Immediate effects of the 2019 oil spill on the macrobenthic fauna associated with macroalgae on the tropical coast of Brazil
Introduction
Oil spills are one of the most destructive environmental impacts in marine ecosystems, particularly coastal zones, and can affect human populations, the physical environment and biota at all trophic levels (Weiss, 2015; McLachlan and Defeo, 2018). Biota are impacted by high toxicity of oil components, mainly hydrocarbons, which can represent 90% of the total chemical compounds (Tissot and Welte, 1984; UNEP, 1992; NRC, 2003). Oil can severely impact faunal and floral populations by physical (smothering, reduced light), habitat (altered pH, decreased dissolved oxygen, decreased food availability), and ecotoxicological effects (Kennish, 1997; Weiss, 2014, Weiss, 2015; Yim et al., 2020). Several studies have demonstrated the effects of petroleum derived compounds on organisms, which include changes in their swimming capacities, prey capture, predation and reproduction, thus demonstrating sublethal and lethal effects on abundance and diversity (Maciel et al., 2015; Torreiro-Melo et al., 2015; Weiss, 2015). In this sense, assessing the acute (short-term) and chronic (long-term) impacts of oil spills on marine biodiversity is of utmost importance (Weiss, 2014; Yuewen and Adzigbli, 2018).
Traces of crude oil from a “mysterious” source were recorded for the first time in late August of 2019 in a few localities on the Northeast Coast of Brazil (Escobar, 2019; Araujo et al., 2020). The oil spread rapidly during the following months, reaching more than 3000 km along the Brazilian coast by January of 2020 (Lourenço et al., 2020; Magris and Giarrizzo, 2020). More than 5000 tons of crude oil had already been removed within approximately five months (Brum et al., 2020). However, stranded oil fragments in some of the affected areas have been reported by the media since then and are expected to keep appearing sporadically for years to come due resuspension from the continental shelf and/or mangroves (Lourenço et al., 2020). In the meantime, geochemical analyses have found that the crude oil that reached the Brazilian Coast was compatible with Venezuelan oil (Oliveira et al., 2020). The oil reached 1000 localities and 55 marine protected areas (Soares et al., 2020b), affecting several coastal ecosystems such as mangroves (489.83 km2), beaches (185.3 km2), intertidal coral reefs (45.95 km2) (Magris and Giarrizzo, 2020) and seagrass meadows (Magalhães et al., 2020). This disaster represents the most extensive and most severe environmental impact for the Brazilian coast, the South Atlantic Ocean, and tropical oceans so far (Soares et al., 2020a, Soares et al., 2020b).
Along the 194 km long Pernambuco coast, coral reefs are very abundant on the inner shelf, occurring parallel to the coastline as patches or elongated bank reefs attached to the coast or at depths of 5–10 m (Laborel, 1970; Laborel-Deguen et al., 2019). These coastal reefs, first described by Darwin (1841), are basically rocky bodies composed of mostly quartz sand grains, cemented by calcium carbonate. The intertidal reefs are densely colonized by macroalgal assemblages that are typically found in the tropical phytogeographic region (Horta et al., 2001). Most of the 1676 tons of oil that arrived on the coast of Pernambuco was deposited between October 19 and 28 of 2019 (Brazilian Navy, 2019; SPG, 2019; Câmara et al., 2020). Upon reaching the coast, oil stains quickly covered extensive areas of sandy beaches and coral reefs with a thick layer of oil. Immediately after the wide publication of images and alerts broadcast on television, non-governmental organizations and civilians started collecting the oil, mainly by hand (frequently without adequate protection), and much oil was rapidly collected at sea or along the beaches (Soares et al., 2020b).
The impacts of the oil arrival were acute and immediate, killing turtles, fish, dolphins and birds, in addition to decimating millions of small animals as invertebrates and plants, whose deaths were not easily perceived by the naked eye. Although less “popular” to the general public, these small organisms are key components of complex food webs and may be good indicators of hidden environmental impacts (Roberts et al., 2008). Despite this, no detailed studies about the consequences of the Brazilian oil spill on macrobenthic fauna have been published until now. Besides impacting several coastal ecosystems, the oil spill severely affected traditional fishing communities (artisanal fishing), since seafood items, such as mollusks, crustaceans and fishes, that constitute the basis of their diets and income were no longer allowed to be sold or consumed (Araujo et al., 2020; Ramalho and Santos, 2020).
