key: cord-0684955-bpsvn7bv
authors: Bates, Amanda E.; Primack, Richard B.; Duarte, Carlos M.
title: Global COVID-19 lockdown highlights humans as both threats and custodians of the environment
date: 2021-05-20
journal: Biol Conserv
DOI: 10.1016/j.biocon.2021.109175
sha: 4e5044047a1ac963be5be3fe1b1c085c881be4cc
doc_id: 684955
cord_uid: bpsvn7bv

The global lockdown to mitigate COVID-19 pandemic health risks has altered human interactions with nature. Here, we report immediate impacts of changes in human activities on wildlife and environmental threats during the early lockdown months of 2020, based on 877 qualitative reports and 332 quantitative assessments from 89 different studies. Hundreds of reports of unusual species observations from around the world suggest that animals quickly responded to the reductions in human presence. However, negative effects of lockdown on conservation also emerged, as confinement resulted in some park officials being unable to perform conservation, restoration and enforcement tasks, resulting in local increases in illegal activities such as hunting. Overall, there is a complex mixture of positive and negative effects of the pandemic lockdown on nature, all of which have the potential to lead to cascading responses which in turn impact wildlife and nature conservation. While the net effect of the lockdown will need to be assessed over years as data becomes available and persistent effects emerge, immediate responses were detected across the world. Thus initial qualitative and quantitative data arising from this serendipitous global quasi-experimental perturbation highlights the dual role that humans play in threatening and protecting species and ecosystems. Pathways to favorably tilt this delicate balance include reducing impacts and increasing conservation effectiveness.

Human-driven alterations of atmospheric conditions, elemental cycles and biodiversity suggest that the Earth has entered a new epoch, the Anthropocene (Crutzen, 2002; Steffen et al., 2007) . Negative impacts associated with human activities include a much warmer Earth state, marked expansion of urbanization, and accelerating species extinctions (Schipper et al., 2008) . The perspective that the main role of humans is a source of threats on species and ecosystems leads to the prediction that the global human lockdown to mitigate COVID-19 health risks may alleviate human impacts, with resulting positive environmental responses (Derryberry et al., 2020; Rutz et al., 2020) .

Indeed, early reports indicate that restrictions led to immediate decreases in air, land and water travel, with similar declines in industry, commercial exploitation of natural resources and manufacturing, and lower levels of PM 10 , NO 2 , CO 2, SO 2 and noise pollution (Bao and Zhang, 2020; March et al., 2021; Millefiori et al., 2021; Otmani et al., Yet a more comprehensive consideration of the links between human activities and species and ecosystems also acknowledges the role of humans as custodians of nature, who engage in conservation research, biodiversity monitoring, restoration of damaged habitats, and enforcement activities associated with wildlife protection Corlett et al., 2020; Evans et al., 2020; Manenti et al., 2020; Rondeau et al., 2020; Zambrano-Monserrate et al., 2020; Kishimoto et al., 2021 Sumasgutner et al., 2021 [this issue]). Indeed, the global COVID-19 human confinement has disrupted conservation enforcement, research activities and policy processes to improve the global environment and biodiversity (Corlett et al., 2020; Evans et al., 2020; Zambrano-Monserrate et al., 2020; Quesada-Rodriguez et al., 2021 [this issue]) . The lockdown has also created economic insecurity in rural areas, which may pose biodiversity threats as humans seek to support themselves through unregulated and illegal hunting and fishing, and conservation spending is reduced. In particular, declines in ecotourism in and around national parks and other protected areas lowered local revenue, park staffing, and funding to enforce hunting restrictions and invasive species management programs (Spenceley et al., 2021; Waithaka et al., 2021) . In many areas, restoration projects have been postponed or even cancelled Corlett et al., 2020; Manenti et al., 2020) .

