 impacts on biodiversity. Before the pandemic, plastic pollution was recognized as a serious
106 problem with significant negative effects on aquatic and terrestrial species (de Souza Machado et
107 al., 2018; Wilcox et al., 2015). With COVID-19, there has been a surge in the personal use of
108 non-recyclable medical materials, such as face masks and rubber gloves. They are now seen
109 littering streets in cities worldwide, and the increased use of packaging and plastic bags for food
110 delivery is increasing plastic pollution (Klemeš et al., 2020). For example, some Asian cities
111 have a two-fold increase in medical waste than before the pandemic, and there is a three-fold
112 increase of unsustainable waste management in some rural UK communities (You et al., 2020).
113 Mitigation actions are desperately required. 114
115 The impact of invasive species on ecosystems is frequently cited as a major source of
116 biodiversity loss globally (van Der Wal et al., 2008), and is strongly correlated with the
117 movement of people and goods between regions (Levine and D’Antonio, 2003). The global
118 spread of SARS-CoV-2, which should be considered an invasive species, was driven by both
119 ecological and socioeconomic factors (Nuñez et al., 2020). As a result of the COVID-19
120 lockdown, global transportations and traffic communications have been greatly limited and the
121 subsequent reduction of economic activity has lowered trade. These responses will invariably
122 reduce the number of non-native species introduced into sensitive habitats around the world. 123
124 Finally, before COVID-19, there was a global move towards increasing isolationism with, for
125 example, the UK leaving the EU and the United States pursuing a plan to build border walls. The
126 pandemic is exacerbating this troubling trend as countries isolate themselves by reducing legal
127 immigration and travel, limiting the movement of expert conservation knowledge and resources
128 into places that desperately need these investments (Bates et al., 2020). More than this, instances
129 of physically isolating regions can impact the movement of species and connections between
130 wild populations. In a related example, to prevent the spread of African swine fever by wild
131 boar, Bulgaria erected a 133-km fence along the border with Romania in 2018 (Mysterud and
132 Rolandsen, 2019). The widespread perception of the zoonotic origin of the SARS-CoV-2 virus
5 133 could cause governments to likewise restrict animal movement to prevent diseases, cause
134 significant habitat loss and fragmentation of wildlife populations, and biodiversity in these
135 transboundary areas would be threatened (Liu et al., 2020). 136
137 Indirect effect of socioeconomic changes
138 While the direct effects of the pandemic lockdowns on wildlife are important, they are mostly
139 temporary or are reversible (Table 1). In contrast, the indirect effects on biodiversity through
140 increased public awareness of the risks of emerging diseases and their relationships with
141 biodiversity could have long-term impacts. It is especially true for segments of the wildlife trade
142 that satisfies non-nutritional demands like perceived medicinal value, such as pangolin scales
143 used in a variety of traditional medicines. These illegal wildlife trades now conflict with the
144 perception that wildlife might carry disease, which is a risk to human health. Wild animals, such
145 as bats and pangolins, were identified as possible natural or intermediate hosts of SARS-CoV-2
146 (Lam et al., 2020; Zhou et al., 2020). To prevent the recurrence of disease transmission to
147 humans from wildlife, Asian nations, like China and Vietnam, are quickly moving to restrict and
148 prohibit the trade and consumption of wildlife (Wang et al., 2020). Given that human
149 exploitation is one of the most important causes of species extinction globally (Díaz et al., 2019),
150 such wildlife trade bans are well-understood to be an important ingredient for the protection and
151 population recovery of wild species. For example, banning the ivory trade in Hong Kong in 2018
152 was seen as a significant step towards improving the long-term persistence of African elephants
153 (Gibson et al., 2018). More importantly, changes in market demand for wild animals will reduce
154 hunting, poaching, and illegal wildlife trade in the long run. 155
156 However, it should be noted that global exploitation of wildlife resources is growing in
157 developing countries during the pandemic (Bates et al., 2020; Evans et al., 2020). According to
158 Asian Development Bank, global economy could suffer losses worth up to $8.8 trillion due to
159 COVID-19. People in precarious economic situations are likely to exploit more local natural
160 resources during the pandemic if incomes are decreased, and thus increase biodiversity threats.
