Skip to main content

Advertisement

SpringerLink
Log in

Conservation status of the southernmost reef of the Amazon Reef System: the Parcel de Manuel Luís

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The Parcel de Manuel Luís (PML) is located at the southern end of the Amazon Reef System, which comprises the northernmost reef formations of the Brazilian biogeographical province. Its unique position and singular seascape make the PML an important stepping-stone for marine organisms between the Brazilian and Caribbean provinces. Yet, due to its distance from the shore, high tidal amplitude, and strong currents associated with a series of pinnacles exposed during low spring tides, the PML is one of the least studied reefs in the Western South Atlantic. Here, we integrated sessile benthic community data, fish assemblage surveys, and remote filming of fish interactions to establish the most complete community assessment of the PML reefs to date. In our surveys, we documented 78 sessile benthic taxa, with a taxonomic dominance of macroalgae (54 taxa), including two new occurrences of sponges for the North Brazilian Shelf, as well as four endemic species, such as the fire coral Millepora laboreli. The fish assemblage comprised 59 reef fish species, with biomass dominated mainly by large carnivorous species (e.g., groupers and snappers). Intra- and interspecific interactions were dominated by herbivorous fishes, particularly underpinned by grazing behavior and chasing by territorial species. The considerably high biomass and large-bodied species found in our surveys is rarely seen elsewhere in the Western South Atlantic, suggesting a low level of fishing compared to most other places, and only a few changes were observed in the fish assemblages since the first assessment made in 1998. We also highlight the usefulness of an integrated approach for continued assessment of Western South Atlantic reefs, particularly given emerging threats from mining and oil exploration, and the heavy traffic of commercial vessels in the region. Our findings support the PML as an area of critical conservation interest for reef systems, emphasizing the need for continued enforcement of this marine protected area and its integration in long-term plans of offshore oil and gas development projects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aued AW, Smith F, Quimbayo JP, Candido DV, Longo GO, Ferreira CEL, Witman JD, Floeter SR, Segal B (2018) Large-scale patterns of benthic marine communities in the Brazilian Province. PLoS ONE 13(6):e0198452

    PubMed  PubMed Central  Google Scholar 

  • Amaral FMD, Hudson MM, Steiner AQ (2006) Note on the widespread bleaching observed at the Manuel Luiz State Park. Maranhão, Brazil Arq Ciên Mar, pp 138–141

    Google Scholar 

  • Amaral FMD, Hudson MM, Steiner AQ, Ramos CAC (2007) Corals and calcified hydroids of the Manuel Luiz Marine State Park (State of Maranhão, Northeast Brazil). Biota Neotrop 7(3):73–81

    Google Scholar 

  • Amado-Filho GM, Moura RL, Bastos AC, Salgado LT, Sumida PY, Guth AZ, Francini-Filho RB, Pereira-Filho GH, Abrantes DP, Brasileiro PS, Bahia RG, Leal RN, Kaufman L, Kleypas JA, Farina M, Thompson FL (2012) Rhodolith beds are major CaCO3 bio-factories in the tropical South West Atlantic. PLoS ONE 7(4):e35171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymounth

    Google Scholar 

  • ANTAQ (2019) National Waterway Transportation Agency. https://web.antaq.gov.br/Anuario/ (accessed 01 July 2019).

  • Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fish 28:189–214

    Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429(6994):827

    CAS  PubMed  Google Scholar 

  • Bellwood DR, Pratchett MS, Morrison TH, Gurney GG, Hughes TP, Álvarez-Romero JG, Day JC, Grantham R, Grech A, Hoey AS, Jones GP, Pandolfi JM, Tebbett SB, Techera E, Weeks R, Cumming GS (2019) Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biol Conserv 236:604–615

    Google Scholar 

  • Bender MG, Machado GR, Silva PJDA, Floeter SR, Monteiro-Netto C, Luiz OJ, Ferreira CEL (2014) Local ecological knowledge and scientific data reveal overexploitation by multigear artisanal fisheries in the Southwestern Atlantic. PLoS ONE 9(10):e110332

    PubMed  PubMed Central  Google Scholar 

  • Bertoncini AA, Aguilar-Perera, Barreiros J, Craig MT, Ferreira B, Koenig C (2018) Epinephelus itajara (errata version published in 2019). The IUCN Red List of Threatened Species 2018: e.T195409A145206345. Downloaded on 28 June 2019

