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 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 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 . 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 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 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 (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

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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

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