Rapid behavioural response of urban birds royalsocietypublishing.org/journal/rspb to COVID-19 lockdown Oscar Gordo1, Lluís Brotons2,3,4, Sergi Herrando1,3 and Gabriel Gargallo1 1 Catalan Ornithological Institute, ES-08019 Barcelona, Spain 2 InForest Joint Research Unit (CTFC-CREAF), ES-25280 Solsona, Spain Research 3 Centre of Ecological Research and Forestry Applications, ES-08193 Bellaterra, Spain 4 Consejo Superior de Investigaciones Científicas, ES-08193 Cerdanyola del Vallès, Spain Cite this article: Gordo O, Brotons L, OG, 0000-0003-3766-0566; LB, 0000-0002-4826-4457; SH, 0000-0002-5153-7970; Herrando S, Gargallo G. 2021 Rapid GG, 0000-0003-3527-1997 behavioural response of urban birds to COVID- 19 lockdown. Proc. R. Soc. B 288: 20202513. Biodiversity is threatened by the growth of urban areas. However, it is still https://doi.org/10.1098/rspb.2020.2513 poorly understood how animals can cope with and adapt to these rapid and dramatic transformations of natural environments. The COVID-19 pandemic provides us with a unique opportunity to unveil the mechanisms involved in this process. Lockdown measures imposed in most countries Received: 8 October 2020 are causing an unprecedented reduction of human activities, giving us an Accepted: 16 February 2021 experimental setting to assess the effects of our lifestyle on biodiversity. We studied the birds’ response to the population lockdown by using more than 126 000 bird records collected by a citizen science project in northeast- ern Spain. We compared the occurrence and detectability of birds during the spring 2020 lockdown with baseline data from previous years in the same Subject Category: urban areas and dates. We found that birds did not increase their probability Ecology of occurrence in urban areas during the lockdown, refuting the hypothesis that nature has recovered its space in human-emptied urban areas. However, Subject Areas: we found an increase in bird detectability, especially during early morning, suggesting a rapid change in the birds’ daily routines in response to quieter ecology and less crowded cities. Therefore, urban birds show high behavioural plas- ticity to rapidly adjust to novel environmental conditions, such as those Keywords: imposed by the COVID-19. coronavirus disease, behavioural plasticity, urban ecology, detectability, citizen science 1. Introduction Author for correspondence: Since the first human settlements some millennia ago, the anthropogenic trans- formation of the natural environment to build towns and cities has been a Oscar Gordo hallmark of humanity. During the last century, urbanization has experienced e-mail: ogvilloslada@gmail.com exponential growth across the world and it is expected to continue as more people will move from rural to urban areas [1–4]. As a result, urbanization has become one of the most important drivers of global change and a major threat to biodiversity [2,4–6]. Novel human-created environments, such as urban areas, represent a formidable challenge for organisms because the mag- nitude and peace of the environmental alterations imposed by humans usually exceed their limits of tolerance, leading to population shrinkage and extinction [5,7]. Urban challenges include dealing with chemical [3], acoustic [8,9] and light pollution [10,11], human disturbance [5,12], new pathogens [13,14] and predators [15,16], and human infrastructures [15,17]. However, some species are able to overcome these challenges and thrive in urban environments [4,7,12,18,19]. Therefore, a key question in urban ecology is how species cope with urbanization. Countless studies have demonstrated that adapting to urban environments implies some kind of phenotypical differentiation from non-urban relatives [7–9,12,18]. Indeed, organisms are forced to adjust their physiology, behaviour and life histories to the novel conditions imposed by Electronic supplementary material is available the city [5,7]. However, little is known about the adaptive mechanisms allowing online at https://doi.org/10.6084/m9.figshare. the differences observed between urban and non-urban dwellers [6,7]. c.5320544. © 2021 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Observed adjustments are mostly consistent with pheno- (1) Did urban birds become more common in response to 2 typically plastic responses [12], but individual sorting and human-empty cities? It can be predicted that decreased royalsocietypublishing.org/journal/rspb microevolutionary changes by divergent selection could be human presence and disturbance allowed animals to playing a role [4,5,7,18,19]. It may be that our inability to dis- occupy spaces that used to be above their fear tolerance entangle these mechanisms comes from a deficit of thresholds [5,34,35]. Therefore, we expected a higher experimental studies in urban ecology [9], in spite of the occurrence in 2020 compared to the historical records for fact that human-transformed environments often provide the same urban areas. This effect is likely to be stronger ready-made