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Diversity and turnover in a rocky shore intertidal community of an upwelling region (Arraial do Cabo, Brazil)

Abstract

The present study describes the community diversity and gives a seasonal distribution of an intertidal macroalgal assemblage at Prainha Beach, Arraial do Cabo City in Rio de Janeiro state, Brazil. Sampling was performed during four seasons of a 1-year period. Organisms were sampled and photographed using photoquadrats to quantify relative coverage. Ninety-six taxa of macroalgae were registered, including 23 chlorophytes, 19 ochrophytes, and 54 rhodophytes, while three barnacles, seven mollusks, one isopod, and one polychaete were recorded among the zoobenthos. In the upper intertidal zone, the coverage was frequently dominated by invertebrates. Macroalgae always dominated the middle and lower zones, covering almost 100 % in both zones. The highest values of species diversity (H’), richness (S), and turnover rates were found during the transition from spring to summer, which coincided with the upwelling period. A comparison with the 1980’s flora revealed that the major changes in the macroalgal assemblage were among species belonging to the same genera, unless new additions were provided. The combination of photoquadrats and minimally destructive sampling allowed a detailed description of the composition and structural characteristics of the intertidal zone, a methodology that should be applied to study protected marine areas.

Key words
intertidal benthic communities; macroalgae; southwestern atlantic ocean; seasonal variability; upwelling system

INTRODUCTION

Rocky shores are dynamic coastal environments that are considered to be zones of transition between aquatic and terrestrial ecosystems and are inhabited predominantly by specially adapted marine organisms (Ros et al. 1985ROS JD, ROMERO J, BALLESTEROS E & GILI JM. 1985. Diving in Blue Water. The Benthos. The Western Mediterranean [(R Margalef Ed)], 1st ed., Buckley: Pergamon Press Oxford, p. 233-295.). The diversity and productivity of rocky shores are associated with the presence of marine macroalgae, which are the main primary producers and serve as substrate, shelter, and reproduction sites for many vertebrates and marine invertebrates (Széchy et al. 2001SZÉCHY MTM, VELOSO VG & PAULA EJ. 2001. Brachyura (Decapoda, Crustacea) of phytobentic communities of the sublittoral region of rocky shores of Rio de Janeiro and São Paulo, Brazil. Trop Ecol 42(2): 231-241., Tano et al. 2016TANO S, EGGERTSEN M, WIKSTRÖM SA, BERKSTRÖM C, BURIYO AS & HALLING C. 2016. Tropical seaweed beds are important habitats for mobile invertebrate epifauna. Estuar Coast Shelf Sci 183(Part A): 1-12.). Besides, the presence of a variety of organisms there may serve as indicators of environmental conditions (Murray et al. 2006MURRAY SN, AMBROSE RF & DETHIER MN. 2006. Monitoring rocky shores. 1st ed., University of California Press, California, 240 p., Pinedo et al. 2007PINEDO S, GARCÍA M, SATTA MP, TORRES M & BALLESTEROS E. 2007. Rocky-shore communities as indicators of water quality: A case study in the Northwestern Mediterranean. Mar Pollut Bull 55(1-6): 126-135., Borja et al. 2012BORJA A, ELLIOTT M, HENRIKSEN P & MARBÀ N. 2012. Transitional and coastal waters ecological status assessment: advances and challenges resulting from implementing the European Water Framework Directive. Hydrobiologia 704(1): 213-229.). For instance, Ulvophyceae may present higher coverage or be favored in anthropogenic disturbed sites (Faveri et al. 2010FAVERI C, FARIAS JN, SCHERNER F, OLIVEIRA EC & HORTA PA. 2010. Temporal changes in the seaweed flora in Southern Brazil and its potential causes. Panam J Aquat Sci 5(2): 350-357., Teichberg TEICHBERG M ET AL. 2010 Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Global Change Biol 16(9): 2624-2637.et al. 2010, Scherner et al. 2013), while the coverage of Phaeophyceae is reduced or locally absent under these conditions (Oliveira & Qi 2003OLIVEIRA EC & QI Y. 2003. Decadal changes in a polluted bay as seen from its seaweed flora: the case of Santos Bay in Brazil. Ambio 32(6): 403-405., Menconi et al. 2012, Széchy et al. 2017SZÉCHY MTM, KOUTSOUKOS VS & BARBOZA CAM. 2017. Long-term decline of brown algal assemblages from southern Brazil under the influence of a nuclear power plant. Ecol Indic 80: 258-267.). Zonation patterns and natural fluctuations are also broadly investigated concepts at different rocky shores worldwide (Masi et al. 2009MASI BP, MACEDO IM & ZALMON IR. 2009. Benthic community zonation in a breakwater on the north coast of the state of Rio de Janeiro, Brazil. Braz Arch Biol Technol 52(3): 637-646., Goméz & Huovinen 2011, Stevčić et al. 2017STEVČIĆ Č, PÉREZ-MIGUEL M, DRAKE P, TOVAR-SÁNCHEZ A & CUESTA JA. 2017. Macroinvertebrate communities on rocky shores: Impact due to human visitors. Estuar Coast Shelf Sci 211: 127-136., Vinagre et al. 2017VINAGRE PA, VERÍSSIMO H, PAIS-COSTA AJ, HAWKINS SJ, BORJA A, MARQUES JC & NETO JM. 2017. Do structural and functional attributes show concordant responses to disturbance? Evidence from rocky shore macroinvertebrate communities. Ecol Indic 75: 57-72., Little et al. LITTLE C, TROWBRIDGE CD, PILLING GM, COTTRELL DM, PLOWMAN CQ, STIRLING P, MORRITT D & WILLIAMS GA. 2018. Long-term fluctuations in epibiotic bryozoan and hydroid abundances in an Irish sea lough. Estuar. Coast Shelf Sci 210: 142-152.2018).

