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Benthic Estuarine Assemblages of the Eastern Marine Brazilian Ecoregion (EME)

  • Angelo Fraga Bernardino
  • Alice Reis
  • Antônio Carlos Dórea Pereira Filho
  • Luiz Eduardo de Oliveira Gomes
  • Lorena Bonno Bissoli
  • Francisco Carlos Rocha de BarrosJr
Chapter
Part of the Brazilian Marine Biodiversity book series (BMB)

Abstract

The Eastern Brazil Marine Ecoregion includes over 50 estuaries along roughly 1200 km of coastline with latitudinal changes in mean rainfall and average yearly atmospheric temperatures. Estuarine ecosystems within this ecoregion have been relatively well studied with respect to the impacts from human pollution and the benthic biodiversity in mangrove forests, estuarine channels, and tidal flats. Benthic estuarine assemblages exhibit typical spatial changes with salinity gradients, with higher diversity towards euhaline sectors. Macrofaunal abundance and biomass are typically higher within mud and organic-rich sediments along tidal flats, although spatial patterns often differ within sectors (euhaline to oligohaline) and between estuaries in the ecoregion. The largest coastal bays and estuaries of the Eastern Marine Ecoregion are impacted by variable levels of sewage and industrial discharge and mangrove forest removal. Although the effects of these impacts likely result in changes in the amount or quality of water supply, decrease of fish stocks, and transformations of food webs, there is limited understanding of the potential loss of estuarine services. Climate change effects including higher mean atmospheric temperatures and lower rainfall are predicted to significantly impact estuarine benthic assemblages in the Eastern ecoregion and localized effects of higher salinity are already in place at some areas. Further studies need to understand accurately what are the most important estuarine functions and services in order to evaluate how different local (biological invasion, habitat destruction, pollution) and global (climate change) impacts will affect these systems. Concomitantly, estuarine areas for conservation must be identified, implemented and managed in Eastern Brazil Marine Ecoregion.

Keywords

Eastern Brazil Benthic ecology Impacts Mangroves Estuaries 

Notes

Acknowledgments

AFB was supported by FAPES (52638090/2011; 61847429/2013) and CNPq (470542/2013-6; 441243/2016-9) research grants. FB was supported by CNPq fellowship (239978/2012-9; 306332/2014-0), Projeto BTS, PRONEX and Baías da Baía (PET 0035/2012). LEOG, LBB, LR, and AD were supported by graduate scholarships from FAPESB/FAPES/CAPES/CNPq. This is also a PELD-HCES contribution #003.