experiments. The current spread of the novel cor- for shyer species (i.e. urban adapters), who are less onavirus disease (COVID-19) and its consequences represents tolerant to human disturbance [5,12,38]. an excellent example, as we are involuntarily involved in a (2) Were urban birds more detectable as a consequence major unintended social experiment. of quieter cities? It can be predicted that decreased After the declaration of the COVID-19 pandemic in March anthropogenic noise increased the effective distance of 2020 by the World Health Organization, most countries have among-bird communications [5,8,9,12] and made birds implemented social and health measures unprecedented in more easily perceived by observers [39,40]. Moreover, as Proc. R. Soc. B 288: 20202513 recent history. These measures, aimed at containing the virus the masking effect of human acoustic contamination spread [20–23], have focused on social distancing and popu- mostly disappeared, we expected an increase in singing lation confinement, as well as the cease of non-essential activity, including potential shifts in its timing, to profit productive and social activities. Overall, the measures have from the new urban soundscape [8,9,41,42]. Therefore, contributed to a global diminishing of human activities [24]. we expected a higher detectability of urban birds during This abrupt and dramatic disruption of most human social the lockdown than in previous years, with possible and economic activities has already had quantifiable effects changes in the daily patterns of detection. on urban environments by marked reductions in air pollution [25–27] and noise [28–30]. One of the most notable and gener- alized measure has been applying certain degree of population lockdown, which renders our city streets empty and virtually 2. Material and methods silent. This situation provides a once-in-a-lifetime opportunity (a) Bird data to study urban wildlife responses to less crowded, noisy and On 14 March 2020, the Spanish Government declared the polluted cities and gain unprecedented mechanistic insights national emergency due to COVID-19 outbreak and imposed into how human activities affect wildlife [24,31–33]. As a severe social restrictions. These restrictions included mandatory result of the human lockdown, unusual observations of ani- and permanent confinement of the population, border closure, mals in urban areas worldwide have flooded the media and limitations in public transport, online education, working from social networks planting in the social imaginary the idea that home whenever possible, and closure of non-essential business ‘nature is getting back its space’ (sensu [34]). Although plaus- and public services. One day later, we launched the project ible, this idea is, in most cases, based on anecdotal records, ‘#JoEmQuedoACasa’ (I stay at home) within the citizen science online platform Ornitho (www.ornitho.cat). This platform aims sometimes false [34,35], without any quantitative scientific to collect wildlife records in Catalonia from birdwatchers and investigation supporting such claim [24,33]. naturalists to improve knowledge of biodiversity in this region. In this work, we aimed to assess the behavioural responses Ornitho has been running since 2009 and has gathered more of birds to the sudden and drastic changes occurring in urban than 6.5 million records to date. The project launched during environments resulting from the COVID-19 lockdown in a the lockdown and aimed to collect information about wildlife densely populated area of northeastern Spain (Catalonia). responses to the new environmental conditions resulting from Following China [23] and Italy [21], Spain was the third people’s confinement. In addition to this valuable information, country worldwide to impose a severe population lockdown the project was important to keep engaged birdwatchers in this to stop COVID-19 spread. The declaration of the national citizen science programme by encouraging them to continue emergency in 14 March 2020 by the Spanish Government complete checklists submission, even during a period of con- imposed the strictest lockdown measures in Europe. Since strained outdoor activities [43–45]. A complete checklist is a checklist with all identified species during any survey. then, social restrictions were alleviated progressively until Lockdown surveys were conducted between 15 March and 13 the end of June (electronic supplementary material, figure S1 April 2020. During these four weeks, people were subjected to the and electronic supplementary material, table S1). As in other most restrictive conditions of mobility and consequently this parts of the world, this big halt of human activities has had sig- period showed the most drastic reduction of human activities nificant environmental effects, with reduced air contamination (electronic supplementary material, figure S1 and table S1). There- and noise in Spanish cities [26,27,36,37]. The severity of the fore, lockdown checklists were carried out only from homes (e.g. lockdown measures imposed in Spain make this country balconies, rooftops or yards). To determine the effect of lockdown especially suitable to study COVID-19 lockdown effects on bird behaviour, we also gathered all complete checklists avail- in urban fauna, as they enjoyed exceptionally quieter towns able in Ornitho recorded during the same dates between 2015 and and cities during many weeks. 