Here, we consider the global COVID-19 lockdown to be a unique, quasi-experimental opportunity to test the role of human activities in both harming and benefiting nature . If the negative roles of humans on species and ecosystems J o u r n a l P r e -p r o o f Journal Pre-proof predominate, we would expect overwhelmingly positive reports of responses of nature to human lockdown. We integrate 30 diverse observations from before and during the peak lockdown period to examine how shifts in human behavior impact wildlife, biodiversity threats, and conservation. We first analyze the mobility of humans on land and waterways, and in the air, to quantify the change in human activities. Second, we compile qualitative reports from social media, news articles, scientists, and published manuscripts, describing seemingly lockdown-related responses of nature, encompassing 406 media reports and 471 observations from 67 countries. Third, we map the direction and magnitude of responses from wildlife, the environment and environmental programs, using data collected before and during lockdown provided by scientists, representing replicated observations across large geographic areas. We collated data from 84 research teams that maintained or accessed existing monitoring programs during the lockdown period, reporting 326 responses analyzed using a standardized analytical framework. We accounted for factors including autocorrelation and observation bias using mixed effects statistical models, and selected the most robust available baselines for each study to report lockdown-specific effect sizes (see methods). We empirically describe the type, magnitude, and direction of responses for those linked with confidence to the lockdown, and offer integrated outcomes supported by examples drawn from our results. Finally, we use these results to provide recommendations to increase the effectiveness of conservation strategies.

Here we interpret data and qualitative observations that represent a non-random sample of available information comprising diverse response variables. Thus, we make inferences about the geographic scope of observations and focus on what integrated understanding can be gained from considering the evidence of both positive and negative effects of the lockdown and their linkages.

From diverse data sources and analyses, we compiled a high-level view of how the lockdown influenced four major categories of responses of shifts in (1) human mobility and activity, (2) biodiversity threats, (3) wildlife responses, and the (3) social structures and systems that influence nature and conservation (described in further detail in Appendix 1, Table A1 ). In brief, human mobility and activities included recreational activities such as park visits and boating, commuting, and activities related to industry, such as shipping. Biodiversity threats included categories which were linked directly to a possible negative wildlife response, such as hunting, fishing, mining, vehicle strikes, wildlife trade, environmental pollution, and deforestation. Wildlife responses represented observations related to biodiversity and species, such as community structure, animal performance (e.g., reproduction, health, foraging) and habitat use (i.e., abundance and distribution). Environmental monitoring, restoration programs, conservation, and enforcement were grouped as representing social systems and structures that influence and support conservation. are available aggregated to regional scales (usually country). Each regional mobility report reflects a percentage change over time compared to a 5-week baseline (Jan. 3 to Feb. 6, 2020) . Similarly, Apple Maps Mobility Trends Reports are based on Apple maps user data and aggregated by region to reflect the percent change in time Apple maps users spent driving relative to a baseline (Jan. 12, 2020). The percent change in the responses of human mobility through time allows identification of extreme inflections related to human behavior. For Google and Apple data, we extracted the overall mobility trends for each country until May 1 st , which was selected from a sensitivity test and before relaxation of confinement measures were introduced in most countries. We further excluded within-country variations in mobility, and removed all countries with extensive data gaps and countries that did not show a response to lockdown.

The first step to quantifying the effect due to the lockdown on community mobility (residential and parks) and driving data identified the date of greatest change in each time-series (data and script files are here: https://github.com/rjcommand/PAN-Environment). Because each country had differing lockdown dates and multiple types of lockdown, we identified critical transition dates which best explained the change in mobility for each country. To do so, we used Generalized Additive Models (GAM (Wood, 2011) ) on daily mobility levels in each country, using the Oxford Covid-19 Government Response Tracker database of country-level containment policies (C1-C7) to define a variable for the before and after lockdown periods, running up to 15 models per country depending on the number of different kinds of lockdown measures imposed. From these models, we selected the lockdown date that explained the greatest amount of change.

We manually identified the confinement dates in cases where the models did not converge or when multiple unexplained inflection points were detected (N = 10 countries). Percent change was calculated as the mean percentages after implementation of the confinement measure selected from the models. 