161 For example, India has witnessed an elevated extinction risk of iconic fish species due to an
162 additional 12 million people in extreme poverty as a result of COVID-19 (Pinder et al., 2020).
163 Meanwhile, the economic strains of the pandemic mean that governments and conservation
6 164 organizations have less funding and staff, challenging biodiversity conservation efforts (Corlett
165 et al., 2020). For example, satellite data from Brazil's National Institute for Space Research
166 showed accelerated deforestation rates in Amazon, mainly due to fewer field agents to combat
167 illegal loggers and miners (Trevisani, 2020). In addition, reductions in effectiveness of wildlife
168 patrolling and security lead to increased poaching in rural areas and nature reserves, resulting in
169 a rapid loss of endangered species. For example, at least nine rhinos in South Africa and six
170 rhinos in Botswana have been killed by poachers as coronavirus halts wildlife tourism (Emma
171 Newburger, 2020). In Cambodia, at least three critical endangered Giant Ibis (Thaumatibis
172 gigantea) and over 100 Painted Stork (Mycteria leucocephala) chicks have been killed by
173 poachers in response to COVID-19 (Wildlife Conservation Society, 2020). 174
175 Given that SARS-CoV-2 originates from wildlife, there is a serious risk of an increase in the
176 perception of wildlife as a threat to human well-being. Under the fear of possible disease
177 transmission from purported hosts of the virus, some hibernating bats have been expelled from
178 their habitats and suffer from misguided persecution (Zhao, 2020). However, not all bats carry
179 such viruses and the greatest risk comes not from the presence of bats but rather activities that
180 increase human-animal interactions that facilitate virus spillover (MacFarlane and Rocha, 2020).
181 Perhaps more insidious than the increase in human-wildlife conflict is that these perception
182 changes could result in less support for endangered species protection, which has always been
183 pitted against human economic wellbeing. Further, people might be less inclined to travel for
184 eco-tourism experiences (Buckley, 2020), which can benefit conservation activities (Krüger,
185 2005), or they might be less likely to donate money or volunteer for conservation organizations. 186
187 Conservation significance of impact types
188 As shown in Table 1, the potential consequences of COVID-19 lockdowns on biodiversity are
189 complex and context-specific, and most of these impacts are temporary, with negligible long-
190 term consequences (Corlett et al., 2020). However, ample signs are indicating a rapid range
191 expansion of wildlife into human spaces due to reduced human mobilities and improved
192 environmental conditions. Factors leading to increased biodiversity in human-dominated areas
193 should inform policy and management going forward to see if we can replicate these with policy
194 tools in a post-COVID-19 world. For example, COVID-19 recovery programs could promote
7 195 sustainable consumer choices and strengthen environmental protections (Pearson et al., 2020).
196 From a research point of view, the pandemic lockdown can be considered as an experiment of
197 “Global Human Confinement Experiment”, and provide opportunities that can benefit
198 biodiversity (Bates et al., 2020; Rutz et al., 2020). 199
200 Unlike lockdowns, impacts of socioeconomic changes on biodiversity can have long-term and
201 far-reaching consequences on biodiversity (Table 1). First, the pandemic has educated the public
202 about the risks of wildlife trade and bushmeat consumption, providing opportunities for easing
203 pressure on wild populations (Evans et al., 2020). For example, after the SARS pandemic, the
204 proportion of people who ate wildlife meat in Hunan Province declined (Yang et al., 2007). In
205 addition, some Asian countries have banned wildlife trade temporarily. It should be noted that
206 blanket bans on hunting bushmeat are impossible. In central Africa, bushmeat provides up to
207 80% of the dietary protein and fat for rural communities (Gilbert, 2008). As such, the priority is
208 critical scrutiny of wildlife trade (Montgomery and Macdonald, 2020). Finally, the loss of
209 human-nature interactions during the lockdowns and increased fear of wildlife species could
210 result in a generation of low conservation willingness and investment in conservation efforts
211 (Buckley, 2020). Such elevated negative impacts need to be mitigated quickly and prioritized as
212 essential governmental operations. 213
214 Lessons learned to prevent future pandemics like COVID-19
215 In recent decades, emerging infectious disease events dominated by zoonoses have increased
216 rapidly, with the majority of these diseases originating from wildlife (Jones et al., 2008). Past
217 pandemics, inlcuding SARS, MERS, Ebola, Nipah, H1N1 flu, have been triggered by close
218 human-animal contacts associated with activities that ultimately result in biodiversity loss
219 (Montgomery and Macdonald, 2020), highlighting the entangled link between the biodiversity
220 crisis and disease transmission to human populations. For example, HIV was derived from
221 consumption of wildlife such as the meat of wild chimpanzees (Faria et al., 2014), while SARS
222 was derived from contacts with bats and masked civets (Li et al., 2005). Illegal hunting, wildlife
223 trade and bushmeat consumption increase opportunities for zoonotic disease transmission
224 (Johnson et al., 2020). Unfortunately, billions of live animals and animal products are traded
225 globally every year (Smith et al., 2009). The global wildlife trade has resulted in at least 1441
8 226 mammal species becoming at risk of extinction (Scheffers et al., 2019), and human consumption
227 of wild animals is the largest threat causing megafauna extinction (Ripple et al., 2019).