  • Bruno JF, Sweatman H, Precht WF, Selig ER, Shutte VGW (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90(6):1478–1484

    PubMed  Google Scholar 

  • Bruno JF, Côté IM, Toth LT (2019) Climate change, coral loss, and the curious case of the parrotfish paradigm: why don’t marine protected areas improve reef resilience? Annu Rev Mar Sci 11:307–334

    Google Scholar 

  • Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk - revisited. World Resources Institute, Washington, 130pp

    Google Scholar 

  • Byers CR, Steinhorst RK, Krausman PR (1984) Clarification of the technique for analysis of utilization-availability data. J Wildlife Manage 48(3):1050–1053

    Google Scholar 

  • Capel KCC, Creed J, Kitahara MV, Chen CA, Zilberberg C (2019) Multiple introductions and secondary dispersion of Tubastraea spp. in the Southwestern Atlantic. Sci Rep 9:13978

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69(2):357–371

    Google Scholar 

  • Chaves LCT, Nunes JACC, Sampaio CLS (2010) Shallow reef fish communities of south Bahia coast, Brazil. Braz J Oceanogr 58:33–46

    Google Scholar 

  • Collette BB, Rützler K (1977) Reef fishes over sponge bottoms off the mouth of the Amazon River. Proceedings of the Third International Coral Reef Symposium: 305–310

  • Colleti G, Basso D, Frixa A (2017). Economic Importance of Coralline Carbonates. https://doi.org/10.1007/978-3-319-29315-8_4

    Article  Google Scholar 

  • Costa OS Jr, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. J S Am Earth Sci 25(2):257–270

    Google Scholar 

  • Coura MF (2016) Contribuição ao plano de manejo do Parque Estadual Marinho do Parcel de Manuel Luís/MA: atualização e avanços da unidade após 25 anos. Dissertation. Fundación Universitaria Iberoamericana, Brasília, Brazil. 73pp.

  • D’Agata S, Mouillot D, Wantiez L, Friedlander AM, Kulbicki M, Vigliola L (2016) Marine reserves lag behind wilderness in the conservation of key functional roles. Nat Commun 7:12000

    PubMed  PubMed Central  Google Scholar 

  • de Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middleburg JJ, de Goiej AFPM, Admiraal W (2014) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342(6154):108–110

    Google Scholar 

  • de Goeij JM, Lesser MP, Pawlik JR (2017) Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In Climate Change, Ocean Acidification and Sponges. Springer, Cham, pp 373–410. https://doi.org/10.1007/978-3-319-59008-0_8

  • DOE – Diário Oficial do Estado do Ceará (1997) Law Nº 12.717 of 5th of September 1997 on the creation of the Parque Estadual Marinho da Pedra da Risca do Meio.

  • Donovan MK, Friedlander AL, Lecky J, Jouffray J-B, Williams GJ, Wedding LM, Crowder LB, Erickson AL, Graham NAJ, Gove JM, Kappel CV, Karr KK, Kittinger JN, Norström AC, Nyström M, Oleson KLL, Stamoulis KA, White C, Williams ID, Selkoe KA (2018) Combining fish and benthic communities into multiple regimes reveals complex reef dynamics. Sci Rep 8:16943

    PubMed  PubMed Central  Google Scholar 

  • Duncombe J (2019) Brazil’s oil spill is a mystery, so scientists try oil forensics. Eos 100:2019. https://doi.org/10.1029/2019EO136177 (Published on 24 October)

    Article  Google Scholar 

  • Dutra LXC, Kikuchi RKP, Leão ZMAN (2006) Effects of sediment accumulation on reef corals from Abrolhos, Bahia, Brazil. J Coast Res 39:633–638

    Google Scholar 

  • Dutra GF, Allen GR, Werner T, McKenna SA (eds) (2005) A Rapid Marine Biodiversity Assessment of the Abrolhos Bank, Bahia. Brazil. RAP Bulletin of Biological Assessment, Conservation International, Washington, DC, USA

    Google Scholar 

  • Earle S (2016) Protect the Ocean, Protect Ourselves. In: Johnson M, Bayley A (eds) Coastal Change. Springer International Publishing Switzerland, Ocean Conservation and Resilient Communities, p 168