References

  1. Almeida ACS, Souza FBC, Gordon DP et al (2015) The non-indigenous bryozoan Triphyllozoon (Cheilostomata: Phidoloporidae) in the Atlantic: morphology and dispersion on the Brazilian coast. Zoologia (Curitiba) 32:476–484. https://doi.org/10.1590/S1984-46702015000600007 CrossRefGoogle Scholar
  2. Alongi DM (2002) Present state and future of the world's mangrove forests. Environ Conserv 29:331–349. https://doi.org/10.1017/S0376892902000231 CrossRefGoogle Scholar
  3. Alvares CA, Stape JL, Sentelhas PC et al (2014) Koppen's climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507 CrossRefGoogle Scholar
  4. Anderson MJ (2008) Animal-sediment relationships re-visited: characterising species’ distributions along an environmental gradient using canonical analysis and quantile regression splines. J Exp Mar Biol Ecol 366:16–27. https://doi.org/10.1016/j.jembe.2008.07.006 CrossRefGoogle Scholar
  5. Arrivabene HP, Souza I, Có WLO et al (2014) Functional traits of selected mangrove species in Brazil as biological indicators of different environmental conditions. Sci Total Environ 476–477:496–504. https://doi.org/10.1016/j.scitotenv.2014.01.032 CrossRefPubMedGoogle Scholar
  6. Barros F, Blanchet H, Hammerstrom K et al (2014) A framework for investigating general patterns of benthic β -diversity along estuaries. Estuar Coast Shelf Sci 149:223–231. https://doi.org/10.1016/j.ecss.2014.08.025 CrossRefGoogle Scholar
  7. Barros F, Carvalho GC, Costa Y et al (2012) Subtidal benthic macroinfaunal assemblages in tropical estuaries: generality amongst highly variable gradients. Mar Environ Res 81:43–52. https://doi.org/10.1016/j.marenvres.2012.08.006 CrossRefPubMedGoogle Scholar
  8. Barros F, Hatje V, Figueiredo MB et al (2008) The structure of the benthic macrofaunal assemblages and sediments characteristics of the Paraguaçu estuarine system, NE, Brazil. Estuar Coast Shelf Sci 78:753–762CrossRefGoogle Scholar
  9. Bernardino AF, Netto SA, Pagliosa PR et al (2015) Predicting ecological changes on benthic estuarine assemblages through decadal climate trends along Brazilian marine ecoregions. Estuar Coast Shelf Sci 166:74–82. https://doi.org/10.1016/j.ecss.2015.05.021 CrossRefGoogle Scholar
  10. Bernardino AF, Pagliosa PR, Christofoletti RA et al (2016) Benthic estuarine communities in Brazil: moving forward to long term studies to assess climate change impacts. Braz J Oceanogr 64:81–96. https://doi.org/10.1590/S1679-875920160849064sp2 CrossRefGoogle Scholar
  11. Bernardino AF, Gomes LEO, Hadlich HL et al (2018) Mangrove clearing impacts on macrofaunal assemblages and benthic food webs in a tropical estuary. Mar Poll Bull 126:228–235. https://doi.org/10.1016/j.marpolbul.2017.11.008 CrossRefGoogle Scholar
  12. Bishop MJ, Powers SP, Porter HJ et al (2006) Benthic biological effects of seasonal hypoxia in a eutrophic estuary predate rapid coastal development. Estuar Coast Shelf Sci 70:415–422. https://doi.org/10.1016/j.ecss.2006.06.031 CrossRefGoogle Scholar
  13. Bissoli LB, Bernardino AF (2018) Benthic macrofaunal structure and secondary production in tropical estuaries on the Eastern Marine Ecoregion of Brazil. PeerJ 6:e4441. https://doi.org/10.7717/peerj.4441 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Boone Kauffman J, Arifanti VB, Bernardino AF, Ferreira TO, Murdiyarso D, Cifuentes M, Norfolk J (2018) And details for land-use carbon footprints arise from quantitative and replicated studies. Front Ecol Environ 16(1):12–13CrossRefGoogle Scholar
  15. Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000 CrossRefGoogle Scholar
  16. Cardoso PG, Raffaelli D, Pardal MA (2008) The impact of extreme weather events on the seagrass Zostera noltii and related Hydrobia ulvae population. Mar Pollut Bull 56:483–492. https://doi.org/10.1016/j.marpolbul.2007.11.006 CrossRefPubMedGoogle Scholar