The coast of Brazil’s Rio de Janeiro state is on the eastern coast of South America and is at the edge of two marine provinces: the Tropical Southwestern Atlantic and the Warm Temperate Southwestern Atlantic (Spalding et al. 2007). The region of Arraial do Cabo within this state is often treated as part of the border between these provinces, and because of this, Prainha Beach (within this region) can be considered an ecotone area. This area is seasonally under the influence of upwelling by the South Atlantic Central Water (SACW), which constitutes a discontinuous biogeographic barrier for marine fauna and flora in the Southwestern Atlantic and is thus recorded as the northern or southern limit of many species’ distributions (Yoneshigue 1985YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., Guimaraens & Coutinho 1996GUIMARAENS MA & COUTINHO R. 1996. Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil. Aquat Bot 52: 283-299., Floeter & Soares-Gomes 1999FLOETER SR & SOARES-GOMES A. 1999. Biogeographic and species richness patterns of Gastropoda on the Southwestern Atlantic. Rev Brasil Biol 59(4): 567-575.). The fisherman population of Arraial do Cabo demanded the establishment of a marine reserve to protect the integrity of the marine biodiversity in this area, which is a locally important economic resource (Mendonça et al. 2013MENDONÇA TCM, MORAES EA & COSTA MAM. 2013. Turismo e pesca nas Reservas Extrativistas Marinhas de Arraial do Cabo (RJ) e da Prainha do Canto Verde (CE): possibilidades e limites de complementaridade. Rio de Janeiro. CVT 13(3): 372-390.). Thus, the Reserva Extrativista Marinha do Arraial do Cabo (RESEX) was established in 1997 to assure the sustainable utilization of marine resources by the traditional fishermen populations and the recreational and other activities under management norms (Silva 2004SILVA PP. 2004. From common property to co-management: lessons from Brazil’s first maritime extractive reserve. Mar Policy 28(5): 419-428., ICMBIO 2017). These particular conditions support the high biodiversity of species with tropical and temperate affinities in the region, leading to the establishment of several lists and spatiotemporal comparisons of macroalgae in this area, particularly those of Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., Guimaraens & Coutinho (1996)GUIMARAENS MA & COUTINHO R. 1996. Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil. Aquat Bot 52: 283-299., and Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66..

Several methodologies have been used to track the diversity of the marine organisms (Gomèz & Huovinen 2011GOMÈZ I & HUOVINEN P. 2011. Morpho-functional patterns and zonation of South Chilean seaweeds: the importance of photosynthetic and bio-optical traits. Mar Ecol Prog Ser 422: 77-91., Trivedi et al. 2016TRIVEDI S, ALOUFI AA, ANSARI AA & GHOSH SK. 2016. Role of DNA barcoding in marine biodiversity assessment and conservation: An update. Saudi J Biol Sci 23: 161-171., Perera-Valderrama et al. 2017, Rohde et al. 2017ROHDE S, SCHUPP PJ, MARKERT A & WEHRMANN A. 2017. Only half of the truth: Managing invasive alien species by rapid assessment. Ocean Coast Manage 146: 26-35.), however, the use of photographic sampling has arisen recently as a particularly quick and non-destructive alternative method to traditional destructive sampling techniques (Solan et al. 2003, Durden et al. 2016, Beisiegel et al. 2018BEISIEGEL K, DARR A, ZETTLER ML, FRIEDLAND R, GRÄWE U & GOGINA M. 2018. Understanding the spatial distribution of subtidal reef assemblages in the southern Baltic Sea using towed camera platform imagery. Estuar Coast Shelf Sci 207: 82-92.). This method, allied to a new generation of software, facilitates statistical analyses and reporting of the occurrence of species in several habitats (Tanner et al. 2015TANNER JE, MELLIN C, PARROTT L & BRADSHAW CJA. 2015. Fine-scale benthic biodiversity patterns inferred from image processing. Ecol Complex 22: 76-85., Arefin 2016AREFIN AME. 2016. Proposal of a marine protected area surveillance system against illegal vessels using image sensing and image processing. Acta Ecol Sin 38(2): 111-116., Gomes-Pereira et al. 2016, Romero-Ramirez et al. 2016ROMERO-RAMIREZ A, GRÉMARE A, BERNARD G, PASCAL L, MAIRE O & DUCHÊNE JC. 2016. Development and validation of a video analysis software for marine benthic applications. J Marine Syst 162: 4-17.).

