key: cord-0758713-vm2jn7m8
authors: Magalhães, Karine Matos; de Souza Barros, Kcrishna Vilanova; de Lima, Maria Cecília Santana; de Almeida Rocha Barreira, Cristina Cristina; Filho, José Souto Rosa; de Oliveira Soares, Marcelo
title: Oil spill + COVID-19: a disastrous year for Brazilian seagrass conservation
date: 2020-10-18
journal: Sci Total Environ
DOI: 10.1016/j.scitotenv.2020.142872
sha: 3894b430b0d7ef19f8f9f1168814de54fa6ade67
doc_id: 758713
cord_uid: vm2jn7m8

The COVID-19 pandemic has been the greatest global public health threat of the 21st century. Additionally, it has been challenging for the Brazilian shores that were recently (2019/2020) affected by the most extensive oil spill in the tropical oceans. Monitoring programs and studies about the economic, social and ecological consequences of the oil disaster were being carried out when the COVID-19 (coronavirus disease 2019) pandemic was declared, which has heavily affected Brazil. For Brazilian seagrasses conservation, this scenario is especially challenging. An estimated area of +325 km2 seagrass meadows was affected by the 2019 oil spill. However, this area is undoubtedly underestimated since seagrasses have not yet been adequately mapped along the 9000 km-long Brazilian coast. In addition to scientific budget cuts, the flexibilization of public and environmental policies in recent years and absence of systematic field surveys due to COVID-19 has increased the underestimation of affected seagrass areas and ecosystem service losses due to the oil spill. Efforts to understand and solve the oil spill crisis were forced to stop (or slow down) due to COVID-19 and the economic crisis, leaving ecosystems and society without answers or conditions to identify the source(s) that was/were responsible for this spill, mitigate the damage to poor communities, promote adequate impact assessment or restoration plans, or properly monitor the environment. Our results highlight that pandemic and large-scale environmental disasters may have had a synergistic effect on the economy (e.g., artisanal fisheries and tourism), public health and ecology, mainly due to government inaction, social inequality and poorly studied tropical ecosystems. The results of this study also demonstrate the need to analyze the short- and long-term impacts of the combined effects (oil spill + COVID-19) on the recovery of the economy and coastal ecosystems.

By the end of August 2019, crude oil from a "mysterious" source (Escobar, 2019) started to appear and spread over more than 3000 km along the Brazilian coast. Almost immediately, several groups including NGOs, state universities, research institutes, local communities, and the general public/volunteers started manually collecting oil without appropriate techniques or coordination with the Federal Government (Brum et al., 2020; Soares et al., 2020a) . Geochemical characteristics of the oil material indicate that it is a heavy oil compatible with Venezuelan sedimentary basin , with the oil that was found along the 3000km coast likely from the same source (Lourenço et al., 2020) . It is crude oil that was badly weathered at sea or a product manufactured with heavy oil produced in Venezuela (Oliveira et al., On the other hand, seagrass meadows are being threatened all over the world, with alarming cover loss rates caused by both natural and anthropogenic sources (Waycott et al., 2009; Orth, 2006; Griffiths et al., 2020) . In Brazilian meadows, this scenario is not different (Copertino et al., 2016) , but has been especially challenging this past year (2019/2020). An estimated area of 325 km 2 of seagrass meadows was affected by the oil spill disaster (Magris and Giarrizzo, 2020) . However, this number is undoubtedly underestimated since seagrass meadows have not yet been fully mapped along the 9000 km-long Brazilian coast (Copertino et al., 2016) , and few researchers have been monitoring these ecosystems (Fig. 1) . Besides scientific budget cuts in recent years, the absence of systematic field surveys due to COVID-19 increases the underestimation of seagrass meadow area affected by the oil spill and the degree and specific ecosystem services affected by such disaster.

Monitoring programs and studies about the economic and ecological consequences of the coastal ecosystems and populations, especially fishermen, were being put in place by a few state research agencies in late 2019 and early 2020. However, in March 2020, the Coronavirus disease (COVID-19) pandemic was declared (World Health Organization, 2020) and heavily affected Latin America after Europe and Asia. Since then, Brazil has the emarginata Hartog, Halodule wrightii Asch., Halophila baillonii Asch., Halophila decipiens Ostenf. and Ruppia maritima L.) (Copertino et al., 2016; Magalhães and Barros, 2017) including unique and rare populations of H. beaudettei (one population) and H. baillonii (2 populations) (Fig. 1) . In this context, the area affected by the oil spill overlaps (Magris and Giarizzo, 2020; Soares et al. 2020a ) with the distribution of the main eco-engineering seagrass species. Therefore, it has affected different types of vegetated ecosystems throughout the distribution area of these tropical benthic habitats. The region also has the most diverse, extensive, and exuberant Brazilian seagrass meadows (Magalhães et al., 2015; Barros et al., 2016; Copertino et al., 2016; ) .