  17. Carvalho LRS, Barros F (2017) Physical habitat structure in marine ecosystems: the meaning of complexity and heterogeneity. Hydrobiol 797:1–9. https://doi.org/10.1007/s10750-017-3160-0 CrossRefGoogle Scholar
  18. Chen R, Twilley RR (1999) Patterns of mangrove forest structure and soil nutrient dynamics along the Shark River Estuary, Florida. Estuaries 22:955–970. https://doi.org/10.2307/1353075 CrossRefGoogle Scholar
  19. Costa P, Dórea A, Mariano-Neto E et al (2015) Are there general spatial patterns of mangrove structure and composition along estuarine salinity gradients in Todos os Santos Bay? Estuar Coast Shelf Sci 166:83–91. https://doi.org/10.1016/j.ecss.2015.08.014 CrossRefGoogle Scholar
  20. Cortelezzi A, Capítulo AR, Boccardi L et al (2007) Benthic assemblages of a temperate estuarine system in South America: transition from a freshwater to an estuarine zone. J Mar Syst 68(3–4):569–580CrossRefGoogle Scholar
  21. Demopoulos AWJ, Fry B, Smith CR (2007) Food web structure in exotic and native mangroves: a Hawaii-Puerto Rico comparison. Oecologia 153:675–686. https://doi.org/10.1007/s00442-007-0751-x CrossRefPubMedGoogle Scholar
  22. Demopoulos AWJ, Smith CR (2010) Invasive mangroves alter macrofaunal community structure and facilitate opportunistic exotics. Mar Ecol Prog Ser 404:51–67. https://doi.org/10.3354/meps08483 CrossRefGoogle Scholar
  23. Dolbeth M, Cardoso PG, Ferreira SM et al (2007) Anthropogenic and natural disturbance effects on a macrobenthic estuarine community over a 10-year period. Mar Pollut Bull 54:576–585. https://doi.org/10.1016/j.marpolbul.2006.12.005 CrossRefPubMedGoogle Scholar
  24. Dolbeth M, Cardoso PG, Grilo TF et al (2011) Long-term changes in the production by estuarine macrobenthos affected by multiple stressors. Estuar Coast Shelf Sci 92:10–18. https://doi.org/10.1016/j.ecss.2010.12.00 CrossRefGoogle Scholar
  25. Donato DC, Kauffman JB, Murdiyarso D et al (2011) Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–297CrossRefGoogle Scholar
  26. Doney SC, Ruckelshaus M, Duffy JE (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37. https://doi.org/10.1146/annurev-marine-041911-111611 CrossRefGoogle Scholar
  27. Edgar GJ, Barrett NS, Last PR (1999) The distribution of macroinvertebrates and fishes in Tasmanian estuaries. J Biogeogr 26:1169–1189. https://doi.org/10.1046/j.1365-2699.1999.00365.x CrossRefGoogle Scholar
  28. Eisma D (1986) Flocculation and deflocculation of suspended matter in estuaries. Neth J Sea Res 20:183–199. https://doi.org/10.1016/0077-7579(86)90041-4 CrossRefGoogle Scholar
  29. Elliott M, Quintino V (2007) The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar Pollut Bull 54:640–645. https://doi.org/10.1016/j.marpolbul.2007.02.003 CrossRefPubMedGoogle Scholar
  30. Faraco LFD, Andriguetto Filho JM, Lana PC (2010) A methodology for assessing the vulnerability of mangroves and fisherfolk to climate change. Panam. J Aquat Sci 5:205–223Google Scholar
  31. Faraco LFD, Lana PC (2004) Leaf-consumption levels in subtropical mangroves of Paranaguá Bay (SE Brazil). Wetl Ecol Manag 12:115–122. https://doi.org/10.1023/B:WETL.0000021666.42546.c2 CrossRefGoogle Scholar
  32. Gilberto DA, Bremec CS, Acha EM et al (2004) Large-scale spatial patterns of benthic assemblages in the SW Atlantic: the Río de la Plata estuary and adjacent shelf waters. Estuar Coast Shelf Sci 61:1–13. https://doi.org/10.1016/j.ecss.2004.03.015 CrossRefGoogle Scholar
  33. Golden Gate Weather Services Comparative Climatic Data (2016) http://ggweather.com/enso/oni.htm. Accessed 15 Mar 2017