Combining evidence from the RESEX implemented in Arraial do Cabo, including its oligotrophic status (Guimaraens & Coutinho 2000GUIMARAENS MA & COUTINHO R. 2000. Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat Bot 66(2): 101-114., Jara et al. 2006JARA VC, MIYAMOTO JHS, GAMA BAP, MOLIS M, WAHL M & PEREIRA R. 2006. Limited evidence of interactive disturbance and nutrient effects on the diversity of microbenthic assemblages. Mar Ecol Prog Ser 308: 37-48., Coelho-Souza et al. 2017COELHO-SOUZA SA, PEREIRA GC, LOPEZ MS, GUIMARÃES JRD & COUTINHO R. 2017. Seasonal sources of carbon to the Brazilian upwelling system. Estuar Coast Shelf Sci 194: 162-171.) and the concept of natural fluctuations induced by environmental and biological factors (Hoek 1982HOEK C VAN DEN. 1982. The distribution of benthic marine algae in relation to the temperature regulation of their life histories. Biol J Linnean Soc 18(2): 81-144., Ives & Carpenter 2007IVES AR & CARPENTER SR. 2007. Stability and diversity of ecosystems. Science 317(5834): 58-62., Nascimento et al. 2014NASCIMENTO A, COELHO - GOMES C, BARBARINO E & LOURENÇO SO. 2014. Temporal variations of the chemical composition of three seaweeds in two tropical coastal environments. Open J Mar Sci 4(2): 118-139.), we hypothesized that the species of marine flora at Prainha has changed over the years by its ecological equivalent (i.e. species with similar ecological function) and, consequently, there has been a large turnover of the species in this area. Thus, the aims of the present study were to (I.) analyze the diversity of an intertidal community of a rocky shore at Prainha and the turnover of its macroalgae assemblage throughout all four seasons, (II.) assess the change in the macroalgal composition of this community over an interval of almost 30 years, and (III.) evaluate the efficiency of different combinations of destructive and photographic approaches to characterize the species coverage and diversity of this rocky shore benthic community.

MATERIALS AND METHODS

Sampling was performed seasonally between 2011 and 2012 at Prainha Beach, Arraial do Cabo city, Rio de Janeiro state, Brazil (22°57’22.1”S, 42°01’36.5”W). It was an integrative approach of a non-destructive method with a minor destructive method and always performed at low tide on the left side of the rocky shore located outside the beach. The area sampled was approximately 10 m in length, which was horizontally delimitated with a line transect above the intertidal region and divided into three vertical zones (upper, middle, and lower) based on the typically predominant organisms found in each zone. At each vertical zone, five 900 cm² quadrats were randomly placed for photographic sampling. IIn addition, we manually collected macroalgae specimens from the transect area and those living around the rocky shore (outside the transect area) within a 40 min period to assist identification of local biodiversity, none marine invertebrates were collected. These collections were done to obtain estimates of the species richness and turnover while also sustaining the photoquadratic identifications. Specimens were collected, separated according to their intertidal zone, and preserved in a solution of 4 % formalin diluted in seawater for later identification.

At the laboratory, macroalgal taxa were identified to the lowest level possible with Olympus CX40 optical microscopy and Olympus SZ51 stereoscopic microscope, following Taylor (1972)TAYLOR WR. 1972. Marine algae of the eastern tropical and subtropical coasts of the Americas. 3rd ed., Michigan: The University of Michigan Press, 870 p., Littler & Littler (2000)LITTLER DS & LITTLER MM. 2000. Caribbean reef plants: An identification guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico, Offshore Graphics, 542 p. and Dawes & Mathieson (2008)DAWES CJ & MATHIESON A. 2008. The seaweeds of Florida, 1st ed., University Press of Florida, 591 p.. Nomenclatural updates followed Flora 2020 (http://floradobrasil.jbrj.gov.br) and AlgaeBase (Guiry & Guiry 2019GUIRY MD & GUIRY GM. 2019. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available at http://www.algaebase.org; Acessed on 16 October 2018.
http://www.algaebase.org;...
). The resulting list of macroalgae was compared to the data provided by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. (Table I) to the same locality. Species that were considered as new occurrences for the area were deposited in the Herbarium Jorge Pedro Pereira Carauta (HUNI). The turnovers between seasons in the present study and between the species list from the current study and that proposed by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., were calculated based on the concept of extinction (absence of species) and immigration (appearance of species) of all species along the shore throughout time as suggested in Brown & Kodrick-Brown (1977)BROWN JH & KODRICK-BROWN A. 1977. Turnover rates in insular biogeography: Effect of immigration on extinction. Ecology 58(2): 445-449. and Magurran (2006)MAGURRAN AE. 2006. Medindo a diversidade biológica. 1a ed., Editora UFPR, Curitiba, 262 p..

Table I
Comparison of intertidal species list from Prainha by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and the current study. Species that were listed only in the present study are highlighted with bold, species registered within Prainha by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and by the present study are also marked with “*” and species listed only by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. are not in bold. The species recognized by CPCe received the classification codes as follow: “ACO” – Articulated Corallinales; “CEG” – Centroceras gasparrinii ; “FRH” – Filamentous Rhodophyta; “GEL” – Gelidiales; “GYM” – Gymnogongrus griffthsiae ; “HIL” – Hildenbrandia rubra ; “HYP” – Hypnea spp.; “LAU” – Laurencia spp.; “TRH” – Turfs of Rhodophyta; “CAN” – Canistrocarpus cervicornis ; “COL” – Colpomenia sinuosa ; “FOC” – Filamentous Ochrophyta; “CHA” – Chaetomorpha antennina ; “ENT”- Tubular Ulva; “ULV” – Foliose Ulva; “FCH” – Filamentous Chlorophyta; “TCH” – Turfs of Chlorophyta; “COE” – Erect Codium; “COC” – Crustose Codium”; “AMA” – Amphibalanus amphitrite ; “CHT” – Chthamalus bisinuatus ; “FIS” – Fissurella clenchi ; “ISO” – Isognomon bicolor ; “LOT – Lottia subrugosa ; “MYT” – Mytilaster solisianus ; “OST” – Ostreidae; “PER” – Perna perna ; “PHR” – Phragmatopoma caudata ; “STA” – Stramonita haemastoma ; “-” Not Identified in the Photography; “ND” No data, i.e., not found during this study.