Observational evidence of the impact of the first four months of the COVID-19 lockdown on society, the environment and biodiversity was collected and collated through: (1) internet searches with the keywords nature, conservation, environment and COVID-19;

(2) calls on social media for personal observations and for volunteers to contribute from our networks; (3) Web of Science general search for papers (terms: nature, J o u r n a l P r e -p r o o f Journal Pre-proof conservation, environment, COVID-19) released released between May to August 2020 that also used qualitative evidence to investigate the lockdown effect, and (4) through volunteer contributions from our global PAN-Environment working group of over 100 scientists. Each qualitative observation (N = 877 observations) was assigned a geographic location (latitude and longitude) and classified by observation type (described in Appendix 1, Table A1 ), including a description and details on the species impacted (where relevant). Reports that listed several impacts (e.g., independent observations, species, or locations) were entered as multiple lines. Following entry to our dataset, each observation was assigned an effect score from 0-10 (as described in Appendix 1, Table A2 ) to distinguish between observations with ephemeral effects with unknown impacts from those that will have widespread or persistent outcomes with strong effects in positive or negative directions. Qualitative data were recorded for all continents, except Antarctica, representing 67 countries. Non country-specific observations were also included, representing 20% of all anecdotes. The majority of countries were represented by less than five observations (51 countries), while South Africa submitted approximately one third of the total observations (total = 297). This high representation in South Africa was a known bias due to the use of African birding forums to collect citizen science data which were organized to communicate and engage widely as lockdown measures were implemented. Similarly, other known biases Table A4 ). In other cases, the reference was an area representing a reference state (i.e., remote areas or large, well-governed protected areas did not undergo a difference in human activities due to lockdown measures). If observations were unavailable prior to the start of the pandemic lockdown or for reference year(s), comparisons were made (if sensible) during and after the lockdown, i.e., the reference was the post-confinement period (8 studies). For instance, litter accumulation at two locations was measured from the strict lockdown in April 2020, and over two months as restrictions eased. Spatial comparisons between areas impacted by the lockdown with unaffected sites were also included to detect lockdown related effects. These unaffected sites were considered as reference areas after evaluation by the relevant research teams who contributed the data (2 studies). The rationale for each study design and selection of the baseline period is reported in Table A4 and A5 (Appendix 4 and 5), and was reviewed by the core analysis team to ensure the baseline period comprised a suitable reference for the given response of interest. Total percent changes were calculated as the difference between the response coefficient (attributed to the lockdown) relative to the reference coefficient. For instance, if we observed a 400% increase in a response during the lockdown, this translates to an effect which was 4 times greater. We used Generalized Linear, Additive Mixed (GAMM (Wood, 2004) ) or Linear Mixed-Effects (LME (Pinheiro et al., 2021) ) models, as best suited for each data type. Suitability was based on the distribution of the response data, fit of the statistical data and the covariates that needed to be accounted for to estimate the appropriate coefficients. In brief, for each dataset, we quantified percentage change from expected or typical values, as well as an effect size in the form of a t-statistic standardized by sample size (Bradley et al., 2019) . Different datasets were analyzed using statistical models with parameters dependent on the type, duration and complexity of each response and study design. Table S5 (Appendix 5) provides a summary of the information that was collected from the authors who contributed each study, a description of the methods and relevant references, analysis type, spatial scale, details on the temporal or spatial baselines and how they were accounted for or interpreted, reports of any confounding factors (included as covariates), model results summary table links to GitHub, interpretation, and confidence score that the observed effect was indeed due to the lockdown (with a rationale for this selection). The relevant information for interpretation across studies was subsequently transcribed to Table S4 (Appendix 4).