The impact of oil on seagrasses varies according to the oil type, degree and time of exposure and affected species, which can result in mortality and reduce their tolerance to other stressors (Zieman and Zieman, 1989) . The variety of oil scenarios and responses leads to a lack of consensus about the degree and overall impacts on the seagrass communities, indicating a situation that is more scenario-dependent than species-dependent (Fonseca et al., 2017) . The hydrophobic nature of oil molecules allows them to bind to membrane cells of aquatic plants, which rapidly reaches the thylakoid (where the photosynthetic apparatus is located) and accumulates, causing membrane oxidation and damaging photosynthesis and respiration (Marwood et al., 1999) .

Thus, disperse oil can reduce shoot and flower densities, plant growth, and area loss (Thorhaug and Marcus, 1987; Marshall, 1990; Dean et al., 1998; Kenworthy et al., 2015) . Mutagenic and carcinogenic substances can be incorporated into plant tissues and can decrease tolerance to other stressors J o u r n a l P r e -p r o o f Journal Pre-proof and transfer these substances to primary and secondary consumers (Zieman and Zieman, 1989) .

In addition to its effects on vegetation, oil spills can have a profound and selective influence on the various animals and plants inhabiting seagrass meadows (den Hartog and Jacobs, 1980) , which is the present case along the Brazilian coastline. Thus, Lourenço et al. (2020) detected that light hydrocarbons were still present in the oil from the mysterious Brazilian spill.

Chemical characterization of this oil (Lourenço et al., 2020; Oliveira et al., 2020) showed that light hydrocarbons were still present, increasing the probability of negative effects and ecotoxicological risks to organisms in seagrass beds upon release in the water column. Therefore, the associated fauna and flora may be killed, poisoned, smothered, fouled, and asphyxiated, reducing their commercial demand and value (Zieman and Zieman, 1989 ; Taylor and Rasheed, 2011) ( Fig. 2 a,b ,c,d).

Brazilian seagrasses shelter and attract diverse invertebrate and fish fauna with high ecological and economic importance (Pereira et al., 2010; Barros et al., 2016; Costa et al., 2020) , including threatened species as the manatee (Trichechus manatus Linnaeus, 1758) and the green sea turtle (Chelonia mydas Linnaeus, 1758). Since it requires habitats with seagrass, manatee sightings drastically diminished at the Federal Protected Area (APA do Delta do Parnaíba) a few weeks after the accident, according to the NGO Comissão Ilha Ativa, which recorded crude oil on seagrass leaves (Portal do Dia, 2020) . After the Deepwater Horizon oil spill, a model was proposed as an attempt to estimate the number of manatees in areas potentially affected by oil J o u r n a l P r e -p r o o f Journal Pre-proof (Martin et al., 2014) , but the impact of the oil on these animals has still not been studied sufficiently. However, official reports have declared that sea turtles seem to be the most affected fauna, representing 66% of the 159 oiled marine animals registered (IBAMA, 2020) (Fig. 2c ).

Since seagrasses are distributed in shallow waters and intertidal areas in the Tropical Southwestern Atlantic (Northeast region of Brazil), meadows have been affected both directly and indirectly by the oil spill. In the eastern portion of the Northeastern coast, crude oil was registered between seagrass leaves in many locations at Carneiros Beach, Pernambuco state. At this location, seagrasses not only suffered from the oil but from the cleaning process by the local population, who tore seagrass leaves as they collected oil by hand. On this beach, small oil stains were observed in the sediments until January 2020. The initial monitoring activities also registered an indirect impact of the oil, which remained in the meadows and percolated underground, in Suape Bay, Pernambuco. Unfortunately, as a result of the COVID-19 quarantine, this monitoring was suspended. At a manatee sanctuary in Japaratinga, Alagoas state, small amounts of oil reached the beach almost daily for at least four months, reaching the seagrass meadow at low tides. In this area, massive mortality of the cockle Tivela mactroides (Born, 1778) was reported, affecting artisanal fisheries of this bivalve (Fig. 2d) .