The coverage of the community by each taxon was analyzed using Coral Point Count with Excel extensions (CPCe) (Kohler & Gill 2006KOHLER KE & GILL SM. 2006. Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32: 1259-1269.) via an adapted database containing the names of the organisms in the studied region. When possible, identification of organisms from the photoquadrats was performed to the species level. However, it was not possible to identify small organisms to the species level using photographic analysis, in which case they were identified to the morphological or order level. In the coverage analysis, all taxa identified were treated as Community Components (CCs) based on their taxonomic or morphological level. Thirty points were randomly placed on each photograph for coverage analysis. The number of points needed to adequately represent the coverage of the community was established according to Silva et al. (2015)SILVA RP, DE PAULA JC & ARAUJO JM. 2015. Estudo metodológico para análise de cobertura do costão rochoso da Prainha, Arraial do Cabo, Rio de Janeiro. Revista Cecil 7: 28-30.. Afterwards, Shannon-Wiener (H’) and Evenness (J) diversity indices were calculated based on the coverage of each and all species (Magurran 2006MAGURRAN AE. 2006. Medindo a diversidade biológica. 1a ed., Editora UFPR, Curitiba, 262 p.).

RESULTS

Coverage analysis

The upper zone of the rocky shore was dominated by invertebrates, which made up more than half of the CCs in all seasons, and the invertebrate cover was higher during winter, summer, and autumn, whereas algae had a higher coverage than invertebrates in the spring (Figure 1). For instance, Tetraclita stalactifera Lamarck 1818 (TET) was the most abundant species during the winter, spring, and summer and Mytilaster solisianus d’Orbigny 1842 (MYT) in autumn, winter and summer. In autumn, however, the crustose non-coralline rhodophyte Hildenbrandia rubra (Sommerfelt) Meneghini (HIL) was the most abundant species. Community components with less percentage coverages were identified during the year and included taxa such as TET, Amphibalanus amphitrite Darwin 1854 (AMA), Perna perna Linnaeus 1758 (PER), Chthamalus bisinuatus Pilsbry 1916 (CHT), crustose Corallinales and laminar forms of Ulva spp. (including Ulva fasciata Delile and Ulva rigida C. Agardh). Spring was the season with the highest diversity (16 CCs), while autumn had the lowest (10 CCs) (Figure 2).

Figure 1
Sum of coverage Mean of Macroalgae and Invertebrate in each intertidal zone.
Figure 2
Percent cover of different community components (CC) in each zone. Values presented are means ± standard deviations. AMA = Amphibalanus amphitrite; CAN = Canistrocarpus cervicornis; CEG = Centroceras gasparrinii; CHA = Chaetomorpha antennina; CHT = Chthamalus bisinuatus; ACO = Articulated Corallinales; COC = Codium spongiosum; CCO = Crustose Corallinales; COL = Colpomenia sinuosa; RCR = Recruit Cirripedia; ENT = Tubular Ulva spp.; FCH = Filamentous Chlorophyta; FIS = Fissurella clenchi; FRH = Filamentous Rhodophyta; GEL = Gelidiales; GYM = Gymnogongrus griffithsiae; HIL = Hildenbrandia rubra; HYP = Hypnea spp.; ISO = Isognomon bicolor; LAU = Laurencia spp.; LOT = Lottia subrugosa; MYT = Mytilaster solisianus; OST = Cassostrea rhizophorae; PAD = Padina spp.; PER = Perna perna; PHR = Phragmatopoma caudata; RAL = Neoralfsia expansa; STA = Stramonita haemastoma; STD = Stramonita haemastoma spawning; TCH = Turfs of Chlorophyta; TET = Tetraclita stalactifera; TRH = Turfs of Rhodophyta; ULV = Laminar Ulva spp.

In the middle and lower zones, macroalgae were the dominant organisms on the substrate throughout the year (Figure 1). The most important CC with the highest coverage was the group of articulated Corallinales (ACO), however, other algae were also found in both zones, e.g., laminar forms of Ulva spp., crustose Corallinales (CCO), Padina spp. (PAD), Colpomenia sinuosa (Mertens ex Roth) Derbès & Solier (COL), and Hypnea spp. (HYP). Some invertebrates that were characteristic of the upper zone, such as TET, AMA and PER were also observed in the middle zone during the summer (Figure 2).

In comparison to other seasons and zones, the coverage of the middle zone during the summer presented the highest total number of CCs, making it the most diverse assemblage in terms of coverage found throughout the year (Figure 2). During winter and spring, the middle zone was dominated by articulated Corallinales (ACO, 36-54 % coverage), while invertebrates were absent. Afterwards, in summer and autumn, the dominance of articulated Corallinales was replaced by Chaetomorpha antennina (Bory) Kützing (CHA, 18.5 %) and HIL (25.7 %), and the invertebrates returned and made up for more than half of the CCs registered.

In the lower zone, macroalgae accounted for more than 87 % of the coverage (Figure 1). The ACO were the prevailing CC for the whole year. The principal component of this algal group was Jania crassa J. V. Lamouroux, but it also included Amphiroa beauvoisii J. V. Lamouroux to a lesser extent. The number of registered CCs in the lower zone went from eight during the winter up to 14 in autumn, with invertebrates accounting for two CCs or less during the entire period sampled (Figure 2).

Macroalgal assemblage richness, diversity, and turnover

The Shannon diversity index values obtained demonstrated that the richness and homogeneity of the species present decreased between summer and autumn in the upper zone (Figure 3). Between spring and summer, the richness in the middle zone increased considerably, although there was no concurrent change in the equitability (Figure 3). This change in the number of species was concomitant with the highest turnover rate for the whole year (Figure 4d). In the transition between spring and summer, six species were not observed, and eight new occurrences appeared in the macroalgal assemblage. This variation was greater than the annual turnover in the region, and thus this was the period out of the year with the largest replacement of organisms (Figure 4d).

