Community and species-specific responses of coastal birds to COVID-19 “anthropause” in the largest hypersaline lagoon of South America
DOI:
https://doi.org/10.1590/Keywords:
Seabirds, Coronavirus, Coastal lagoon, SARS-CoV-2, LockdownAbstract
The COVID-19 pandemic led to a reduction in human mobility, known as “anthropause.” Few studies have
compared birds’ community patterns between lockdown and “new normal” periods, especially in extremophile
environments. This study presents the first baseline by monitoring coastal birds on 10 beaches along the largest
hypersaline lagoon in South America. The birds were counted in September and October 2021 (during a lockdown
period) and in October 2022 (after the lockdown – “new normal”) during the morning. The continuous route
transect methodology was applied by the same observer in all beaches. The Analysis of Covariance (ANCOVA)
was used to investigate the response of community abundance to urbanization (raster-based variable) and time
of COVID-19 pandemic (lockdown vs. new normal). Rarefaction curve and Permutational Analysis of Variance
(PERMANOVA) were used to compare community richness and composition, respectively, between lockdown
and new normal periods. Generalized Linear Models (GLM) with negative binomial distribution were applied to
test the effect of the same predictors on the three more abundant species. The bird community structure and
composition did not change when comparing lockdown and new normal periods, mainly due to dominance of
synanthropic species. Among species-specific responses to lockdown, the Southern Lapwing Vanellus chilensis
was more abundant during the lockdown on six of the nine beaches where it occurred. Oppositely, the Kelp Gull
Larus dominicanus and the Neotropic Cormorant Nannopterum brasilianus were more abundant in new normal
period, reinforcing that these species benefit from human subsidies. This may provide a unique opportunity for
science-based sustainable ecotourism activities in urban areas with synanthropic species, capitalizing activities
such as birdwatching, that would certainly contribute to environmental education actions.
References
Ariyama, N., Moroni, M. & Hernandez, C. 2019. Molecular
identification of avian viruses in neotropic cormorants
(Phalacrocorax brasilianus) in Chile. The Journal
of Wildlife Diseases, 55(1), 105-112. https://doi.
org/10.7589/2017-10-256
Barboza, C., Mattos, G., Soares-Gomes, A., Zalmon, I.
& Costa, L. 2021. Low Densities of the Ghost Crab
Ocypode quadrata Related to Large Scale Human
Modification of Sandy Shores. Frontiers in Marine
Science, 8. https://doi.org/10.3389/fmars.2021.589542
Ben-Haddad, M., Hajji, S., Abelouah, M., Costa, L.,
Rangel-Buitrago, N. & Alla, A. 2022. Has the “Covid-19”
lockdown an impact on beach faunal communities?
The central Atlantic coast of Morocco as a case
study. Marine Pollution Bulletin. 185, 114259. DOI:
https://doi.org/10.1016/j.marpolbul.2022.114259
Bertucci, T., Silva, E., Marques Jr., A. & Monteiro Neto, C.
Tourism and Urbanization: Environmental Problems
of the Araruama Lagoon, State of Rio De Janeiro,
Brazil. Ambiente & Sociedade, 19(4), 59-80. https://doi.
org/10.1590/1809-4422asoc137111v1942016
Bibby, C., Jones, M. & Marsde, S. (eds.). 2000. Bird Surveys -
Expedition Field Techniques. London: Expedition Advisory
Centre of the Royal Geographical Society.
Bivand, F., Keitt, T. & Rowlingson, B. 2021. rgdal: Bindings
for the “Geospatial” Data Abstraction Library.
Brown, S., Hickey, C. & Harrington, B. (eds.). 2000.
United States Shorebird Conservation Plan. Manomet:
Manomet Center for Conservation Sciences.
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H.,
Colwell, R. K. & Ellison, A. M. 2014. Rarefaction and
extrapolation with Hill numbers: a framework for
sampling and estimation in species diversity studies.
Ecological Monographs, 84(1), 45-67. https://doi.
org/10.1890/13-0133.1
Coleman, J. & Milton, D. 2012. Feeding and roost site fidelity
of two migratory shorebirds in Moreton Bay, SouthEastern Queensland, Australia. The Sunbird, 42, 41.