228 Immediate remedies from governmental and transnational institutions, and conservation-prone
229 actvities encourage close human-nature contacts, such as bird watching and ecotourism, are
230 urgently required. 231
232 Outbreaks of novel diseases and past pandemics have also been linked to deforestation. For
233 example, increasing deforestation by 10% leads to a 3% rise in malaria cases among people
234 living in the Amazon (MacDonald and Mordecai, 2019). Similarly, past outbreaks of Ebola
235 occurred mostly in sites with recent loss of intact forests (Olivero et al., 2017). This pattern was
236 also observed for avian infectious diseases and other diseases (Morris et al., 2016; Sehgal, 2010).
237 Deforestation amplifies human exposure to deadly pathogens because wild species carrying
238 diseases are pushed into human-dominated landscapes. For example, deforestation led Pteropus
239 bats carrying the Nipah virus into anthropized environments where they foraged on mangos near
240 barns, where the virus was transmitted to pigs and then to humans (Chadha et al., 2006). In
241 addition, frequent human-wildlife contacts in newly created forest edges can increase
242 transmission risk of zoonotic infections (Bloomfield et al., 2020). Intact forests provide a
243 plethora of environmental contributions to human well-being (Mori et al., 2017), but we should
244 add to the exaptational value of intact forests in controlling the spread of emerging diseases
245 (Watson et al., 2018). Unfortunately, large intact forests are declining globally (Potapov et al.,
246 2017). As such, it is urgent to preserve intact forest ecosystems to prevent further outbreaks of
247 infectious diseases (Keesing et al., 2010). 248
249 There is a lesson that needs to be learned and communicated, conserving biodiversity generally
250 reduces the transfer of infectious diseases to human populations, and is therefore a fundamental
251 component of effective public health policy (Keesing et al., 2010). To avoid further pandemics
252 and protect human health, local governments need to consider biodiversity conservation as a core
253 value and strengthen conservation efforts. Rapid biodiversity responses to changes in human
254 activity reveal that we have many lessons to learn about our impacts on species. Ultimately, the
255 pandemic is showing us that humans and nature can coexist better. To protect biodiversity in the
256 post-COVID-19 era, governments and conservation organizations need to create policies and
9 257 management scenarios, and to address changes in the exploitation of wildlife resources in rural
258 areas, where the increased plastic pollution is ending up in urban areas, and to guide COVID-19
259 recovery programs so that they strengthen environmental protections. Moreover, we need to
260 educate the public about the risks of inappropriate human–animal contacts. In particular,
261 maintenance of the wildlife’s intact habitats and global ban on illegal wildlife trade are urgently
262 required. 263
264 Acknowledgments:
265 We thank doctors, nurses and other frontline workers in the fight against COVID-19. We
266 appreciate insightful comments from two anonymous reviewers. We declare no competing
267 interests.