    Google Scholar 

  • Feitosa LM, Martins AP, Giarrizzo T, Macedo W, Monteiro IL, Gemaque R, Nunes JLS, Schneider H, Sampaio I, Souza R, Sales JB, Rodrigues-Filho LF, Tchaika L, Carvalho-Costa LF (2018) DNA-based identification reveals illegal trade of threatened shark species in a global elasmobranch conservation hotspot. Sci Rep 8:3347

    PubMed  PubMed Central  Google Scholar 

  • Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux JC (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31:1093–1106

    Google Scholar 

  • Ferreira CEL, Gonçalves JEA (2006) Community structure and diet of roving herbivorous reef fishes in the Abrolhos Archipelago, south-western Atlantic. J Fish Biol 69:1533–1551

    Google Scholar 

  • Ferreira CM, Coni EOC, Medeiros DV, Sampaio CLS, Reis-Filho JA, Barros F, Loiola M, Costa Nunes JACC (2015) Community structure of shallow rocky shore fish in a tropical bay of the southwestern Atlantic. Braz J Oceanogr 63(4):379–396

    Google Scholar 

  • Ferreira CEL, Luiz OJ, Floeter SR, Lucena MB, Barbosa MC, Rocha RC, Rocha LA (2015) First record of invasive lionfish (Pterois volitans) for the Brazilian coast. PLoS ONE 10(4):e0123002

    PubMed  PubMed Central  Google Scholar 

  • Floeter SR, Guimarães RZP, Rocha LA, Ferreira CEL, Rangel CA, Gasparini JL (2001) Geographic variation in reef-fish assemblages along the Brazilian coast. Glob Ecol Biogeogr 10:423–433

    Google Scholar 

  • Floeter SR, Halpern BS, Ferreira CEL (2006) Effects of fishing protection on Brazilian reef fishes. Biol Conserv 128:391–402

    Google Scholar 

  • Floeter SR, Krohling W, Gasparini JL, Ferreira CEL, Zalmon IR (2007) Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover. Environ Biol Fishes 78:147–160

    Google Scholar 

  • Fontoura L, Cantor M, Longo GO, Bender MG, Bonaldo RM, Floeter SR (2020) The macroecology of reef fish agonistic behaviour. Ecography 43:1278–1290. https://doi.org/10.1111/ecog.05079

    Article  Google Scholar 

  • Fowler AM, Booth DJ (2012) Evidence of sustained populations of a small reef fish on artificial structures. Does depth affect production on artificial reefs? J Fish Biol 80(3):613–629

    CAS  PubMed  Google Scholar 

  • Francini-Filho RB, Asp NE, Siegle E, Hocevar J, Lowyck K, D’Avila N, Vasconcelos AA, Baitelo R, Rezende CE, Omachi CY, Thompson CC, Thompson FL (2018) Perspectives on the Great Amazon Reef: Extension, Biodiversity, and Threats. Front Mar Sci 5:142

    Google Scholar 

  • Frédou T, Ferreira BP, Letourneur Y (2006) A univariate and multivariate study of reef fisheries off northeastern Brazil. ICES J Mar Sci 63:883e896

    Google Scholar 

  • Frédou T, Ferreira BP, Letourneur Y (2009) Assessing the stocks of the primary snappers caught in Northeastern Brazilian Reef Systems. 2-A multi-fleet age-structured approach. Fish Res 99:97–105

    Google Scholar 

  • Freitas LM, Oliveira MDM, Leão ZMAN, Kikuchi RKP (2019) Effects of turbidity and depth on the bioconstruction of the Abrolhos reefs. Coral Reefs 38:241–253

    Google Scholar 

  • Froese R, Pauly D (ed) (2019) FishBase. World Wide Web electronic publication. www.fishbase.org, accessed in April 2019

  • Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian Islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264

    Google Scholar 

  • Friedlander A, Sandin S, DeMartini EE, Sala E (2010) Spatial patterns of the structure of reef fish assemblages at a pristine atoll in the central Pacific. Mar Ecol Prog Ser 410:219–231

    Google Scholar 

  • Friedlander AM, Caselle JE, Ballesteros E, Brown EK, Turchik A, Sala E (2014) The real bounty: marine biodiversity in the Pitcairn Islands. PLoS ONE 9(6):e100142