The global peak of lockdown occurred on April 5 th , 2020, at which time 4.4 billion people were impacted (Fig. 1) , representing 57% of the world"s population. In the weeks before and after this lockdown peak, residents of most countries spent much more time at J o u r n a l P r e -p r o o f Journal Pre-proof home (Fig. 2) . Country specific critical transition dates (which occurred primarily in late March leading up to the April peak) were used to assess the total change in mobility until May 1 st . During this period, driving decreased by 41%, there was a 20% overall reduction in park visits, particularly in Central and South American countries, although Nordic countries were an exception (Figs. S1 & S2). The April 2020 period also saw major disruptions in community, food transport, and supply chains, with a 9% decrease in marine traffic globally and a 75% total reduction in air traffic (both relative to April 2019, Figs. A3-A5). Thus, the COVID-19 lockdown has led to a significant global reduction in human mobility, notably travel, causing an "anthropause" (Rutz et al., 2020) .

As humans retreated, animals quickly moved to fill vacated spaces (Fig. 3) (Derryberry et al., 2020; Zellmer et al., 2020) . In our dataset, approximately half of the qualitative observations and more than one third of all measured quantitative species responses that were linked with some confidence to the lockdown related to unusual animal sightings in urban areas (both land and waterways), and to species occurring in different abundances compared to pre-perturbation baseline estimates (Figs. 4 and 5). Many initial observations painted a rosy picture of wildlife "rebounding"; indeed, our qualitative observations of wildlife responses are predominantly positive, likely reflecting reporting biases (Fig. 4) . Reports include changes in behavior, reproductive success, health, and J o u r n a l P r e -p r o o f Journal Pre-proof reductions in mortality, apparently in response to altered levels of human activity (Fig.   4 ).

Our quantitative assessments suggest a mixed role of human confinement in positively and negatively influencing wildlife (Fig. 5) . Some species changed their behavior (e.g., daily activity patterns) and relocated to entirely new areas, including seeking new food sources and roaming to unusual areas. This included air space, such as when critically endangered Griffon vultures in Israel flew further afield in 2020, apparently due to reduced military training during the lockdown (Appendix 4, Table A4 , StudyID 55). Some animals also moved to human settlements from rural locations (e.g., golden jackals:

Appendix 4, Table A4 , StudyID 28), while other species showed very little changes ( Fig.   5 showing distribution of wildlife responses as effect sizes which center on zero).

There was also qualitative evidence of increased human-wildlife conflicts (described in Appendix 3, Table A3 under the categories: Biodiversity threat, Human-wildlife interaction, Aggression). Four non-fatal shark attacks on humans occurred over a span of five weeks in French Polynesia, a number typically observed over a whole year, and an unusually high number of fatal shark attacks has been reported for Australia. On land, monkeys that normally live closely and peacefully with humans near a pilgrim center in Uttar Pradesh, in northern India, attacked residentsatypical behavior that may be related to starvation and corresponding aggression.

The pandemic lockdown generally highlighted the enormous and wide-ranging impacts that humans have on the environment and wildlife. For instance, in a remote forest area in Spain, a 45% reduction in NO 2 and SO 2 lead to reduced atmospheric deposition of NO 3 and SO 4 2-, and limited the input of N and S to soil ecosystems (Appendix 4, Table   A4 , StudyID 84). Ocean fishing was also reduced by 12% based on our analysis of 68,555 vessels representing 145 national flags and 14 gear types (including drifting longlines and nets, purse seines and trawlers, Appendix 4, Table A4 , StudyID 5).

Animal deaths from vehicle strikes on roads and vessel strikes in the water during peak lockdown were dramatically lower than baseline periods in two data sets (e.g., 19%

reduction: South Korea, 42% reduction: USA, Appendix 4, and beaches around the world, direct pollution from humans was also reduced during combination of reduced protection from forest departments, increased sales of hunting permits, and greater illegal hunting. This is surprising considering the possible role of pangolins as intermediary hosts of SARS-COV-2, and calls to halt the consumption of wildlife to avoid future zoonoses . Furthermore, it is clear that resilient socio-ecological systems are fundamental to supporting nature conservation.