268
269 References: 270 Bates, A.E., Primack, R.B., Moraga, P., Duarte, C.M., 2020. COVID-19 pandemic and 271 associated lockdown as a “Global Human Confinement Experiment” to investigate 272 biodiversity conservation. Biol. Conserv. 246, 108571. 273 https://doi.org/10.1016/j.biocon.2020.108665 274 Bloomfield, L.S.P., McIntosh, T.L., Lambin, E.F., 2020. Habitat fragmentation, livelihood 275 behaviors, and contact between people and nonhuman primates in Africa. Landsc. Ecol. 35, 276 985–1000. https://doi.org/10.1007/s10980-020-00995-w 277 Buckley, R., 2020. Conservation implications of COVID19: Effects via tourism and extractive 278 industries. Biol. Conserv. 247, 108640. https://doi.org/10.1016/j.biocon.2020.108640 279 Cadotte, M., 2020. Early evidence that COVID-19 government policies reduce urban air 280 pollution. EarthArXiv. https://doi.org/10.31223/OSF.IO/NHGJ3 281 Chadha, M.S., Comer, J.A., Lowe, L., Rota, P.A., Rollin, P.E., Bellini, W.J., Ksiazek, T.G., 282 Mishra, A.C., 2006. Nipah virus-associated encephalitis outbreak, Siliguri, India. Emerg. 283 Infect. Dis. 12, 235–240. https://doi.org/10.3201/eid1202.051247 284 Corlett, R.T., Primack, R.B., Devictor, V., Maas, B., Goswami, V.R., Bates, A.E., Koh, L.P., 285 Regan, T.J., Loyola, R., Pakeman, R.J., Cumming, G.S., Pidgeon, A., Johns, D., Roth, R., 286 2020. Impacts of the coronavirus pandemic on biodiversity conservation. Biol. Conserv. 287 246, 108571. https://doi.org/10.1016/j.biocon.2020.108571 288 de Souza Machado, A.A., Kloas, W., Zarfl, C., Hempel, S., Rillig, M.C., 2018. Microplastics as 289 an emerging threat to terrestrial ecosystems. Glob. Chang. Biol. 24, 1405–1416. 290 https://doi.org/10.1111/gcb.14020 291 Deryabina, T.G., Kuchmel, S. V., Nagorskaya, L.L., Hinton, T.G., Beasley, J.C., Lerebours, A., 292 Smith, J.T., 2015. Long-term census data reveal abundant wildlife populations at
10 293 Chernobyl. Curr. Biol. 25, R824–R826. https://doi.org/10.1016/j.cub.2015.08.017 294 Díaz, S., Settele, J., Brondízio, E.S., Ngo, H.T., Agard, J., Arneth, A., Balvanera, P., Brauman, 295 K.A., Butchart, S.H.M., Chan, K.M.A., Lucas, A.G., Ichii, K., Liu, J., Subramanian, S.M., 296 Midgley, G.F., Miloslavich, P., Molnár, Z., Obura, D., Pfaff, A., Polasky, S., Purvis, A., 297 Razzaque, J., Reyers, B., Chowdhury, R.R., Shin, Y.J., Visseren-Hamakers, I., Willis, K.J., 298 Zayas, C.N., 2019. Pervasive human-driven decline of life on Earth points to the need for 299 transformative change. Science. 366, eaax3100. https://doi.org/10.1126/science.aax3100 300 Emma Newburger, 2020. ‘Filthy bloody business:’ Poachers kill more animals as coronavirus 301 crushes tourism to Africa. CNBC. URL https://www.cnbc.com/2020/04/24/coronavirus- 302 poachers-kill-more-animals-as-tourism-to-africa-plummets.html (accessed 4.28.20). 303 Enserink, M., 2020. Coronavirus rips through Dutch mink farms, triggering culls to prevent 304 human infections. Science. 368, 1169. https://doi.org/10.1126/science.abd2483 305 Evans, K.L., Ewen, J.G., Guillera-Arroita, G., Johnson, J.A., Penteriani, V., Ryan, S.J., 306 Sollmann, R., Gordon, I.J., 2020. Conservation in the maelstrom of Covid-19 – a call to 307 action to solve the challenges, exploit opportunities and prepare for the next pandemic. 308 Anim. Conserv. 