    PubMed  PubMed Central  Google Scholar 

  • Fujii MT, Cocentino ALM, Pereira SMB (2001) Ceramium nitens (Ceramiaceae, Rhodophyta), an uncommon species from Brazil. Revista Brasileira de Botânica 24(3):359–363. https://doi.org/10.1590/s0100-84042001000300014

    Article  Google Scholar 

  • FUNBIO (2019) Termo de referência para contratação de consultoria pessoa jurídica especializada para elaborar o plano de manejo da unidade de conservação “Parque Estadual Marinho do Parcel de Manuel Luís”, no estado do Maranhão (termo de referência no. 2018.0822.00057-5). Available only in portuguese at https://www.funbio.org.br/wp-content/uploads/2020/01/TdR-2018.0822.00057-5.pdf. Accessed 10 June 2020

  • Gerhardinger LC, Bertoncini AA, Hostin-Silva, (2006) Local ecological knowledge and Goliath grouper spawning aggregations in the South Atlantic Ocean: Goliath grouper spawning aggregations in Brazil. Traditional Marine Resource Management and Knowledge Information Bulletin 20:33–34

    Google Scholar 

  • Gouveia NA, Gherardi DFM, Wagner FH, Paes ET, Coles VJ, Aragão LEOC (2019) The salinity structure of the Amazon river plume drives spatiotemporal variation of oceanic primary productivity. J Geophys Res Biogeosci 124:147–165

    Google Scholar 

  • Graham NAJ, McClanaham TR (2013) The last call to wilderness? Bioscience 63(5):397–402

    Google Scholar 

  • Green AL, Fernandes L, Almany G, Abesamis R, McLeod E, Aliño PM, White AT, Salm R, Tanzer J, Pressey RL (2014) Designing marine reserves for fisheries management, biodiversity conservation, and climate change adaptation. Coast Manage 42:143–159

    Google Scholar 

  • Gualberto LPS, El-Robrini M (2005) Faciologia da cobertura sedimentar superficial da plataforma continental do Maranhão. Estudos Geológicos 15:234–243

    Google Scholar 

  • Guilhem I, Mais B, Creed J (2020) Impact of invasive Tubastraea spp. (Cnidaria: Anthozoa) on the growth of the space dominating tropical rocky-shore zoantharian Palythoa caribaeorum (Duchassaing and Michelotti, 1860). Aquat Invasions 15:98–113

    Google Scholar 

  • Hancock P (2020) Stellar Banner. Accessed on 18th of June 2020. Available at https://shipwrecklog.com/log/2020/02/stellar-banner/

  • Harborne AR, Mumby PJ (2018) FAQs about Caribbean parrotfish management and their role in reef resilience. In: Bonaldo RM (ed) Hoey AS. Biology of parrotfishes. CRC Press Taylor & Francis Group, Florida, USA

    Google Scholar 

  • Honório PPF, Ramos RTC, Feitoza BM (2010) Composition and structure of reef fish communities in Paraiba State, north-eastern Brazil. J Fish Biol 77(4):907–926

    PubMed  Google Scholar 

  • Hothorn T, Bretz F, Peter W (2008) Simultaneous inference in general parametric models. Biometrical J 20:346–363

    Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25(11):633–642

    PubMed  Google Scholar 

  • ICMBio (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Vols I - 6. Brasília, DF: ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade)/MMA (Ministério do Meio Ambiente), 492 pp

  • IBAMA – Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais (2018) Online permit documentation. Available at: https://servicos.ibama.gov.br/licenciamento/consulta_empreendimentos.php. Accessed 26 Feb 2018

  • Jackson JBC, Sala E (2001) Unnatural oceans. Sci Mar 65:273–281

  • Klein EL, Moura CAV (2003) Síntese geológica e geocronológica do Cráton São Luís e do Cinturão Gurupi na região do Rio Gurupi (NE-Pará / NW-Maranhão). Geol USP Sér Cient 3:97–112

    CAS  Google Scholar 

  • Leão ZMAN, Kikuchi PKP, Testa V (2003) Corals and coral reefs of Brazil. In: Cortés J (ed) Latin American Coral Reefs. Elsevier Science B. p 9–52. https://doi.org/10.1016/B978-044451388-5/50003-5