We further find that impacts of the lockdown on human hunting activity have created not Fig. 3 ).

The magnitudes of some effects were also more dramatic than anticipated, such as in cases where the lockdown coincided with reproductive activity. For example, in Colombia, a hotspot of bird diversity, species richness in residential urban areas in Cali increased on average by 37% when human activity was lowest during the lockdown, In Florida, for instance, lockdown-related beach closures in a conservation area were linked to a surprising 39% increase in nesting success in loggerhead turtles, attributed to a lack of disturbances from fishers and tourists with flashlights, and lack of obstructions such as sandcastles (Appendix 4, Table A4 , StudyID 74).

The global human lockdown experiment has revealed the strong potential for humans as custodians of the environment. The wealth of observations collated here provides compelling, near-experimental evidence for the role of humans as a source of threats to species ecosystems, illustrated by a range of increases in biodiversity threats with release from human disturbance during lockdown. Increases in biodiversity threats are consistent with the assumed role of human activity as a source of negative impacts on the environment. These observations help identify ways in which human disturbance may play stronger roles in impeding conservation efforts than previously recognized, even for well-studied species such as sea turtles. Our data also reveal contexts where rather than reducing traffic volume, reducing traffic speed would lead to less noise pollution and protect both wildlife and human safety.

Considering how wildlife and humans have responded during the lockdown offers the potential to improve conservation strategies. In particular, restrictions and enforcement mechanisms to control human activities in conservation areas and parks seem critical to their effective functioning. Adaptive conservation management during reproductive seasons, such as during the nesting season of birds and sea turtles, may also have much stronger positive impacts than previously recognized. The pandemic also highlights the value of parks near urban centers that protect species and the environment, and offer opportunities for humans to conveniently enjoy nature without traveling long distances (Airoldi et al., 2021) . The role of humans in supplying food for some animal species is also apparent, and suggests that this interaction can be managed to improve conservation outcomes, and avoid risks such as wildlife-human conflicts. Regulation of marine shipping traffic speed and volume can also have a major contribution to conservation, which would require, similar to the case of terrestrial systems, the identification and regulation of hotspots where strikes are frequent and noise levels are elevated; the analysis of detailed animal tracking data could further inform such interventions (Rutz et al., 2020) . Our results also provide compelling evidence for the benefits of reducing noise levels, particularly at sea, and give additional impetus to policies that incentivize the development of noise reduction technologies (Duarte et al., 2021) .

Journal Pre-proof While many changes were linked to the lockdown, we failed to link effects to the lockdown in 18 different studies which represent a wide range of systems and contexts.

Even so, what was interesting is that 15 of these studies focussed on wildlife responses. Table A4 , StudyID 54). We also found strong changes that were attributed to other factors, such as the use of the Kerguelen toothfish fishing grounds (Australia) by seals in 2020 (Appendix 4, Table A4 , supporting intense human activity may retreat back to smaller ranges once human activity resumes full-scale. However, negative impacts resulting from the interruption of conservation efforts may be long-lasting and reverse years and decades of such efforts.

It is likely that long-term impacts of hunting will be apparent into the future in the abundance of this species (Appendix 4, Table A4 Assuming fractions of 5% and 10%, April 26th was the day with the maximum population under lockdown equal to 53% and 54% of the population, respectively. Table A4 ). Bubble size represents data density (the largest bubble represents 41-60 observations and the smallest is 1-20). Only responses that were attributed to the lockdown with high confidence are included. a) Human activities and mobility (blue) includes measured responses in human activities and mobility, such as related to commuting and recreational activities (categories are described in Appendix 1, Table A1 . Categories describing the type of effect related to human activities, biodiversity threats, biodiversity and social systems. Table A2 . Effect scoring scheme applied to anecdotal observations.

Supplementary Methods. Statistical analysis methods.

J o u r n a l P r e -p r o o f Journal Pre-proof 

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