23, 235–238. https://doi.org/10.1111/acv.12601 309 Faria, N.R., Rambaut, A., Suchard, M.A., Baele, G., Bedford, T., Ward, M.J., Tatem, A.J., 310 Sousa, J.D., Arinaminpathy, N., Pépin, J., Posada, D., Peeters, M., Pybus, O.G., Lemey, P., 311 2014. The early spread and epidemic ignition of HIV-1 in human populations. Science. 346, 312 56–61. https://doi.org/10.1126/science.1256739 313 Gibney, E., 2020. Coronavirus lockdowns have changed the way Earth moves. Nature 580, 176– 314 177. https://doi.org/10.1038/d41586-020-00965-x 315 Gibson, L., Hofford, A., Dudgeon, D., Song, Y., Chen, Y., Baker, D.M., Andersson, A., 2018. 316 Hong Kong’s delayed ivory ban endangers African elephants. Front. Ecol. Environ. 16, 317 378–380. https://doi.org/10.1002/fee.1921 318 Gilbert, N., 2008. Bushmeat ban would have dire effects. Nature. 319 https://doi.org/10.1038/news.2008.1114 320 Gillespie, T.R., Leendertz, F.H., 2020. COVID-19: protect great apes during human pandemics. 321 Nature 579, 497. https://doi.org/10.1038/d41586-020-00859-y 322 Johnson, C.K., Hitchens, P.L., Pandit, P.S., Rushmore, J., Evans, T.S., Young, C.C.W., Doyle, 323 M.M., 2020. Global shifts in mammalian population trends reveal key predictors of virus 324 spillover risk. Proc. R. Soc. B Biol. Sci. 287, 20192736. 325 https://doi.org/10.1098/rspb.2019.2736 326 Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L., Daszak, P., 2008. 327 Global trends in emerging infectious diseases. Nature 451, 990–993. 328 https://doi.org/10.1038/nature06536 329 Keesing, F., Belden, L.K., Daszak, P., Dobson, A., Harvell, C.D., Holt, R.D., Hudson, P., Jolles, 330 A., Jones, K.E., Mitchell, C.E., Myers, S.S., Bogich, T., Ostfeld, R.S., 2010. Impacts of 331 biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647– 332 652. https://doi.org/10.1038/nature09575 333 Klemeš, J.J., Fan, Y. Van, Tan, R.R., Jiang, P., 2020. Minimising the present and future plastic
11 334 waste, energy and environmental footprints related to COVID-19. Renew. Sustain. Energy 335 Rev. 127, 109883. https://doi.org/10.1016/j.rser.2020.109883 336 Köndgen, S., Kühl, H., N’Goran, P.K., Walsh, P.D., Schenk, S., Ernst, N., Biek, R., Formenty, 337 P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., 338 Lipkin, W.I., Pauli, G., Boesch, C., Leendertz, F.H., 2008. Pandemic Human Viruses Cause 339 Decline of Endangered Great Apes. Curr. Biol. 18, 260–264. 340 https://doi.org/10.1016/j.cub.2008.01.012 341 Krüger, O., 2005. The role of ecotourism in conservation: Panacea or Pandora’s box? Biodivers. 342 Conserv. 14, 579–600. https://doi.org/10.1007/s10531-004-3917-4 343 Lam, T.T.-Y., Shum, M.H.-H., Zhu, H.-C., Tong, Y.-G., Ni, X.-B., Liao, Y.-S., Wei, W., 344 Cheung, W.Y.-M., Li, W.-J., Li, L.-F., Leung, G.M., Holmes, E.C., Hu, Y.-L., Guan, Y., 345 2020. Identifying SARS-CoV-2 related coronaviruses in Malayan pangolins. Nature https:// 346 doi.org/10.1038/s41586-020-2169-0. https://doi.org/10.1038/s41586-020-2169-0 347 Leroy, E.M., Ar Gouilh, M., Brugère-Picoux, J., 2020. The risk of SARS-CoV-2 transmission to 348 pets and other wild and domestic animals strongly mandates a one-health strategy to control 349 the COVID-19 pandemic. One Heal. 100133. https://doi.org/10.1016/j.onehlt.2020.100133 350 Levine, J.M., D’Antonio, C.M., 2003. Forecasting biological invasions with increasing 351 international trade. Conserv. Biol. 17, 322–326. https://doi.org/10.1046/j.1523- 352 1739.2003.02038.x 353 Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J.H., Wang, H., Crameri, G., Hu, Z., Zhang, 354 H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B.T., Zhang, S., Wang, L.F., 355 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science. 