  • León PSD, Acuña-Marrero D, Rastoin E, Friedlander AM, Donovan MK, Sala E (2016) Largest global shark biomass found in the northern Galápagos Islands of Darwin and Wolf. PeerJ, 4

  • Lellys NT, De Moura RL, Bonaldo RM, Francini-Filho RB, Gibran FZ (2019) Parrotfish functional morphology and bioerosion on SW Atlantic reefs. Marine Ecol Prog Ser 629:149–163. https://doi.org/10.3354/meps13102

    Article  Google Scholar 

  • Loiola M, Cruz ICS, Lisboa DS, Mariano-Neto E, Leão ZMAN, Oliveira MDM, Kikuchi RKP (2019) Structure of marginal coral reef assemblages under different turbidity regime. Mar Environ Res 147:138–148

    CAS  PubMed  Google Scholar 

  • Longo GO, Floeter SR (2012) Comparison of remote video and diver’s direct observations to quantify reef fishes feeding on benthos in coral and rocky reefs. J Fish Biol 81:1773–1780

    CAS  PubMed  Google Scholar 

  • Longo GO, Ferreira CEL, Floeter SR (2014) Herbivory drives large-scale spatial variation in reef fish trophic interactions. Ecol Evol 4:4553–4566

    PubMed  PubMed Central  Google Scholar 

  • Longo GO, Hay ME, Ferreira CEL, Floeter SR (2019) Trophic interactions across 61 degrees of latitude in the Western Atlantic. Global Ecol Biogeogr 28:107–117

    Google Scholar 

  • Luiz OJ, Allen AP, Robertson DR, Floeter SR, Kulbicki M, Vigliola L, Becheler R, Madin JS (2013) Adult and larval traits as determinants of geographic range size among tropical reef fishes. P Natl Acad Sci USA 110(41):16498–16502

    CAS  Google Scholar 

  • Magris RA, Grech A, Pressey RL (2018) Cumulative human impacts on coral reefs: assessing risk and management implications for Brazilian coral reefs. Diversity 10(2):26

    Google Scholar 

  • Mahiques MM, Siegle E, Francini-filho RB, Thompson FL, Rezende CE, Gomes JD, Asp NE (2019) Insights on the evolution of the living Great Amazon Reef System, equatorial West Atlantic. Sci Rep 9:13699

    PubMed  PubMed Central  Google Scholar 

  • Maida M, Ferreira BP (1997) Coral reefs of Brazil overview and field guide. Proceedings 8th International Coral Reef Symposium 1:263–274

    Google Scholar 

  • Martins APB, Feitosa LM, Lessa RP, Almeida ZS, Heupel M, Silva WM, Tchaicka L, Nunes JLS (2018) Analysis of the supply chain and conservation status of sharks (Elasmobranchii: Superorder Selachimorpha) based on fisher knowledge. PLoS ONE 13(3):e0193969

    PubMed  PubMed Central  Google Scholar 

  • McCook LJ (1996) Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: cross-shelf transplants. Mar Ecol Prog Ser 139:179–192

    Google Scholar 

  • Meirelles PM, Amado-Filho GM, Pereira-Filho GH, Pinheiro HT, de Moura RL, Joyeux J-C et al (2015) Baseline assessment of mesophotic reefs of the Vitória-Trindade seamount chain based on water quality, microbial diversity, benthic cover and fish biomass data. PLoS ONE 10(6):e0130084. https://doi.org/10.1371/journal.pone.0130084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MMA – Ministério do Meio Ambiente (2016) Portaria N°19 - Plano de Ação Nacional para a Conservação dos Ambientes Coralíneos – PAN Corais (Processo nº 02070.001393/2013–01).

  • Morais RA, Ferreira CEL, Floeter SR (2017) Spatial patterns of fish standing biomass across Brazilian reefs. J Fish Biol 91(6):1642–1667

    CAS  PubMed  Google Scholar 

  • Motta FS, Moura RL, Francini-Filho RB, Namora RC (2009) Notas sobre a biologia reprodutiva e alimentar de elasmobrânquios no Parque Estadual Marinho Parcel Manoel Luís, Maranhão, Brasil. Pan-Am J Aquat Sci 4:593–598