2019. Surveyed sites were classified as urban or non-urban accord- We compared bird records collected during the first four ing to the 2017 land use/land cover map of Catalonia [46]. All surveys during the lockdown were in urban environments, weeks of the lockdown in towns and cities of Catalonia with except a few observers living in the countryside, which were the available records for the same region and dates since excluded from the analyses. Therefore, we obtained three 2015. These historical records were used as baseline data. groups of checklists: urban lockdown, historical urban and his- Our broad scale approach (hundreds of study sites covering torical non-urban, which contained a total of 126 315 bird and area of 32 000 km2) at the community level (we studied records. Historical urban data represented baseline data, while 16 different species) allowed us a robust testing of two key historical non-urban data were included as control data without questions: human disturbances. We used 5 years of historical data together 1.0 spotless starlings (Sturnus vulgaris and S. unicolor, respectively) 3 * were merged as Sturnus spp. as both were not usually identified probability of occurrence 0.9 * at the species level in most observations due to their high resem- royalsocietypublishing.org/journal/rspb * blance [50]. Both species are common, widespread, sympatric, 0.8 and share similar habits and behaviour [49]. Thus, we did not 0.7 expect important differences in their occurrence or detectability. * 0.6 (b) Statistical analyses 0.5 To disentangle the effects of individuals’ presence (first question) and detection (second question) in our bird data, we used hier- 0.4 archical occupancy models [51,52]. We considered as replicated Colliv Pasdom Parmaj Serser Picpic Carcar Larmic Strdec Stuspp Turmer Cyacae Chlchl Colpal Motalb Myimon Phooch surveys those checklists reported by the same observer within the same 1 × 1 km UTM cell. By combining observer and location, we avoided variability in detection rates due to observer Figure 1. Probability of occurrence of birds in urban areas before (2015– expertise. We could assume confidently that observer experience Proc. R. Soc. B 288: 20202513 2019, black dots) and during (2020; white dots) the COVID-19 lockdown. was randomly distributed across our study area. The equations Asterisks indicate significant differences (p-value < 0.05). Error bars denote defining our model were: 95% confidence intervals. Acronyms for the species: Carcar Carduelis carduelis, logit(Cj ) ¼ b0 þ b1 groupLj þ b2 groupUj þ b3 groupNj Chlchl Chloris chloris, Colliv Columba livia, Colpal Columba palumbus, Cyacae Cyanistes caeruleus, Larmic Larus michahellis, Motalb Motacilla alba, Myimon and Myiopsitta monachus, Parmaj Parus major, Pasdom Passer domesticus, Phooch Phoenicurus ochruros, Picpic Pica pica, Serser Serinus serinus, Strdec Strepto- logit(ri ) ¼ a0 þ a1 groupLi þ a2 groupUi þ a3 groupNi þ a4 timei pelia decaocto, Stuspp Sturnus spp., Turmer Turdus merula. (Online version þ a5 timei  groupLi þ a6 timei  groupUi þ a7 timei  groupNi in colour.) þ a8 f(houri ) þ a9 f(houri )  groupLi þ a10 f(houri )  groupUi þ a11 f(houri )  groupNi , where Ψj is the occurrence of a species at site j and ρi is its detect- to have a comparable number of checklists in urban areas to those ability in the checklist i; groups L, U and N refer to lockdown, recorded during the lockdown. By using several years of historical urban historical and non-urban, respectively; time refers to the data we got a more representative baseline of the usual conditions duration of the survey; and hour refers to the starting hour. previous to the COVID-19 pandemics, although we could not The hour was included as an unpenalized thin plate regression assess variability among years. spline basis function ( f ) with five degrees of freedom because All checklists had associated basic information about the we expected that detectability could vary in a non-linear way survey: site (geographical coordinates), date, hour, time invested along the day [53,54]. Interactions between group and time and (which was used as a proxy for sampling effort) and observer between group and hour allowed us to model the effect of identity. We excluded checklists lasting greater than 3 h, as these two variables on detectability within each group. To test they might be discontinuous surveys. We also excluded those the significance of hour and interactions, we used log likelihood checklists started 1 h earlier or later than sunrise or sunset, ratio tests. Basis functions were built