After the broad publication of images and alerts from the regions that were first affected, non-governmental organizations and civil society along the northern sector of the Brazilian coast were on alert, which lead to most oil being rapidly collected at sea or along the beaches (Soares et al., 2020b) pandemic. The oil spill temporarily decreased (or eliminated in some areas) catches of fishes, crustaceans, and mollusks, and also drastically reduced fish

The federal government's response to the oil spill was very late, slow, and uncoordinated (Brum et al., 2020; Soares et al., 2020a Soares et al., , 2020b , making local governments, universities and NGOs responsible for initial mobilization and research (Fig. 2f) Even without financial support, field activities started in January 2020, especially in Pernambuco State, to select monitoring areas, focusing on sites with data from before the disaster. Nonetheless, as the COVID-19 pandemic was declared, research field activities were suspended, and no money has been allocated to research projects (updated in September 2020). Such suspension is probably the worst effect of the quarantine on these studies since field activities were interrupted before management tools and strategies could be tested or implemented. Most universities and research centres were closed and remain so, with no reopening dates, leaving most samples that were collected before March 2020 unprocessed/ unanalyzed.

During the Brazilian COVID-19 quarantine that started on March 16, 2020, a new wave of oil arrived on the shores of at least six states (Brazilian Navy, 2020) after a week of strong winds, high waves and spring tides. Oil samples analyzed from this event proved to be from the same source as the 2019 disaster (Brazilian Navy, 2020). As verified by our field team, this new arrival confirms that the oil is still out there, buried in intertidal, estuarine, and seafloor sediments or trapped in coral reefs, and is still negatively affecting coastal and marine systems. However, since the pandemic was declared, researchers have been unable to maintain studies, and all financial support was reallocated to combat COVID-19.

It is still early to assess the real impacts of this massive oil spill on the seagrass meadows on the Brazilian coast, especially in light of the unknown origin of the oil, amount of oil spilt, unexpected recurrences, and the necessary COVID-19 quarantine, but effective actions are urgent. Although the visual effects of the disaster have almost disappeared, monitoring the affected areas is highly recommended, and mitigation and restoration are essential. In this way, ecosystem services provided by seagrass meadows should drive studies and efforts, since seagrasses act as blue carbon storage and nursery grounds for commercial species, and since much of the biodiversity associated with seagrass meadows may have been lost. Furthermore, since all six seagrass species are in the affected area (Fig. 1) , species-dependent effects should also be addressed.

The oil spill and the pandemic of COVID-19 were not only environmental and health issues, but have also highlighted the need for public policies regarding labour, social security and social assistance, as well as for the protection of coastal ecosystems , whose quality and ecosystem services are essential for thousands of families along the coast of Northeastern Brazil. Our discussion highlights that pandemic and large-scale environmental disasters may have caused a negative combination of economic (e.g., artisanal fisheries and tourism), public health, and ecological impacts, mainly due to government inaction, prolonged social isolation, social inequality and poorly studied tropical ecosystems. Moreover, efforts to understand and solve the oil spill crisis were forced to slow down or stop, leaving both ecosystems and society without answers and conditions to identify the primary source of this spill, mitigate the damage, promote adequate impact assessment, J o u r n a l P r e -p r o o f determine pollution effects, implement restoration plans or properly monitor the environments. These results also highlight the need to analyze the short-and long-term impacts of these combined effects (oil spill + COVID-19) and recover the economy, public policies, and coastal ecosystems.

The affected seagrass meadows and traditional local human communities on the Brazilian coast should receive attention in the forthcoming years due to the short, medium, and long-term impacts of this large oil spill (Brum et al., 2020; Shakil et al., 2020; Soares et al., 2020a) and  which has severely affected their main sources of food and income were, especially after the quarantine. Monitoring programs, adequate scientific budgets and proper response measures must be implemented to minimize the cultural, spiritual, ecological, economic, and social effects of the spill and COVID-19 in affected states, localities and poorly studied vegetated ecosystems (Araújo et al., 2020; Soares et al., 2020b) .

To elucidate the real magnitude of these impacts and to contribute to the restoration of the affected seagrass beds, we emphasize the utmost need for policies and research focused on the following key issues: (1) assessments of the severity of impacts on seagrass beds and connected coral reefs, sandy beaches and mangroves using approaches based on comparisons of past and present data (including satellite imagery); (2) experimental oil exposure studies on seagrass and fauna must be conducted with the specific kind of mysterious oil that reached the Brazilian coast, in different quantities, to understand the impacts at the ecosystem level; (3) identification of oil toxicity and its residues on marine organisms and in food webs using proxies such as stable isotope ratios, plant photosynthetic rates and DNA damage; (4) development of novel J o u r n a l P r e -p r o o f analytical techniques for chemical detecting of oil-derived compounds at low concentrations in water to predict the approach of oil before it arrives in the coast, allowing early actions to prevent oil from reaching environments such as seagrass; (5) the effects of a prolonged COVID-19 quarantine on the health of seagrass meadows and fishing activities, especially on artisanal fishermen, indigenous people, and quilombolas (African-slave descendants). The development of community-based restoration efforts (Soares et al., 2020b; Nasri Sissini et al., 2020) and sustainable economic activities are particularly important to help recover seagrass beds and communities doubly affected by the largest oil spill ever recorded in Brazilian history and the COVID-19 pandemic that has heavily impacted social inequality and poor communities.