    Google Scholar 

  • Mouillot D, Villeger S, Parravicini V, Kulbicki M, Arias-Gonzalez JE, Bender M, Chabanet P, Floeter SR, Friedlander A, Vigliola L, Bellwood DR (2014) Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc Natl Acad Sci 111(38):13757–13762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moura RL, Rodrigues-Martins MC, Francini-Filho RB, Sazima I (1999) Unexpected richness of reef corals near the southern Amazon river mouth. Coral Reefs 18:170

    Google Scholar 

  • Moura RL, Secchin NA, Amado-Filho GM, Francini-Filho RB, Freitas MO, Minte-Veta CV, Teixeira JB, Thompson FL, Dutra GF, Sumida PYG, Guth AZ, Lopes RM, Bastos AC (2013) Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank. Cont Shelf Res 70(1):109–117

    Google Scholar 

  • Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM, Bastos AC, Almeida MG, Silva JM Jr, Araujo BF, Brito FP, Rangel TP, Oliveira BCV, Bahia RG, Paranhos RP, Dias RJS, Siegle E, Figueiredo AG Jr, Pereira RC, Leal CV, Hajdu E, Asp NE, Gregoracci GB, Neumann-Leitão S, Yager PL, Francini-Filho RB, Fróes A, Campeão M, Silva BS, Moreira APB, Oliveira L, Soares AC, Araujo L, Oliveira NL, Teixeira JB, Valle RAB, Thompson CC, Rezende CE, Thompson FL (2016) An extensive reef system at the Amazon River mouth. Sci Adv 2:e1501252

    PubMed  PubMed Central  Google Scholar 

  • Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conserv Biol 4(4):355–364

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2015) vegan: Community Ecology Package. R package version 2:3–4

    Google Scholar 

  • Omachi CY, Aspa NE, Siegleb E, Couceiro MAA, Francini-Filho RB, Thompson FL (2019) Light availability for reef-building organisms in a plume-influenced shelf. Cont Shelf Res 181:25–33

    Google Scholar 

  • Perkol-Finkel S, Shashar N, Benayahu Y (2006) Can artificial reefs mimic natural reef communities? The roles of structural features and age. Marine Environ Res 61(2):121–135. https://doi.org/10.1016/j.marenvres.2005.08.001

    Article  CAS  Google Scholar 

  • Pinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, Di Dario F, Ferreira CEL, Francini-Filho RB, Gasparini JL et al (2018) Southwestern Atlantic reef fishes: zoogeographic patterns and ecological drivers reveal a secondary biodiversity center in the Atlantic Ocean. Divers Distrib 24:951–965

    Google Scholar 

  • Richter C, Wunsch M, Rasheed M, Kötter I, Badran MI (2001) Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413:726–730

    CAS  PubMed  Google Scholar 

  • Rilov G, Benayahu Y (2000) Fish assemblage on natural versus vertical artificial reefs: the rehabilitation perspective. Mar Biol 136(5):931–952

    Google Scholar 

  • Robinson JPW, Williams ID, Edwards AM, McPherson J, Yeager L, Vigliola L, Baum JK (2017) Fishing degrades size structure ofcoral reef fish communities. Global Change Biol 23(3):1009–1022. https://doi.org/10.1111/gcb.13482

    Article  PubMed  Google Scholar 

  • Rocha LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 30(8):1161–1171

    Google Scholar 

  • Rocha LA, Rosa IL (2001) Baseline assessment of reef fish assemblages of Parcel Manuel Luiz Marine State Park, Maranhão, north-east Brazil. J Fish Biol 58(4):985–998

    Google Scholar 

  • Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal and the comparative phylogeography of three Atlantic Acanthurus (Teleostei: Acanthuridae). Mol Ecol 11(2):243–252

    CAS  PubMed  Google Scholar 

  • Roos NC, Pennino MG, Carvalho AR, Longo GO (2019) Drivers of abundance and biomass of Brazilian parrotfishes. Mar Ecol Prog Ser 623:117–130

    Google Scholar 

  • Roos NC, Taylor BM, Carvalho AR, Longo GO (2020) Demography of the largest and most endangered Brazilian parrotfish, Scarus trispinosus, reveals overfishing. Endang Species Res 41:319–327

    Google Scholar 

  • Russ GR, Questel SA, Rizzari JR, Alcala AC (2015) The parrotfish–coral relationship: refuting the ubiquity of a prevailing paradigm. Mar Biol 162:2029–2045