310, 676–679. 356 https://doi.org/10.1126/science.1118391 357 Liu, J., Yong, D.L., Choi, C.Y., Gibson, L., 2020. Transboundary Frontiers: An Emerging 358 Priority for Biodiversity Conservation. Trends Ecol. Evol. 35, 679–690. 359 https://doi.org/10.1016/j.tree.2020.03.004 360 Lyons, P.C., Okuda, K., Hamilton, M.T., Hinton, T.G., Beasley, J.C., 2020. Rewilding of 361 Fukushima’s human evacuation zone. Front. Ecol. Environ. 18, 127–134. 362 https://doi.org/10.1002/fee.2149 363 MacDonald, A.J., Mordecai, E.A., 2019. Amazon deforestation drives malaria transmission, and 364 malaria burden reduces forest clearing. Proc. Natl. Acad. Sci. U. S. A. 116, 22212–22218. 365 https://doi.org/10.1073/pnas.1905315116 366 MacFarlane, D., Rocha, R., 2020. Guidelines for communicating about bats to prevent 367 persecution in the time of COVID-19. Biol. Conserv. 248, 108650. 368 https://doi.org/10.1016/j.biocon.2020.108650 369 McQuate, S., 2017. Human noise in US parks threatens wildlife. Nature 370 doi:10.1038/nature.2017.21933. https://doi.org/10.1038/nature.2017.21933 371 Messenger, A.M., Barnes, A.N., Gray, G.C., 2014. Reverse zoonotic disease transmission 372 (Zooanthroponosis): A systematic review of seldom-documented human biological threats 373 to animals. PLoS One 9, e89055. https://doi.org/10.1371/journal.pone.0089055 374 Montgomery, R.A., Macdonald, D.W., 2020. COVID-19, Health, Conservation, and Shared
12 375 Wellbeing: Details Matter. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2020.06.001 376 Mori, A.S., Lertzman, K.P., Gustafsson, L., 2017. Biodiversity and ecosystem services in forest 377 ecosystems: a research agenda for applied forest ecology. J. Appl. Ecol. 54, 12–27. 378 https://doi.org/10.1111/1365-2664.12669 379 Morris, A.L., Guégan, J.F., Andreou, D., Marsollier, L., Carolan, K., Le Croller, M., Sanhueza, 380 D., Gozlan, R.E., 2016. Deforestation-driven food-web collapse linked to emerging tropical 381 infectious disease, mycobacterium ulcerans. Sci. Adv. 2, e1600387. https://doi.org/10.1126/ 382 sciadv.1600387 383 Mysterud, A., Rolandsen, C.M., 2019. Fencing for wildlife disease control. J. Appl. Ecol. 56, 384 519–525. https://doi.org/10.1111/1365-2664.13301 385 Nuñez, M.A., Pauchard, A., Ricciardi, A., 2020. Invasion Science and the Global Spread of 386 SARS-CoV-2. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2020.05.004 387 Olivero, J., Fa, J.E., Real, R., Márquez, A.L., Farfán, M.A., Vargas, J.M., Gaveau, D., Salim, 388 M.A., Park, D., Suter, J., King, S., Leendertz, S.A., Sheil, D., Nasi, R., 2017. Recent loss of 389 closed forests is associated with Ebola virus disease outbreaks. Sci. Rep. 7, 14291. 390 https://doi.org/10.1038/s41598-017-14727-9 391 Pearson, R.M., Sievers, M., McClure, E.C., Turschwell, M.P., Connolly, R.M., 2020. COVID-19 392 recovery can benefit biodiversity. Science. 368, 838–839. 393 https://doi.org/10.1126/science.abc1430 394 Pinder, A.C., Raghavan, R., Britton, | J Robert, Cooke, S.J., 2020. COVID-19 and biodiversity: 395 The paradox of cleaner rivers and elevated extinction risk to iconic fish species. Aquat. 396 Conserv. Mar. Freshw. Ecosyst. 