Costa, L., Rangel, D. & Zalmon, I. 2023. The presence
of COVID-19 face masks in the largest hypersaline
lagoon of South America is predicted by urbanization
level. Marine Pollution Bulletin, 189, 114746. https://doi.
org/10.1016/j.marpolbul.2023.114746
Costa, L., Tavares, D., Suciu, M., Rangel, D. & Zalmon, I.
Human-induced changes in the trophic functioning
of sandy beaches. Ecological Indicators, 82, 304-315.
https://doi.org/10.1016/j.ecolind.2017.07.016
Delfino, H. C. & Carlos, C. J. 2021. Macro and micro-habitat
selection by Vanellus chilensis (Aves: Charadriiformes)
in southern Brazil. El Hornero, 36(1), 11-20.
MacGregor-Fors, I., Arbaláez-Cortés, E., Estela, F. A.,
Ocampo, D., Sánchez-Sarria, C. E., García-Arroyo, M.,
Aguirre-Samboní, G. K., Cortés-Díaz, D., Franco
Morales, J. C., Gaitán-García, C. D., Guerrero-Pelaez,
S., Gutiérrez Parodys, Y., Holguín-Ruiz, M., MezaAngulo, E., Vides, H. A. & Wilches-Vega, J. D. 2022.
Increases in avian diversity associated with COVID – 19
lockdowns in urban Colombia. Animal Biodiversity and
Conservation, 45(2), 553-572.
Gilby, B. L., Henderson, C. J., Olds, A. D., Ballantyne, J. A.,
Bingham, E. L., Elliott, B. B., Jones, T. R., Kimber,
O., Mosman, J. D. & Schlacher, T. A. 2021. Potentially
negative ecological consequences of animal
redistribution on beaches during COVID-19 lockdown.
Biological Conservation, 253, 108926. https://doi.
org/10.1016/j.biocon.2020.108926
Gil-Weir, K., Weir, E., Casler, C. L. & Aniyar, S. 2011.
Ecological functions and economic value of the
Neotropic Cormorant (Phalacrocorax brasilianus) in
Los Olivitos Estuary, Venezuela. Environment and
Development Economics, 16(5), 553-572.
Gordo, O., Brotons, L., Herrando, S. & Gargallo, G. 2020.
Rapid behavioural response of urban birds to COVID-19
lockdown. Biological Conservation, 253, 108926.
https://doi.org/10.1101/2020.09.25.313148
Hijmans, R. J. 2022. Geographic Data Analysis and
Modeling [R package raster version 3.6-3].
Coastal bird responses to COVID-19 lockdown
Ocean and Coastal Research 2024, v72:e24009 8
Rangel et al.
Je, J. 2020. A Review of Avian Influenza A Virus
Associations in Synanthropic Birds. Viruses. 12, 1209.
Jourdan, C., Fort, J., Pinaud, D., Delaporte, P., Gernigon, J.,
Lachaussée, N., Lemesle, J.-C., Pignon-Mussaud, C.,
Pineau, P., Robin, F., Rousseau, P. & Bocher, P. 2021.
Nycthemeral Movements of Wintering Shorebirds
Reveal Important Differences in Habitat Uses of Feeding
Areas and Roosts. Estuaries and Coasts, 44(5),
-1468. https://doi.org/10.1007/s12237-020-00871-5
Kennedy, C. M., Oakleaf, J. R., Theobald, D. M., BaruchMordo, S. & Kiesecker, J. 2019. Managing the middle:
A shift in conservation priorities based on the global
human modification gradient. Global Change Biology,
(3), 811-826. https://doi.org/10.1111/GCB.14549
Kennedy, C., Oakleaf, J., Theobald, D., Baruch‐mordo, S.