by the smooth.construct respectively, as they represented nocturnal surveys. To correct function from package ‘mgcv’ (v. 1.8–22 [55]), while occupancy for the adjustment of daylight saving time at the end of March, models were run with the occu function of package ‘unmarked’ we rescaled recorded hours in civil time to the relevant daily (v. 0.12–3 [56]) for R. sun events: sunrise, noon and sunset, which were established as −1, 0 and 1, respectively. Sunrise, noon and sunset were calcu- lated for every geographical coordinate and date by the ‘suncalc’ library (v. 0.5.0) for R software [47]. Rescaling was calculated as 3. Results the quotient between the difference of noon and checklist hour The probability of occurrence of a species during the lockdown and the difference of sunrise or sunset and checklist hour, did not differ significantly from the occurrence recorded in depending on whether the checklist started earlier or later than urban areas in previous years in 12 out of the 16 studied species noon, respectively. This transformation allowed to fix the small after accounting for their imperfect detection (figure 1; elec- bias caused by the longitudinal differences in sunrise and tronic supplementary material, table S2). In the four species sunset across Catalonia as well as by the progressive day length increase during the study period. Not many observers with significant differences, three increased their occurrence recorded the number of individuals for each species. For this and one decreased it. As expected, most of the species (10) reason, we opted to work with presence/absence data. showed significant differences in their occurrence between We gathered 1289 complete bird checklists at 149 sites for the lockdown and non-urban checklists (electronic supplementary lockdown period. The number of replicated surveys per site and material, table S2). On average, these species were approxi- observer ranged from 1 to 91 (mean = 8.7, s.d. = 12.4). Historical mately 15% more common in the lockdown checklists than in records in urban areas were the scarcest: 1062 checklists in 410 sites the non-urban checklists, confirming that most of the studied with up to 48 replicates per site (mean = 2.6, s.d. = 5.2). As expected, species were preferentially urban dwellers. data from non-urban areas were the most abundant, as observers For most species (10), the probability of detection was usually preferred birdwatching in natural habitats. We gathered higher in lockdown checklists than in historical urban ones, 5849 checklists from 3113 sites. Although one observer made 84 repli- but this difference was not statistically significant in most cates for the same site, on average, observers in this group showed the lowest site fidelity (mean replicates = 1.9, s.d. = 3.6). cases (electronic supplementary material, figure S2 and We selected data for the 16 most common sedentary urban table S3). Most species were less detectable in non-urban species in Catalonia [48,49] (figure 1). We focused only on checklists than in urban ones. sedentary birds to avoid seasonal changes in occurrence and abun- As we predicted, detectability varied along the day in a dance associated with migration. Data from the common and the nonlinear way for all species (figure 2; electronic lockdown urban non-urban material, figure S4 and table S5). In most of them (11), such a 4 1.0 time effect was significantly different among groups (electronic Chloris chloris royalsocietypublishing.org/journal/rspb 0.8 supplementary material, table S4). Therefore, a certain increase of the sampling time implied a different increase in chances of 0.6 detection in the lockdown, the historical urban and the histori- 0.4 cal non-urban groups for most species. For half of the species, 0.2 the sampling time effect was significantly lower in the lock- Columba palumbus down group than in the historical urban group (mean probability of detection 1.0 reduction of 17%; electronic supplementary material, table Cyanistes caeruleus 0.8 S5). This systematic reduction contrasts with the comparison 0.6 of time effect between lockdown and non-urban groups, where for nine species there were significant differences 0.4 between both groups, but such differences were disparate 0.2 (mean change −0.8%; electronic supplementary material, Pica pica Proc. R. Soc. B 288: 20202513 table S5). 