Figure 3
Diversity indices calculated for the upper, middle, and lower zones of the rocky shore at Prainha.
Figure 4
Turnover of taxa found on the rocky shore at Prainha. Turnover is shown for Chlorophyta, Rhodophyta, Ochrophyta, all taxa of macroalgae, and is compared between Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and the present study.

In the lower zone, the richness and equitability exhibited little variation, which was reflected in the fact that the diversity of this zone was similar in all seasons of the year (Figure 3). Regarding the turnover rate between winter and spring, eight new species were recorded, while seven were not observed on the rocky shore after this period (Figure 4d).

In terms of the turnover of phyla, the turnover rate of Chlorophyta ranged from 0.27 to 0.42, with the largest change occurring between spring and summer (Figure 4a). Rhodophyta exhibited high turnover rates (> 0.50) for all seasons, indicating constant and major shifts in the composition of red macroalgal assemblages (Figure 4b). Comparing the present study and the former (Yoneshigue 1985YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461.) community compositions were compared, green algae were also found to have a lower turnover rate than Rhodophyta (Figure 4e). However, Ochrophyta was a phylum that underwent lower annual variations than others (Figure 4c), nevertheless, it experienced a higher turnover during the transitions from spring to summer and winter to spring. Comparing to Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. dataset, Ochrophyta also showed the lowest turnover rate, with low exclusion and immigration rates compared to those of other phyla (Figure 4c).

Macroalgal comparison

Yoneshigue (1985) registered 85 species as occurring at Prainha Beach, of which 20 were species of Chlorophyta, 12 were Ochrophyta, and 53 were Rhodophyta. In addition, the review of Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66. registered 207 taxa for Arraial do Cabo, of which Prainha had 98 species and was the second most diverse location in the region after Ponta da Cabeça (108 species). The present study found 96 taxa at Prainha, of which 23 belonged to the phylum Chlorophyta, 19 to Ochrophyta, and 54 to Rhodophyta, with the last phylum remaining the most well-represented at Prainha.

Rhodomelaceae and Ceramiaceae (Rhodophyta), were the families with the higher diversity at Prainha, with 12 species (22 % of the total) and eight species (15 %), respectively. The most well-represented families of Chlorophyta at the study site were Cladophoraceae and Ulvaceae, with seven and six species present, respectively. Comprising together 57 % of the total abundance of the phyla observed. Among Ochrophyta, two families comprised most of the composition: Dictyotaceae, which increased its representation from 15 to 21 % of the total (four species) over time; and Scytosiphonaceae, which increased its representation (two species) in the community in comparison to that in the early 1980s.

Altogether, compared to past surveys (Yoneshigue 1985YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., Brasileiro et al. 2009) 55 new occurrences were added for Prainha Beach and 27 for Arraial do Cabo. Considering these new occurrences, Prainha reached a total of 125 taxa, which would make it the most diverse area in Arraial do Cabo. These new records also increased the number of taxa present in Arraial do Cabo, enhancing it from 207 to 234 species.

DISCUSSION

Autumn and winter in this region are periods that are marked by the frequent occurrence of cold fronts and storms. As a result, the water column is mixed in these seasons, increasing the amount of organic and inorganic particles it contains (Coelho-Souza et al. 2017COELHO-SOUZA SA, PEREIRA GC, LOPEZ MS, GUIMARÃES JRD & COUTINHO R. 2017. Seasonal sources of carbon to the Brazilian upwelling system. Estuar Coast Shelf Sci 194: 162-171.) and causing the senescence of a large part of the coastal flora (Riggs et al. 1998RIGGS SR, AMBROSE WG, COOK JW, SNYDER SW & SNYDER SW. 1998. Sediment production on sediment-starved continental margins; the interrelationship between hardbottoms, sedimentological and benthic community processes, and storm dynamics. J Sediment Res 68(1): 155-168.). In addition to these physical disturbances, the prevalence of south-southwest quadrant winds favors the proximity and residence of the Brazilian Current along the coast and prevents upwelling of the SACW. The proximity of the Brazilian Current could lead to inorganic nutrient stress and/or limitation, especially for organisms in the upper zone of the coast, resulting in the deceased abundance of several components of the community and increasing the turnover rates, as was observed during the present study. Under nutrient limitation, resistant macroalgae with shorter canopies are selected (Steneck & Dethier 1994STENECK RS & DETHIER MN. 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69(3): 476-498.). The same seasonal effects on the benthic community were observed at Ubatuba (state of São Paulo, Brazil), another upwelling region that is influenced by the SACW (Alves et al. 2014ALVES BGR, GÜTH AZ, BÍCEGO MC, GAETA SA & SUMIDA PYG. 2014. Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Cont Shelf Res 85: 106-116.). On the other hand, during spring and summer, upwelling events increase in frequency and intensity at Arraial do Cabo. The water column stratifies more frequently and becomes enriched with inorganic nutrients, such as nitrate and phosphate (Coelho-Souza et al. 2012COELHO-SOUZA SA, LOPÉZ MS, GUIMARÃES JRD, COUTINHO R & CANDELLA RN. 2012. Biophysical interactions in the Cabo Frio upwelling system, Southeastern Brazil. Braz J Oceanogr 60(3): 353-365., 2017). The increased input of such inorganic nutrients could explain the rising number of macroalgal species in the middle and lower zones of the coast that we observed, as well their turnover rates during the beginnings of these periods.