    Google Scholar 

  • Sala E, Ballesteros E, Dendrinos P, Di Franco A, Ferretti F, Foley D, Simonetta F, Friedlander A, Garrabou J, Güçlüsoy H, Guidetti P, Halpern BS, Hereu B, Karamanlidis AA, Kizilkaya Z, Macpherson E, Mangialajo L, Mariani S, Micheli F, Pais A, Riser K, Rosenberg AA, Sales M, Selkoe KA, Starr R, Tomas F, Zabala M (2012) The structure of Mediterranean rocky reef ecosystems across environmental and human gradients, and conservation implications. PLoS ONE 7(2):e32742

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sandin S, Smith J, Demartini E, Dinsdale E, Donner S et al (2008) Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3:e1548

    PubMed  PubMed Central  Google Scholar 

  • Santos CSG, Lino JB, Veras PC, Amado-Filho GM, Francini-Filho RB, Motta FS, Moura RL, Pereira-Filho GH (2016) Environmental licensing on rhodolith beds: insights from a worm. Nat Conserv 14(2):137–141

    Google Scholar 

  • Schutter VGW, Selig ER, Bruno JF (2010) Regional spatio-temporal trends in Caribbean coral reef benthic communities. Mar Ecol Prog Ser 402:115–122

    Google Scholar 

  • Segal B, Castro CB (2011) Coral community structure and sedimentation at different distances from the coast of the Abrolhos Bank. Brazil Braz J Oceanogr 59(2):119–129

    Google Scholar 

  • Simon T, Pinheiro HT, Joyeux J-C (2011) Target fishes on artificial reefs: evidences of impacts over nearby natural environments. Sci Total Environ 409(21):4579–4584

    CAS  PubMed  Google Scholar 

  • Simon T, Joyeux J-C, Pinheiro HT (2013) Fish assemblages on shipwrecks and natural rocky reefs strongly differ in trophic structure. Mar Environ Res 90:55–65

    CAS  PubMed  Google Scholar 

  • Soares MO, Lotufo TMC, Vieira ML, Salani S, Hadju E, Matthews-Cascon, H, Leão ZMAN, Kikuchi RKP (2016) Brazilian marine animal forests: a new world to discover in the Southwestern Atlantic. p.1–38 In: Rossi S, Bramanti L, Gori A, del Valle COS (Org.) Marine Animal Forests. 1ed. Springer, Cham

  • Stukel MR, Coles VJ, Brooks MT, Hood RR (2014) Top-down, bottom-up and physical controls on diatom-diazotroph assemblage growth in the Amazon River plume. Biogeosciences 11:3259–3278

    Google Scholar 

  • Terashima H, Sato M, Kawasaki H, Thiam D (2007) Quantitative biological assessment of a newly installed artificial reef in Yenne. Senegal Zool Stud 46(1):69–82

    Google Scholar 

  • Trygonis V, Sini M (2012) photoQuad: a dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. J Exp Mar Biol Ecol 424–425:99–108

    Google Scholar 

  • Tucker CM, Cadotte MW, Carvalho SB, Davies TJ, Ferrier S, Fritz SA, Grenyer R, Helmus MR, Jin LS, Mooers AO, Pavoine S, Purschke O, Redding DW, Rosauer DF, Winter M, Mazel F (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev 92:698–715

    PubMed  Google Scholar 

  • UNCTAD - United Nations Conference on Trade and Development (2018) Review of maritime transport. Geneva, Switzerland, 162p

  • Vale NF, Amado-Filho GM, Braga JC, Brasileiro PS, Karez CS, Moraes FC, Bahia RG, Bastos AC, Moura RL (2018) Structure and composition of rhodoliths from the Amazon River mouth, Brazil. A S Am Earth Sci 84:149–159

    Google Scholar 

  • Van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, Hajdu E, Pisera AB, Manconi R, Schönberg C, Klautau M, Picton B, Kelly M, Vacelet J, Dohrmann M, Díaz M-C, Cárdenas P, Carballo JL, Rios P, Downey R (2017) World Porifera database. Accessed at https://www.marinespecies.org/porifera on 2019–10–20

  • Vázquez DP, Melián CJ, Williams NM, Blüthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116(7):1120–1127