1.0 0.8 0.6 0.4 4. Discussion Birds did not occur in higher rates in towns and cities during the 0.2 Serinus serinus Turdus merula lockdown than before it, contrary to the hypothesis that birds moved into the human emptied urban areas [33,34,38]. As the sunrise midday sunset midday sunset changes induced by the COVID-19 lockdown were drastic, Figure 2. Variation in the probability of detection along the day for each sudden and of relatively short duration, they probably did group of data (collected during the lockdown, collected historically in not allow for colonization processes. The few species with a sig- urban sites and collected in non-urban environments). Shaded areas rep- nificant increase of their prevalence in urban surveys during resent the 95% confidence intervals. See figure S2 in the electronic lockdown were, interestingly, the ones that are mostly urban. supplementary material for the rest of species. Bird illustrations by Martí As these species are not present in large numbers away from Franch/Catalan Ornithological Institute. (Online version in colour.) urban areas, they could hardly rely on non-urban source popu- lations to occupy cities and towns during the lockdown. Their occurrence in a higher proportion of checklists during the lock- 1.0 down could be due to the observers being constrained to survey from their homes. Urban checklists recorded during the lock- detection at sunrise 0.8 down probably were more focused on more extreme urban probability of environments (i.e. core urban areas) than those checklists 0.6 historically recorded in urban areas of Catalonia, which per- 0.4 haps included a greater proportion of surveys in urban parks, landscaped plots or suburbs. These areas are considered 0.2 urban areas from a land-use perspective, but they have more diversity of habitats at our working micro-scale (1 × 1 km), 0 2015–2019 2020 where the most urban exploiter species, such as feral pigeons (Columba livia), collared doves (Streptopelia decaocto) and monk Figure 3. Probability of detection in urban environments at sunrise for the parakeets (Myiopsitta monachus), may not find their most 16 studied bird species before (2015–2019) and during (2020) the COVID-19 suitable niche. The absence of some non-essential activities lockdown. during the lockdown, such as feral populations’ management and culling [32], can be discarded as a cause for the increase supplementary material, figure S3). Except for two species, the of occurrence of these species. Despite being harmful invasive pattern of daily variation in detectability was significantly species [57,58], there is no management of the Catalan popu- different among groups (electronic supplementary material, lations of Psittacidae yet. Culling of feral pigeons in big cities, table S4). A difference consistently found in most species was such as Barcelona, was suspended due to ethical considerations higher detectability in the first hours of the morning during in 2006 [59] and thus control measures for this species were the lockdown compared to the urban records from previous unaffected by the lockdown. Finally, the collared dove colo- years (figures 2 and 3). In most species, during the lockdown nized Catalonia naturally in the 1970s and occupied quickly detectability peaked at dawn and decreased until midday, most of the urban areas during the 1980s and 1990s [49,60]. Cur- while in the historical urban checklists the peak of detectability rently, its population grows at a 2% annual rate [61], which is was around mid-morning. In fact, the pattern of detectability too small to justify an 18% increase of population occupancy along the day in the lockdown group resembled more the in 2020. non-urban pattern than the urban pattern in many species. Pre- Birds changed their detectability pattern throughout the dicted detectability at sunrise by our models in the lockdown day as a consequence of the lockdown. In general, there was group was on average 27% higher than in the urban group an increase in detection probability, which was especially (sign test: Z = 3.25, p-value = 0.001; figure 3). marked in the early morning. As observed in non-urban habi- As expected, in all but one species, chances of detection tats, detectability during the lockdown decreased from dawn increased with longer surveys (electronic supplementary onwards, while at the same urban locations detectability was historically low at dawn and increased until reaching a peak 2 only those individuals in the best physical condition can 5 or 3 h later. It is interesting to note that the Eurasian blackbird, undergo dawn fasting [62]. In Mediterranean regions, where royalsocietypublishing.org/journal/rspb a model species in urban ecology studies [7,8,12,62,63], was the spring nights are mild, the role of dawn singing as a signal of only exception to this pattern. Overall, many species showed a male quality might be less important. Attracting mates would pattern of detection during the lockdown in urban areas more be the prime objective for singing, and consequently males similar to that commonly seen in natural environments. would be more pressed to place this activity when the interfer- Although in urban areas the 2020 detectability pattern was ence of anthropogenic noise is at its lowest. Since sunrise, these patently different from the 2015–2019 baseline level, such lowest levels of noise are just after the morning rush hour (i.e. differences could have been partially enhanced because of later than 9.00), when the physical properties of the air still comparing a single year against several pooled years. Neverthe- keep sound attenuation and fluctuation low [70]. less, it