The interactions between macroalgae and invertebrates over the three zones of the intertidal community of Prainha observed in the present study were similar to those described by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., as well as to those in other upwelling regions of the world (Hosegood et al. 2017HOSEGOOD PJ, NIGHTINGALE PD, REES AP, WIDDICOMBE CE, WOODWARD EMS, CLARK DR & TORRES RJ. 2017. Nutrient pumping by submesoscale circulations in the mauritanian upwelling system. Prog Oceanogr 159: 223-236., Jiang & Wang 2018JIANG R & WANG Y. 2018. Modeling the ecosystem response to summer coastal upwelling in the northern South China Sea. Oceanologia 60(1): 32-51., Walter et al. 2018WALTER RK, ARMENTA KJ, SHEARER B, ROBBINS I & STEINBECK J. 2018. Coastal upwelling seasonality and variability of temperature and chlorophyll in a small coastal embayment. Cont Shelf Res 154: 9-18.). However, some exceptions were observed, such as the differences in the species dominating the upper zone throughout all seasons, wherein Chthamalus bisinuatus Pilsbry, 1916 dominated community coverage in the early 1980s (Yoneshigue 1985YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461.), while Tetraclita stalactifera and Hildenbrandia rubra dominated in the present study. The results for the middle and lower zones agreed between this and past studies in relation to species dominance, with one exception during autumn; specifically, Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. recorded a large settlement of crustose Corallinales algae in the lower zone in the autumn, whereas our study observed that the complex thalli of articulated Corallinales dominated this season.

Previous studies emphasized the influence of upwelling on the megafaunistic composition of marine communities at other sites around the world (e.g., Lavaleye et al. 2002LAVALEYE MSS, DUINEVELD GCA, BERGHUIS EM, KOK A & WITBAARD R. 2002. A comparison between the megafauna communities on the N.W. Iberian and Celtic continental margins-effects of coastal upwelling? Prog Oceanogr 52(2-4): 459-476., Kelaher & Castilla 2005KELAHER BP & CASTILLA JC. 2005. Habitat characteristics influence macrofaunal communities in coralline turf more than mesoscale coastal upwelling on the coast of Northern Chile. Estuar Coast Shelf Sci 63(1-2): 155-165., Carlier et al. 2015). At Cabo Frio, Brazil, in particular, most species have subtropical affinities and food resources are available in larger amounts for the entire food chain (Léo & Pires-Vanin 2006LÉO FC & PIRES-VANIN AMS. 2006. Benthic megafauna communities under the influence of the South Atlantic Central Water intrusion onto the Brazilian SE shelf: A comparison between an upwelling and a non-upwelling ecosystem. J Marine Syst 60(3-4): 268-284., Braga et al. 2018BRAGA HO, AZEITEIRO UM, OLIVEIRA HMF & PARDAL MA. 2018. Conserving Brazilian Sardine: Fisher’s attitudes and knowledge in the Marine Extractive Reserve of Arraial do Cabo, Rio de Janeiro State, Brazil. Fish Res 204: 402-411.). Furthermore, in addition to the afore mentioned physicochemical and/or biological disturbances, invertebrates compete with macroalgae for available space, which is a potentially limiting resource in coastal habitats. This competition thus exerts an influence on the community and likely alters its species richness and diversity (Dayton 1971DAYTON PK. 1971. Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41(4): 351-389., Tlig-Zouari et al. 2010TLIG-ZOUARI S, RABAOUI L, FGUIRI H, DIAWARA M & HASSINE OKB. 2010. Spatial diversity of rocky midlittoral macro-invertebrates associated with the endangered species Patella ferruginea (Mollusca: Gastropoda) of Tunisian coastline. Estuar Coast Shelf Sci 87(2): 275-283.).

Changes in the macroalgal composition and relative occurrence of different algal families were observed at Prainha before and after an interval of almost 30 years. According to Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66., among Chlorophyta families, Cladophoraceae and Codiaceae were the most diverse families, representing half of the green macroalgae found on the rocky shore. In the present study, Cladophoraceae and Ulvaceae were the most well-represented families. Bryopsis corymbosa J. Agardh and Valonia macrophysa Kützing, whose abundance characterized Prainha to Yonesigue (1985), were not recorded in the present study, which might indicate that significant alterations in the community have occurred. Furthermore, B. corymbosa was replaced by different species of the same genus at this site (B. pennata J. V. Lamouroux, B. plumosa (Hudson) C. Agardh, and B. ramulosa Montagne), increasing the representation of Bryopsidaceae; this change was considered a substitution of one species by its ecological equivalent(s). Nevertheless, other previously reported species were not recorded during the present study, such as Derbesia marina (Lyngbye) Solier, Derbesia tenuinissima (Moris & De Notaris) P. Crouan & H. Crouan and Ulvella lens P. Crouan & H. Crouan. When comparing the previous studies’ lists of macroalgae, 12 species of Chlorophyta were added for Prainha, and six new occurrences were recorded for the larger region of Arraial do Cabo: Bryopsis ramulosa, Cladophora sericea (Hudson) Kützing, Cladophoropsis macromeres W. R. Taylor, Phyllodictyon anastomosans (Harvey) Kraft & M. J. Wynne, Ulva prolifera O. F. Müller, and Willeella brachyclados (Montagne) M. J. Wynne.