    Google Scholar 

  • Vermeij MJA, Moorselaar IV, Engelhard S, Hörnlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrowth coral in the Caribbean. PLoS ONE 5(12):e14312

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vilar CC, Magris RA, Loyola R, Joyeux J-C (2020) Strengthening the synergies among global biodiversity targets to reconcile conservation and socio-economic demands. Aquat Conserv 30(3):497–513

    Google Scholar 

  • Ward-Paige C, Flemming JM, Lotze HK (2010) Overestimating fish counts by non-instantaneous visual censuses: Consequences for population and community descriptions. PLoS ONE 5(7):1–9. https://doi.org/10.1371/journal.pone.0011722

    Article  CAS  Google Scholar 

  • Williams ID, Polunin NVC (2001) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19:358–366

    Google Scholar 

Download references

Acknowledgements

We are grateful to Márcia F Coura for sharing key information that supported the development of this manuscript, and Silveira M for logistic and administrative support; Angela M Canterle, Luisa Fontoura, Davi Candido, Gustavo L Kasper and Camille VLC Silva for assistance with video and photo analysis, species identification and sample processing. We thank the crew of the catamaran “Seo Manélis” for taking the team safely to the PML, and back. This research is a product of the Brazilian Marine Biodiversity Research Network (SISBIOTA–Mar) and was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq #563276/2010‐0) and Fundação de Amparo à Pequisa e Inovação do Estado de Santa Catarina (FAPESC #6308/2011-8) through the grants leaded by SRF. The Secretaria Estadual do Meio Ambiente do Estado do Maranhão provided sampling permits for the Parcel de Manuel Luís Marine State Park (SEMA #06/2012 and 2013).

Author information

Authors and Affiliations

  1. Laboratório de Ecologia e Conservação de Ambientes Recifais, Universidade Federal Fluminense, Outeiro de São João Batista - s/n, Niterói, Rio de Janeiro, 24020-005, Brazil

    C. A. M. M. Cordeiro & A. W. Aued

  2. Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro, 68020, Rio de Janeiro, RJ, Brasil

    C. A. M. M. Cordeiro

  3. Centro de Biologia Marinha, Universidade de São Paulo, Rodovia Manuel Hipólito do Rego - km 131.5 - s/n, São Sebastião, São Paulo, 11600-000, Brazil

    J. P. Quimbayo

  4. Laboratório de Ecologia Bentônica, Universidade Federal da Bahia, Rua Augusto Viana - s/n, Salvador, Bahia, 40110-909, Brazil

    J. A. C. C. Nunes

  5. Laboratório de Biogeografia e Macroecologia Marinha, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, 88040-900, Brazil

    L. T. Nunes & S. R. Floeter

  6. Phycology Laboratory, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, 88040-900, Brazil

    M. N. Sissini & P. A. Horta

  7. Laboratório de Ictiologia e Conservação, Universidade Federal de Alagoas, Unidade Penedo. Av. Beira Rio, s/n, Penedo, Alagoas, 57200-000, Brazil

    C. L. S. Sampaio

  8. College of Science and Engineering and ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, 4811, Australia

    R. A. Morais

  9. Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista - s/n, Rio de Janeiro, Rio de Janeiro, 20940-040, Brazil

    J. L. Carraro & E. Hajdu

  10. California Academy of Sciences, 55 Music Concourse Dr, San Francisco, CA, 94118, USA

    L. A. Rocha

  11. Laboratório de Ecologia de Ambientes Recifais, Universidade Federal de Santa Catarina, Instituto Coral Vivo, Florianópolis, Santa Catarina, 88040-900, Brazil

    B. Segal

Authors
  1. C. A. M. M. Cordeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. P. Quimbayo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. A. C. C. Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. T. Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. N. Sissini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. L. S. Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. A. Morais
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. A. Horta
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. W. Aued
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J. L. Carraro
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. E. Hajdu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. L. A. Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. B. Segal
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. S. R. Floeter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. A. M. M. Cordeiro.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Mark Vermeij

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 6195 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cordeiro, C.A.M.M., Quimbayo, J.P., Nunes, J.A.C.C. et al. Conservation status of the southernmost reef of the Amazon Reef System: the Parcel de Manuel Luís. Coral Reefs 40, 165–185 (2021). https://doi.org/10.1007/s00338-020-02026-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-02026-1

Keywords

Search

Navigation