would be necessary to know whether or not there is If birds have changed their behaviour, this adaptive, flexible significant among-years variability in bird daily routines. If behavioural response must have been mediated by phenotypic that is the case, we would expect that behavioural responses plasticity. Human lockdown was sudden and the environ- to extreme events, such as the COVID-19 lockdown, would mental scenario in urban areas changed radically from one Proc. R. Soc. B 288: 20202513 fall out of the normal variability. Unfortunately, we could not day to the next (electronic supplementary material, figure S1) properly explore the between-years variation in detectability [27,36,37]. This unprecedented social experiment imposed by patterns due to sample size constraints. COVID-19 allowed us to test and support the hypothesis of Urban birds during lockdown may have shown this detect- the high plasticity displayed by individuals living in urban ability peak at dawn, typical of non-urban habitats, because of a areas in order to cope with a constantly changing environment rapid behavioural response to adjust to the new environmental [5–7,64]. However, this fast adaptive response might have been conditions imposed by the COVID-19 measures [64–68]. Birds facilitated by a previous conditioning of birds to weekly rely heavily on acoustic communication. During reproduction, rhythms of human activities. Birds change their behaviour males sing to attract females and defend their territories, from working to weekend days to match with human beha- becoming highly conspicuous and detectable. COVID-19 lock- viours [41,73,79]. Therefore, birds could assimilate the down was imposed just at the beginning of the breeding season, lockdown as a very long and especially peaceful weekend, when singing activity was expected to be especially high [69]. and consequently we may speculate that behavioural adjust- Therefore, there was a strong pressure to time singing activity ments to novel lockdown conditions happened quickly to the optimal moment of the day. This moment is dawn (necessarily in less than one month). Nevertheless, it would because the physical properties of the atmosphere enhance be interesting to explore the long-lasting consequence at a com- acoustic transmission [70,71] and consequently birds can munity level of this environmental change [76]. Weekends are reach the maximum audience. Thus, urban birds during the just 2 days long, while strict human lockdown lasted for at lockdown may have advanced their main period of singing least 2 months in most regions of Spain. One may speculate activity to dawn, increasing their detection at those hours, that bolder and faster-adapting species are able to modify similar to what is observed in non-urban areas. their behaviour on a weekly basis. However, during the lock- During the lockdown, human presence and activities down, all species had enough time to habituate to the long- decreased drastically (electronic supplementary material, lasting new conditions. In fact, as we have demonstrated, all figure S1 and table S1), this being especially notable during of them modified their daily patterns of detectability. Maybe rush hours, which almost disappeared [27,30,36]. During the the most urban species have benefited the least from this lock- spring in Spain, morning rush hour matches with the first down as their boldness and higher human tolerance was no hours of light, when birds are expected to be especially commu- longer an advantage in empty cities. nicative [42,63,72]. The dramatic decrease in noise during the In addition to the birds’ rapid behavioural response to the lockdown released early morning acoustic space that could be anomalous environmental conditions during the lockdown, recovered by the dawn chorus. Empirical and experimental evi- observers had certainly enhanced opportunities to detect dence demonstrates that urban birds avoid the masking effect birds during this period. Urban areas were quieter than of anthropogenic noise [8,9,41,42,73]. Our findings match usual [27–30], improving the chances of listening the birds these previous studies, but instead of advancing the dawn [34,39,40,70]. Moreover, the absence of people outdoors chorus [42,62,63,74], our historical urban data suggest that allowed for the display of shy and distrustful behaviours birds would delay their peak of activity (and consequently of [5], facilitating bird observations, especially for those less sing- detectability) to mid-morning. In our study context, this can ing species, such as the magpie (Pica pica) or the yellow-legged be explained because civil and solar time are heavily decoupled gull (Larus michahellis). Hence, birds’ detectability during 2020 in Spain since the country is located in the westernmost part of could be higher just as a by-product of a reduced interference its time zone [75]. For this reason, if birds in Catalonia advance in urban birdwatching of the human activities during the their activities before