Although several studies about the marine life of Pernambuco have been conducted since 1950, surprisingly little information exists concerning reef intertidal communities. In July 2019, a research project was started to understand the role of macroalgae morphology and chemical composition in structuring macrobenthos at Paiva beach (one of the best-preserved Brazilian coral reefs), and on the 21st of October 2019 LaBen's researchers were collecting samples on this beach when oil stains started arriving at the reefs. During the 2019 oil spill these reefs were severely impacted, since more than 1000 tons of oil were collected in just one week in the Cabo de Santo Agostinho municipality, where the Paiva's reefs are located (week between 19 and 28 October 2019) (SPG, 2019). This presented a unique opportunity to study the acute (short-term) effects of crude oil on the benthic macrofauna associated with seaweed in tropical coastal reefs. This paper describes the immediate impacts of the 2019 oil spill on the structure of macrobenthic communities associated with Jania capillacea and Penicillus capitatus on coastal coral reefs of Paiva beach (Northeastern Brazil).
Section snippets
Study area
Paiva beach (8°16′46.4″S and 34°56′47.1″W) is an open ocean sandy beach approximately 7.8 km long (Holanda et al., 2020) (Fig. 1). Paiva beach, located on the southern Pernambuco coast, has also some of the best-preserved coral reef areas on the tropical coast of Brazil (Vasconcelos et al., 2019) and is surrounded by two Protected Areas (MPA Estuários dos rios Jaboatão e Pirapama and PA Mata de Camaçari) (Barbosa, 2016). The climate is tropical hot/humid, with average annual temperatures above
Results
A total of 19,446 specimens belonging to 40 taxa were collected (Jania capillacea - 16,702 individuals, 35 taxa; Penicillus capitatus - 2744 individuals, 31 taxa). The main phyla were Cnidaria, Platyhelminthes, Annelida, Mollusca, Arthropoda and Echinodermata. Crustaceans were dominant in both algae, particularly amphipods and the isopod Janaira gracilis. In addition to these taxa, ostracods and tanaids were the most abundant crustaceans in J. capillacea algae. Among polychaetes, the second
Discussion
Significant differences were observed in the structure of epibenthic fauna associated with macroalgae after the oil spill. The immediate effects of oil on epifauna were distinct among algae, being stronger in J. capillacea than in P. capitatus, as indicated by the significant changes on richness and abundance values of the communities associated with J. capillacea on the week of the arrival, and its slower recovery posteriorly. Since Jania generally occurs around tide pool borders, they may be
Funding declaration
None.
CRediT authorship contribution statement
Nykon Craveiro: Resources, Conceptualization, Methodology, Investigation, Writing – original draft, Writing – review & editing. Rodrigo Vinícius de A. Alves: Investigation, Writing – original draft, Writing – review & editing. Juliana Menezes da Silva: Investigation, Writing – review & editing. Edson Vasconcelos: Writing – review & editing. Flavio de Almeida Alves-Junior: Writing – review & editing. José Souto Rosa Filho: Project administration, Resources, Conceptualization, Methodology,
Declaration of competing interest
The authors declare that there is no competing interest.
Acknowledgements
The authors would like to thank Universidade Federal de Pernambuco - UFPE for financing the project “Monitorando os efeitos do óleo na costa pernambucana. O antes e o depois da chegada do óleo nas comunidades bentônicas” (edital 09/2019 - edital emergencial para o enfrentamento de questões relativas ao óleo que atinge as praias pernambucanas) process number: 23076.057497/2019-78. Also, we would like to thank the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco - FACEPE for
References (80)
- et al.
Evaluation of the impacts of oil spill disaster on communities and its influence on restiveness in Niger Delta, Nigeria
Procedia Engineering
(2018) - et al.
Response of benthic macrofauna to an oil pollution: lessons from the “Prestige” oil spill on the rocky shore of Guéthary (south of the Bay of Biscay, France)
Deep-Sea Res. II Top. Stud. Oceanogr.
(2014) The effect of wave exposure on the amphipod fauna of the alga Caulerpa brownii
J. Exp. Mar. Biol. Ecol.
(1976)- et al.
Assessment of Jessica oil spill impacts on intertidal invertebrate communities
Mar. Pollut. Bull.
(2003) - et al.
Bacterial accumulation by Branchiomma luctuosum (Annelida: Polychaeta): a tool for biomonitoring marine systems and restoring polluted waters
Mar. Environ. Res.
(2007) - et al.
Evaluation of macroalgae and amphipods as bioindicators of petroleum hydrocarbons input into the marine environment
Mar. Pollut. Bull.