The most representative Ochrophyta flora reported by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. belonged to the families Acinetosporaceae, Dictyotaceae, and Scytosiphonaceae, with each family comprising 15 % of the Ochrophyta flora. In the present study, Acinetosporaceae, Dictyotaceae, Sargassaceae, and Scytosiphonaceae were the families with the highest coverage. The latter three families form complex thalli important to microhabitat formation. Some species that form less complex thalli were recorded by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66., but were not registered in the present study. Eleven species of Ochrophyta were added to the list of Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. for Prainha: Bachelotia antillarum (Grunow) Gerloff, Canistrocarpus cervicornis (Kützing) De Paula & De Clerck, Chnoospora minima (Hering) Papenfuss, Sphacelaria novae-hollandiae Sonder, Sphacelaria tribuloides Meneghini, Ectocarpus fasciculatus Harvey, Dictyopteris delicatula J. V. Lamouroux, Feldmannia indica (Sonder) Womersley & A. Bailey, Padina antillarum (Kützing) Piccone, Rosenvingea orientalis (J. Agardh) Børgesen, and Sargassum vulgare C. Agardh. However, only the last five of these algae represented new occurrences for the region of Arraial do Cabo.

The diversity of Rhodophyta families, unlike the other macroalgal phyla, did not change in the present study, comparing to the lists of Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. and Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66.. On the other hand, one species registered by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461., Ceramium codii (H. Richards) Mazoyer, was replaced by its ecological equivalent C. vagans P. C. Silva in P. C. Silva, Meñez & Moe. The families Callithamniaceae, Lomentariaceae, Gelidiellaceae, Plocamiaceae, and Rhodymeniaceae were recorded by Yoneshigue (1985)YONESHIGUE Y. 1985. Taxonomie et ecologie des algues marines dans la région de Cabo Frio (Rio de Janeiro) Brèsil. Thesis, Université d’Aix-Marseille II, 1(1): 461. at Prainha but were not found in the present study. In relation to the review by Brasileiro et al. (2009)BRASILEIRO PS, YONESHIGUE-VALENTIN Y, BAHIA RG, REIS RP & AMADO FILHO G. 2009. Algas Marinhas Bentônicas da Região de Cabo Frio e Arredores: Síntese do Conhecimento. Rodriguésia 60(1): 39-66., the present study added 18 rhodophyte species for Arraial do Cabo region: Arthrocardia variabilis (Harvey) Weber-van Bosse, Amphiroa brasiliana Decaisne, Centroceras gasparrinii (Meneghini) Kützing, Ceramium clarionense Setchell & N. L. Gardner, Dasya ocellata (Grateloup) Harvey in Hooker, Taenioma perpusillum (J. Agardh) J. Agardh, Chondria atropurpurea Harvey, Herposiphonia delicatula Hollenberg, Herposiphonia nuda Hollenberg, Herposiphonia parca Setchell, Laurencia aldingensis Saito & Womersley, Laurencia dendroidea J. Agardh, Melanothamnus gorgoniae (Harvey) Díaz-Tapia & Maggs, Melanothamnus sphaerocarpus (Børgesen) Díaz-Tapia & Maggs, Pterocladiella caerulescens (Kützing) Santelices & Hommersand, Hypnea cervicornis (J. Agardh), Chondracanthus saundersii C. W. Schneider & C. E. Lane, and Gracilaria mammillaris (Montagne) M. A. Howe.

The changes in the macroalgal composition observed may have been related to several factors acting over the intervening years. The RESEX was created in 1997, establishing a protection area for the marine resources in the area and at the same time implementing a plan for the sustainable utilization of these resources by the local community (Silva 2004SILVA PP. 2004. From common property to co-management: lessons from Brazil’s first maritime extractive reserve. Mar Policy 28(5): 419-428.). Additionally, the Companhia Nacional de Álcalis, which was established in 1960 at Prainha, used to constantly discharge warmer water and sodium carbonate (barrilha) into the seawater. This company ceased its operations in 2006 (FEEMA 1988FEEMA. 1988. Perfil ambiental do Município de Arraial do Cabo, 1a ed., Rio de Janeiro, 43 p., Pereira 2010PEREIRA WLCM. 2010. Vagas da modernidade: a Companhia Nacional de Alcalis em Arraial do Cabo (1943-964). Estud hist (Rio J.) 23(46): 321-343.). Thus, the absence of chemical material inputs and the creation of a protection policy for this area could have influenced the increases we observed in the number of species at Prainha and, consequently, the area’s biodiversity.

The present study recorded a reduced turnover rate of brown algal species in relation to Yoneshigue’s (1985) data. This group of algae is frequently referred to as one that is particularly ecologically susceptible to anthropogenic influences (Ballesteros et al. 2007BALLESTEROS E, TORRAS X, PINEDO S, GARCÍA M, MANGIALAJO L & TORRES M. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar Pollut Bull 55(1-6): 172-180., Pinedo et al. 2007PINEDO S, GARCÍA M, SATTA MP, TORRES M & BALLESTEROS E. 2007. Rocky-shore communities as indicators of water quality: A case study in the Northwestern Mediterranean. Mar Pollut Bull 55(1-6): 126-135., Martins et al. 2012). Therefore, this suggests that the results of this study present a favorable diagnosis to the water quality at Prainha. The presence of macroalgae with structurally complex thalli (such as Canistrocarpus cervicornis, Laurencia spp., and Sargassum spp.) is also an indicator of good water quality at the site because in polluted environments, opportunistic taxa (i.e. macroalgae with simple thalli) are favored and intensely compete with invertebrates for space on the rocky shore, which decreases the local diversity (Soares-Gomes et al. 2016SOARES-GOMES A, DA GAMA BAP, NETO JAB & THOMPSON F. 2016. An environmental overview of Guanabara Bay, Rio de Janeiro. Reg Stud Mar Sci 8: 319-330.).