30, 1061–1062. https://doi.org/10.1002/aqc.3416 397 Potapov, P., Hansen, M.C., Laestadius, L., Turubanova, S., Yaroshenko, A., Thies, C., Smith, 398 W., Zhuravleva, I., Komarova, A., Minnemeyer, S., Esipova, E., 2017. The last frontiers of 399 wilderness: Tracking loss of intact forest landscapes from 2000 to 2013. Sci. Adv. 3, 400 e1600821. https://doi.org/10.1126/sciadv.1600821 401 Ripple, W.J., Wolf, C., Newsome, T.M., Betts, M.G., Ceballos, G., Courchamp, F., Hayward, 402 M.W., Valkenburgh, B., Wallach, A.D., Worm, B., 2019. Are we eating the world’s 403 megafauna to extinction? Conserv. Lett. 12, e12627. https://doi.org/10.1111/conl.12627 404 Rolland, R.M., Parks, S.E., Hunt, K.E., Castellote, M., Corkeron, P.J., Nowacek, D.P., Wasser, 405 S.K., Kraus, S.D., 2012. Evidence that ship noise increases stress in right whales. Proc. R. 406 Soc. B Biol. Sci. 279, 2363–2368. https://doi.org/10.1098/rspb.2011.2429 407 Rutz, C., Loretto, M., Bates, A.E., Davidson, S.C., Duarte, C.M., Jetz, W., Johnson, M., Kato, 408 A., Kays, R., Mueller, T., Primack, R.B., Ropert-coudert, Y., Tucker, M.A., Wikelski, M., 409 Cagnacci, F., 2020. COVID-19 lockdown allows researchers to quantify the effects of 410 human activity on wildlife. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-020-1237-z 411 Saha, D.C., Padhy, P.K., 2011. Effect of air and noise pollution on species diversity and 412 population density of forest birds at Lalpahari, West Bengal, India. Sci. Total Environ. 409, 413 5328–5336. https://doi.org/10.1016/j.scitotenv.2011.08.062 414 Saraswat, R., Saraswat, D.A., 2020. Research opportunities in pandemic lockdown. Science. 368, 415 594–595. https://doi.org/10.1126/science.abc3372
13 416 Scheffers, B.R., Oliveira, B.F., Lamb, I., Edwards, D.P., 2019. Global wildlife trade across the 417 tree of life. Science. 366, 71–76. https://doi.org/10.1126/science.aav5327 418 Sehgal, R.N.M., 2010. Deforestation and avian infectious diseases. J. Exp. Biol. 213, 955–960. 419 https://doi.org/10.1242/jeb.037663 420 Sharma, P., Kaur, M., Narwal, G., 2020. Other side of the COVID-19 Pandemic: A review. 421 Pharma Innov. 9, 366–369. 422 Shi, J., Wen, Z., Zhong, G., Yang, H., Wang, C., Huang, B., Liu, R., He, X., Shuai, L., Sun, Z., 423 Zhao, Y., Liu, P., Liang, L., Cui, P., Wang, J., Zhang, X., Guan, Y., Tan, W., Wu, G., Chen, 424 H., Bu, Z., 2020. Susceptibility of ferrets, cats, dogs, and other domesticated animals to 425 SARS–coronavirus 2. Science. eabb7015. https://doi.org/10.1126/science.abb7015 426 Smith, K.F., Behrens, M., Schloegel, L.M., Marano, N., Burgiel, S., Daszak, P., 2009. Reducing 427 the risks of the wildlife trade. Science. 324, 594–595. 428 https://doi.org/10.1126/science.1174460 429 Trevisani, P., 2020. Amazon Deforestation Accelerates as Coronavirus Pandemic Hinders 430 Enforcement. Wall Str. J. URL https://www.wsj.com/articles/amazon-deforestation- 431 accelerates-as-coronavirus-pandemic-hinders-enforcement-11587586399 (accessed 432 4.29.20). 433 van Der Wal, R., Truscott, A.M., Pearce, I.S.K., Cole, L., Harris, M.P., Wanless, S., 2008. 434 Multiple anthropogenic changes cause biodiversity loss through plant invasion. Glob. 435 Chang. Biol. 14, 1428–1436. https://doi.org/10.1111/j.1365-2486.2008.01576.x 436 Wang, H., Shao, J., Luo, X., Chuai, Z., Xu, S., Geng, M., Gao, Z., 2020. Wildlife consumption 437 ban is insufficient. Science. 