& Kiesecker, J. 2019. Managing the middle: A shift in
conservation priorities based on the global human
modification gradient. Global Change Biology, 25(3),
-826. https://doi.org/10.1111/gcb.14549
Kjerfve, B., Schettini, C., Knoppers, B., Lessa, G. &
Ferreira, H. O. 1996. Hydrology and salt balance in a
large, hypersaline coastal lagoon: Lagoa de Araruama,
Brazil. Estuarine, Coastal and Shelf Science, 42, 701–
https://doi.org/10.1006/ecss.1996.0045
Lafferty, K. D. 2001. Birds at a Southern California Beach:
Seasonality, Habitat Use and Disturbance by Human
Activity. Biodiversity and Conservation, 10, 1949–1962.
https://doi.org/10.1023/A:1013195504810
Lewis, J., Collison, J. & Pillay, D. 2022. Effects of COVID-19
lockdowns on shorebird assemblages in an urban South
African sandy beach ecosystem. Scientific Reports, 12(1),
https://doi.org/10.1038/s41598-022-09099-8
Møller, A. P., Díaz, M., Flensted-Jensen, E., Grim, T.,
Ibáñez-Álamo, J. D., Jokimäki, J., Mänd, R., Markó, G.
& Tryjanowski, P. 2015. Urbanized birds have superior
establishment success in novel environments.
Oecologia. https://doi.org/10.1007/s00442-015-3268-8
Murchison, C. R., Zharikov, Y. & Nol, E. 2016. Human Activity
and Habitat Characteristics Influence Shorebird Habitat
Use and Behavior at a Vancouver Island Migratory
Stopover Site. Environmental Management, 58(3),
-398. https://doi.org/10.1007/s00267-016-0727-x
Noy-Meir, I. 1979. Structure and function of desert
ecosystems. Israel Journal of Plant Sciences.
(1), 1-19. DOI: https://doi.org/10.1080/002121
X.1979.10676851
R Core Team. 2022. R: A language and Environment for
Statistical Computing.
Rangel, D.F., Castro Tavares, D., Zalmon, I.R., 2020.
Composição e abundância de aves marinhas costeiras
em Arraial do Cabo, Estado do Rio de Janeiro, Brasil.
Ornithologia 11(1), 1-6
Rutz, C., Loretto, M.C., Bates, A.E., Davidson, S.C., Duarte,
C.M., Jetz, W., Johnson, M., Kato, A., Kays, R., Mueller, T.,
Primack, R.B., Ropert-Coudert, Y., Tucker, M.A.,
Wikelski, M., Cagnacci, F., 2020. COVID-19 lockdown
allows researchers to quantify the effects of human
activity on wildlife. Nature Ecology and Evolution. 4,
–1159. https://doi.org/10.1038/s41559-020-1237-z
Santos, E. S. & Macedo, R. H. 2011. Load lightening in
southern lapwings: group‐living mothers lay smaller eggs
than pair‐living mothers. Ethology, 117(6), 547-555.
Scarton F. 2017. Long-term trend of the waterbird
community breeding in a heavily man-modified coastal
lagoon: the case of the Important Bird Area “Lagoon of
Venice”. Journal of Coastal Conservation, 21, 35-45.
Sheaves, M., Baker, R., Nagelkerken, I. & Connolly, R. M.
True value of estuarine and coastal nurseries for
fish: incorporating complexity and dynamics. Estuaries
Coasts, 38, 401-414.
Tavares, D. C., Guadagnin, D. L., Moura, J. F., Siciliano, S.
& Merico, A. 2015. Environmental and anthropogenic
factors structuring waterbird habitats of tropical coastal
lagoons: Implications for management. Biological
Conservation, 186, 12-21. https://doi.org/10.1016/j.
biocon.2015.02.027
Tavares, D. C. & Siciliano, S. 2013. An inventory of wetland
non-passerine birds along a southeastern Brazilian
coastal area. Journal of Threatened Taxa, 5(11),
-4597. https://doi.org/10.11609/JoTT.o3424.4586-97
Thompson, B. S. 2022. Blue bonds for marine conservation
and a sustainable ocean economy: Status, trends, and
insights from green bonds. Marine Policy, 144, 105219.
Underwood, A.J., 1992. Beyond BACI: the detection of
environmental impacts on populations in the real, but
variable, world. Journal of Experimental Marine Biology
and Ecology, 161, 145-178.
Velando, A. & Munilla, I. 2011. Disturbance to a foraging
seabird by sea-based tourism: Implications for reserve
management in marine protected areas. Biological
Conservation, 144(3), 1167-1174.
Zuur, A. F., Ieno, E. N. & Elphick, C. S. 2010. A protocol
for data exploration to avoid common statistical
problems: data exploration. Methods in Ecology and
Evolution, 1(1), 3-14. https://doi.org/10.1111/j.2041-
X.2009.00001.x