(2019) - et al.
Mysterious oil spill along Brazil’s northeast and southeast seaboard (2019–2020): trying to find answers and filling data gaps
Mar. Pollut. Bull.
(2020) - et al.
Mysterious oil spill in the Atlantic Ocean threatens marine biodiversity and local people in Brazil
Mar. Pollut. Bull.
(2020) - et al.
The effects of the Braer oil spill on rocky intertidal communities in South Shetland, Scotland
Mar. Pollut. Bull.
(1995) - et al.
Contamination of marine biogenic habitats and effects upon associated epifauna
Mar. Pollut. Bull.
(2008)
The macrofaunal communities in the shallow subtidal areas for the first 3 years after the Hebei Spirit oil spill
Mar. Pollut. Bull.
Oil spill in South Atlantic (Brazil): Environmental and governmental disaster
Marine Policy
Bioconcentration of phenanthrene and metabolites in bile and behavioral alterations in the tropical estuarine guppy Poecilia vivipara
Chemosphere
Rapid recovery of coastal environment and ecosystem to the Hebei Spirit oil spill’s impact
Environment International
Initial impacts of the Hebei Spirit oil spill on the sandy beach macrobenthic community west coast of Korea
Mar. Pollut. Bull.
PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods
Artisanal fishers, consumers and the environment: immediate consequences of the oil spill in Pernambuco, Northeast Brazil
Cadernos de Saúde Pública
Biology and new records of the invasive species Branchiomma bairdi (Annelida: Sabellidae) in the Mediterranean Sea
Medit. Mar. Sci.
Entrepreneurial urban planning in real estate, residential and service complexes: Reserva do Paiva under analysis
Cadernos Metrópole
Large-scale risk assessment of polycyclic aromatic hydrocarbons in shoreline sediments from Saudi Arabia: environmental legacy
Saccate thallus of the red alga Halosaccion glandiforme harbor diverse invertebrate fauna
International Aquatic Research
Comando de Operações Navais. Note the press in: 08/07/2019
Brazil oil spill response: government inaction
Science
Socioeconomic vulnerability of communities on the Brazilian coast to the largest oil spill (2019–2020) in tropical oceans
Ocean & Coastal Management
The structure of gammarid amphipod (Crustacea, Peracarida) assemblages associated with Sargassum (Phaeophyta, Fucales) and their link with the structural complexity of algae
Hydrobiologia
Macrobenthos of the nearshore Aleutian Archipelago, with emphasis on invertebrates associated with Clathromorphum nereostratum (Rhodophyta, Corallinaceae)
Mar. Biodivers.
Change in Marine Communities: An Approach to Statistical Analysis and Interpretation
Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation
Mar. Ecol. Prog. Ser.
On a remarkable bar of sandstone off Pernambuco on the coast of Brazil
The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science
Remediation technologies for marine oil spills: a critical review and comparative analysis
Am. J. Environ. Sci.
Hydrography and currents on the Pernambuco Continental Shelf
Brazilian Journal of Water Resources
Mystery oil spill threatens marine sanctuary in Brazil
Science
Heavy metals in five Sabellidae species (Annelida, Polychaeta): ecological implications
Environ. Sci. Pollut. Res.
Small-scale experimental contamination with diesel oil does not affect the recolonization of Sargassum (Fucales) fronds by vagile macrofauna
Zoologia
Polychaete assemblages and sediment pollution in a harbour with two opposing entrances
Helgol. Mar. Res.
Habitat architecture and the abundance and body-size-dependent habitat selection of a phytal amphipod
Ecology
The macro and microfauna associated with Fucus serratus L. with some ecological remarks
Ophelia
Morphodynamic classification, variations and coastal processes of Paiva beach
Revista Brasileira de Geomorfologia
Considerações sobre a distribuição e origem da flora de macroalgas brasileiras
Hoehnea
Impacts on intertidal epibiota: Exxon Valdez spill and subsequent clean-up
Cited by (31)
Traces of oil in sea turtle feces
2024, Marine Pollution BulletinPAH residues and toxicity levels two years after an extensive oil spill on the northeast Brazilian coast
2024, Marine Pollution BulletinMarine amphipods as integral members of global ocean ecosystems
2024, Journal of Experimental Marine Biology and EcologyForaminifera associated with macroalgae on tropical coastal sandstone reefs
2024, Marine MicropaleontologyMethodology for the estimation of an oil spill origin: Analysis of the 2019 Brazilian coast oil spill
2023, Marine Pollution Bulletin