367, 1435. https://doi.org/10.1126/science.abb6463 438 Watson, J.E.M., Evans, T., Venter, O., Williams, B., Tulloch, A., Stewart, C., Thompson, I., 439 Ray, J.C., Murray, K., Salazar, A., McAlpine, C., Potapov, P., Walston, J., Robinson, J.G., 440 Painter, M., Wilkie, D., Filardi, C., Laurance, W.F., Houghton, R.A., Maxwell, S., 441 Grantham, H., Samper, C., Wang, S., Laestadius, L., Runting, R.K., Silva-Chávez, G.A., 442 Ervin, J., Lindenmayer, D., 2018. The exceptional value of intact forest ecosystems. Nat. 443 Ecol. Evol. 2, 599–610. https://doi.org/10.1038/s41559-018-0490-x 444 Wilcox, C., Van Sebille, E., Hardesty, B.D., Estes, J.A., 2015. Threat of plastic pollution to 445 seabirds is global, pervasive, and increasing. Proc. Natl. Acad. Sci. U. S. A. 112, 11899– 446 11904. https://doi.org/10.1073/pnas.1502108112 447 Wildlife Conservation Society, 2020. COVID-19 FUELING AN UPTICK IN POACHING: 448 Three Critically Endangered Giant Ibis – Cambodia’s National Bird – Killed in Protected 449 Area. URL https://programs.wcs.org/press/News-Releases/articleType/ArticleView/ 450 articleId/14039/categoryId/127/COVID-19-FUELING-AN-UPTICK-IN-POACHING- 451 Three-Critically-Endangered-Giant-Ibis-Cambodias-National-Bird-Killed-in-Protected- 452 Area.aspx (accessed 4.28.20). 453 Yang, D., Dai, X., Deng, Y., Lu, W., Jiang, Z., 2007. Changes in attitudes toward wildlife and 454 wildlife meats in Hunan Province, central China, before and after the severe acute 455 respiratory syndrome outbreak. Integr. Zool. 2, 19–25. https://doi.org/10.1111/j.1749- 456 4877.2007.00043.x
14 457 You, S., Sonne, C., Ok, Y.S., 2020. COVID-19’s unsustainable waste management. Science. 458 368, 1438. https://doi.org/10.1126/science.abc7778 459 Zhao, H., 2020. COVID-19 drives new threat to bats in China. Science. 367, 1436. 460 https://doi.org/10.1126/science.abb3088 461 Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., 462 Huang, C.-L., Chen, H.-D., Chen, J., Luo, Y., Guo, H., Jiang, R.-D., Liu, M.-Q., Chen, Y., 463 Shen, X.-R., Wang, X., Zheng, X.-S., Zhao, K., Chen, Q.-J., Deng, F., Liu, L.-L., Yan, B., 464 Zhan, F.-X., Wang, Y.-Y., Xiao, G.-F., Shi, Z.-L., 2020. A pneumonia outbreak associated 465 with a new coronavirus of probable bat origin. Nature 570, 270–273. 466 https://doi.org/10.1038/s41586-020-2012-7 467 468
15 469 Table 1 Conservation significance of the effect of COVID-19 on biodiversity. 470 Responses Consequences Effect on biodiversity Reversibility Extent after reopening Direct Infection of wildlife Affect mammals, No Global effect especially great apes
Lockdowns Wildlife exapansion into Mostly positive Yes Global human spaces Reduced air/water pollution Mainly positive Yes Global Increased plastic pollution Harmful to fish, marine Yes Global birds, mammals and turtles, and soil biota Reduced transportation of Positive for native Yes Global invasive species species and ecosystems Border closure Mostly negative effect Yes- if Global on transboundary physical species barriers are not erected
Socioecono Prohibition of wildlife trade Critical for threatened Not likely Asian countries mic wilidlife protection changes Increased fear of wildlife Misguided persecution Not likely Mainly in Asian species of bats and other wild and African animals regions Increased human Drive extinction of Likely Mainly in exploitation threatened species developing countries Failure of conservation Drive extinction of rare Yes Mainly in efforts and endangered developing species countries 471
16