sunrise, they would be still suffering an lockdown (e.g. traffic, pedestrians, factories, etc. [30,36,37]). important overlap with morning noisy human activities, such However, these improved conditions for urban birdwatching as commuting, school attendance, shop opening, etc. [63,72]. were heavily constrained by the fact that observers were Hence, the best option for birds would be to delay the peak forced to stay at their homes and their sampling area was of activity to after the morning rush hour [73]. Moreover, reduced to what they could see from there. Therefore, most of the previous studies have been carried out in more improved detection was to some extent counterbalanced by northern latitudes [8,62,76], where climate conditions can still the limited scope from the survey sites. The observed effect be severe at night in early spring. Under these circumstances, in increased sampling time would support this hypothesis, individual survival can be challenged by a strong nocturnal as we demonstrated that the discovery rate in most species energy demand [77,78]. There, dawn singing can become a rel- was slower during the lockdown than in the historical evant and honest signal of the phenotypic quality of males, as urban surveys. The differences observed between urban and non-urban The COVID-19 shutdown has revealed the stress, noise 6 environments were expected as habitat configuration and and pollution present in urban areas [25,26,28,29]. Under royalsocietypublishing.org/journal/rspb bird densities are patently different between them. In fact, typical urban conditions, bird behaviour is apparently altered populations of urban exploiter birds show usually higher by our lifestyle, and thus the possibility to enjoy the natural densities in cities than in rural or natural close areas [5–7], facil- values of our cities is notably diminished [7]. Our society itating their detection in urban areas. Such differences may should reflect on our urban lifestyle and how it affects the have serious consequences for monitoring schemes aiming to welfare of urban fauna and jeopardizes its conservation. As quantify wildlife occurrence and abundance by standardized the world is becoming more urbanized and animals will be protocols, as the assumption of equal detectability under simi- forced to live more often in anthropogenic environments lar circumstances is usually violated [39,52,53,80]. For instance, [5–7], one way to ensure their adaptation as urban dwellers one sampling hour at dawn is not equivalent in terms of would be by reducing our noisier and more disturbing chances to detect a species in urban and non-urban habitats. activities. Most importantly, not only urban populations of Traditional protocols assume that the best moment to detect non-human animals would benefit, but also ourselves from birds is early morning [70,81], which is actually true, but appar- quieter, more peaceful and less polluted cities. Proc. R. Soc. B 288: 20202513 ently only in natural conditions without human disturbance, as we have demonstrated here (figure 2). If the detectability peak in most urban populations is reached at mid-morning, their Data accessibility. Data available from the Dryad Digital Repository: abundance would be systematically underestimated by usual https://doi.org/10.5061/dryad.8w9ghx3kc [82]. sampling protocols based on early morning bird surveys. It Authors’ contributions. G.G. had the original idea and designed the moni- toring programme. O.G. and G.G. formulated formal hypotheses, does not matter whether this lower detectability in urban and collected and arranged the necessary data for the study. O.G. areas in early morning is caused by different daily routines of analysed data. O.G. wrote the manuscript, with contributions from urban versus non-urban populations or by the masking effect all the authors. of human activities in the city (or a combination of both). As Competing interests. The authors declare no competing interests. there is an increased awareness about the importance of Funding. This study did not receive any funding. urban populations for bird conservation [7,48], it is necessary Acknowledgements. We warmly thanks to the thousands of observers to ensure its accurate quantification, which may imply a redefi- who shared their observations by Ornitho website, for their long- nition of the most popular current census techniques [7]. term involvement in this project and the special efforts undertaken during the lockdown. Ornitho project is supported by the Generalitat Additionally, in this work, we demonstrated the utility of occu- de Catalunya. Margarida Barceló-Serra provided valuable English pancy models and the necessity to account for imperfect edits and suggestions. We would also like to thank the anonymous detection [53,54]. reviewers and the editor for their comments. References 1. Seto KC, Güneralp B, Hutyra LR. 2012 Global 8. Slabbekoorn H, Ripmeester EA. 2007 Birdsong and 16. 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