A non-destructive sampling approach is widely used in ecological studies, including in Brazil, due to its ability to analyze rocky shore communities efficiently and cost-effectively without negatively impacting sensitive species (Masi et al. 2016MASI BP, COUTINHO R & ZALMON IR. 2016. Analytical successional tools of fouling communities submitted to different light effects. Community Ecol 17(2): 178-187., Beisiegel et al. 2017BEISIEGEL K, DARR A, GOGINA M & ZETTLER ML. 2017. Benefits and shortcomings of non-destructive benthic imagery for monitoring hard-bottom habitats. Mar Pollut Bull 121(1-2): 5-15., Mantelatto et al. 2018MANTELATTO MC, SILVA AG, LOUZADA TS, MCFADDEN CS & CREED JC. 2018. Invasion of aquarium origin soft corals on a tropical rocky reef in the southwest Atlantic, Brazil. Mar Pollut Bull 130: 84-94.). Despite having some limitations (e.g., it can be difficult to visualize small organisms, and requires one to have previous knowledge of the occurrence of relevant species for the area to perform analyses), the photoquadrat technique is still recognized as an important tool for non-destructive environmental monitoring (Pech et al. 2004PECH D, CONDAL AR, BOURGET E & ARDISSON PL. 2004. Abundance estimation of rocky shore invertebrates at small spatial scale by high-resolution digital photography and digital image analysis. J Exp Mar Biol Ecol 299(2): 185-199., Gomes-Pereira et al. 2016, Perkins et al. 2016PERKINS NR, FOSTER SD, HILL NA & BARRETT NS. 2016. Image subsampling and point scoring approaches for largescale marine benthic monitoring programs. Estuar Coast Shelf Sci 176: 36-46.).

The utilization of the methodology discussed above may similarly provide assistance to monitoring programs aiming to prevent new (invasive) organisms from settling in an area and control the behavior of exotic species that are already established. For instance, such programs detected and continuously monitoring the Caribbean mollusk Isognomon bicolor C. B. Adams, 1845, which has been detected at Prainha since the early 1990s (Domaneschi & Martins 2002DOMANESCHI O & MARTINS CM. 2002. Isognomon bicolor (C.B. Adams) (Bivalvia, Isognomonidae): primeiro registro para o Brasil, redescrição da espécie e considerações sobre a ocorrência e distribuição de Isognomon na costa brasileira. Rev Bras Zool 19(2): 611-627.). This invasive species has been expanding its geographical distribution in the southwestern Atlantic since the 1980s, and is present from Rio Grande do Norte, Brazil to Uruguay (Domaneschi & Martins 2002DOMANESCHI O & MARTINS CM. 2002. Isognomon bicolor (C.B. Adams) (Bivalvia, Isognomonidae): primeiro registro para o Brasil, redescrição da espécie e considerações sobre a ocorrência e distribuição de Isognomon na costa brasileira. Rev Bras Zool 19(2): 611-627., Breves et al. 2014BREVES A, SCARABINO F & LEONI V. 2014. First records of the non-native bivalve Isognomon bicolor (C. B. Adams, 1845) rafting to the Uruguayan coast. Check List 10(3): 684-686.). The monitoring of exotic species in benthic communities is important due to the threat they pose to native biota, and even entire ecosystems (Amaral & Jablonski 2005AMARAL ACZ & JABLONSKI S. 2005. Conservation of marine and coastal biodiversity in Brazil. Conserv Biol 19(3): 625-631.).

In conclusion, our analyses of the species coverage, richness, and diversity of a rocky shore community demonstrated that seasonal upwelling-downwelling events may lead to species turnover and changes in diversity between seasons (Weir & Schluter 2007WEIR JT & SCHLUTER D. 2007. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315(5818): 1574-1576.). The studied rocky shore community at Prainha is therefore susceptible to alterations during upwelling periods, but the replacement of any lost species was basically driven by their ecological equivalents (i.e. species from the same families or genera), which we consider to be relatively natural and expected intra-annual changes. The comparison of the currently registered flora to those registered almost 30 years ago demonstrated (I.) new occurrences; (II.) high turnover, especially among red algae; and low turnover among brown algae. These temporal differences were smaller than our hypothesis had expected, which indicates good water quality at the site, perhaps related to the changes in coastal waste disposal between the previous and present studies. The present study used approaches that combined reduced sampling impacts (only carried out to obtain some specimens for identification) and photoquadrats, which allowed us to make a detailed description of the intertidal composition and structural characteristics of different zones on the rocky shore with minimal impact, and is recommended as a good methodology for the study of protected marine areas. The information obtained and techniques developed could assist in the management of the RESEX of Arraial do Cabo , for example to improve the supervision and protection of the benthic community that occupies the rocky shore of Prainha.

ACKNOWLEGMENTS

We thank the Universidade Federal do Estado do Rio de Janeiro (UNIRIO) for research support, and for the Scientific Initiation scholarship to RPS. JCDP thanks Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, Jovem Cientista do Nosso Estado Fellowship E-26/203.240/2017) for financial support. EAPLF thanks CNPq for financial support. EAPLF thanks CNPq Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Doctoral fellowship, and ACSC also thanks CNPq for the Scientific Initiation fellowship. This study is dedicated to Museu Nacional, an important scientific, cultural and historical institution which was severely burned in September 2nd 2018.

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Publication Dates

  • Publication in this collection
    05 June 2020
  • Date of issue
    2020

History

  • Received
    10 Oct 2018
  • Accepted
    22 Apr 2019
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