The synergistic impacts of a massive oil spill that happened on the Brazilian coast in 2019, with oil recurrence in 2020, and the COVID-19 pandemic in socio, cultural, economic and ecological reflections have been disastrous. As the quarantine was imposed, budgets for ecosystem restoration actions, e.g. seagrass beds, were cut and ecological monitoring activities were stopped and are still restricted in September 2020. The Brazilian Federal government's response to both disasters was slow, late and unorganized, potentiating the negative consequences of both. For future policies and research about the oil spill, we urge that the main focuses should be the chronic and acute toxicity of the oil to plant, animal and human communities, loss of ecosystem services, and the effects of prolonged COVID-19 quarantine on J o u r n a l P r e -p r o o f seagrasses and traditional communities which use them as their source of income or food. As a long-term strategy, the data generated by the next years' research should be incorporated in a National Governmental action plan for oil spill rescue in different levels and ecosystems. 

Seagrass Meadows on the Northeast Coast of Brazil: Habitat Influence on the Spatial and Seasonal Variations

Environmental effects of the Deepwater Horizon oil spill: A review

BRAZILIAN NAVY -Marinha do Brasil. Comando de Operações Navais

The moment to see the poor

Brazil oil spill response: Government inaction

Seagrass and rhodolith beds are important seascapes for the development of fish eggs and larvae in tropical coastal areas

Eelgrass (Zostera marina L.) in Prince William Sound, Alaska: Effects of the Exxon Valdez oil spill

Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches: a preliminary study of the "Prestige" oil spill

Effects of the 'Amoco Cadiz' Oil Spill on the Seagrass Community at Roscoff with Special Reference to the Benthic Infauna

Critical gaps in seagrass protection reveal the need to address multiple pressures and cumulative impacts

Brasileiro do Meio Ambiente e dos Recursos Renováveis

Seagrass response following exposure to Deepwater Horizon oil in the Chandeleur Islands, Louisiana (USA)

The dark cloud with a silver lining: Assessing the impact of the SARS COVID-19 pandemic on the global environment. Sci. Total and southeast seaboard (2019-2020): Trying to find answers and filling data gaps

Halophila baillonis Ascherson: first population dynamics data for the Southern Hemisphere

Halodule genus in Brazil: A new growth form

Mysterious oil spill in the Atlantic Ocean threatens marine biodiversity and local people in Brazil

Department of the Interior, Minerals Management Service, publication number MMS 90-0031. Gulf of Mexico OCS Region

COVID-19 -6 million cases worldwide and an overview of solar radiation

Brazil oil spill response: Protect rhodolith beds

Seagrass ecosystem services -What's next?

Global significance of seagrass fishery activity

Environmental disaster in the northeast coast of Brazil: Forensic geochemistry in the identification of the source of the oily material

Community structure of the ichthyofauna associated with seagrass beds (Halodule wrightii) in Formoso River estuary -Pernambuco

Após vazamento de óleo, peixes-boi desaparecem de santuário no PI

The experience of Pernambuco's fishing communities with the oil and the coronavirus tragedies

Current state of seagrass ecosystem services: Research and policy integration

The macrofaunal communities in the shallow subtidal areas for the first 3 years after the Hebei Spirit oil spill

Política pública da previdência social e trabalhadores da pesca artesanal: dilemas estruturais em contextos conjunturais do covid-19

COVID-19 and the environment: A critical review and research agenda

Brazil oil spill response: Time for coordination

Oil spill in South Atlantic (Brazil): Environmental and governmental disaster

Initial effects of a moderate-sized oil spill on benthic assemblage structure of a subtropical rocky shore

COVID-19: Healthy environmental impact for marine habitat monitoring in high-risk areas

Oil spill clean-up: The effect of three dispersants on three subtropical/tropical seagrasses

Accelerating loss of seagrasses across the globe threatens coastal ecosystems

Virtual press conference on COVID-19

Indirect effects of COVID-19 on the environment

The ecology of the seagrass meadows of the west coast of Florida: a community profile

Karine Magalhaes: Conceptualization, Writing -Original, Methodology, Writing -Review & Editing, Visualization

Writing -Original, Methodology, Writing -Review & Editing, Visualization Maria Cecilia S Lima: Writing -Review & Editing, Visualization

The authors are grateful to Paulo Freitas for help with the graphical abstract diagramming. Kcrishna Barros