  34. Granek E, Ruttemberg BI (2008) Changes in biotic and abiotic processes following mangrove clearing. Estuar Coast Shelf Sci 80:555–562. https://doi.org/10.1016/j.ecss.2008.09.012 CrossRefGoogle Scholar
  35. Grilo CF, Neto RR, Vicente MA et al (2013) Evaluation of the influence of urbanization processes using mangrove and fecal markers in recent organic matter in a tropical tidal flat estuary. Appl Geochem 38:82–91. https://doi.org/10.1016/j.apgeochem.2013.08.009 CrossRefGoogle Scholar
  36. Gomes LEO, Correa LB, Sá F et al (2017) The impacts of the Samarco mine tailing spill on the Rio Doce estuary, eastern Brazil. Mar Pollut Bull 120:28–36CrossRefPubMedGoogle Scholar
  37. Harris LA, Duarte CM, Nixon SW (2006) Allometric laws and prediction in estuarine and coastal ecology. Estuar Coasts 29:340–344. https://doi.org/10.1007/BF02782002 CrossRefGoogle Scholar
  38. Hatje V, Barros F (2012) Overview of the 20th century impact of trace metal contamination in the estuaries of Todos os Santos Bay: past, present and future scenarios. Mar Pollut Bull 64:2603–2614. https://doi.org/10.1016/j.marpolbul.2012.07.009 CrossRefPubMedGoogle Scholar
  39. Hatje V, Barros F, Figueiredo DG et al (2006) Trace metal contamination and benthic assemblages in Subaé estuarine system. Brazil. Mar Pollut Bull 52:969–987. https://doi.org/10.1016/j.marpolbul.2006.04.016 CrossRefGoogle Scholar
  40. Hatje V, Barros F, Magalhaes W et al (2008) Trace metals and benthic macrofauna distributions in Camamu Bay, Brazil: sediment quality prior oil and gas exploration. Mar Pollut Bull 56:363–370. https://doi.org/10.1016/j.marpolbul.2007.10.029 CrossRefPubMedGoogle Scholar
  41. Hatje V, de Souza MM, Ribeiro LF et al (2016) Detection of environmental impacts of shrimp farming through multiple lines of evidence. Environ Pollut 219:1–13. https://doi.org/10.1016/j.envpol.2016.06.056 CrossRefGoogle Scholar
  42. Hatje V, Pedreira RMA, de Rezende CE, Schettini CAF, de Souza GC, Marin DC, Hackspacher PC (2017) The environmental impacts of one of the largest tailing dam failures worldwide. Sci Rep 7(1):10706CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328(5985):1523–1528. https://doi.org/10.1126/science.1189930 CrossRefPubMedGoogle Scholar
  44. Jesus H, Costa EA, Mendonça ASF et al (2004) Distribuição de metais pesados em sedimentos do sistema estuarino da ilha de Vitória-ES. Quim Nova 27:378–386. https://doi.org/10.1590/S0100-40422004000300004 CrossRefGoogle Scholar
  45. Kauffman JB, Arifanti VB, Trejo HH et al (2017) The jumbo carbon footprint of a shrimp: carbon losses from mangrove deforestation. Front Ecol Environ 15(4):183–188. https://doi.org/10.1002/fee.1482 CrossRefGoogle Scholar
  46. Kauffman JB, Bernardino AF, Ferreira TO, Bolton NW, de Gomes LE, O, Nobrega GN (2018) Shrimp ponds lead to massive loss of soil carbon and greenhouse gas emissions in northeastern Brazilian mangroves. Ecol Evol. doi.org/10.1002/ece3.4079Google Scholar
  47. Kristensen E, Delefosse M, Quintana CO et al (2014) Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries. Front Mar Sci 1:1–14. https://doi.org/10.3389/fmars.2014.00041 CrossRefGoogle Scholar
  48. Krull M, Abessa DMS, Hatje V et al (2014) Integrated assessment of metal contamination in sediments from two tropical estuaries. Ecotoxicol Environ Saf 106:195–203. https://doi.org/10.1016/j.ecoenv.2014.04.038 CrossRefPubMedGoogle Scholar
  49. Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75:435–450. https://doi.org/10.1890/05-0549 CrossRefGoogle Scholar
  50. Lessa GC, Santos FM, Souza Filho PW et al (2018) Brazilian estuaries: a geomorphologic and oceanographic perspective. In: Lana PC, Bernardino AF (eds) Brazilian Estuaries. Springer International Publishing, Brazilian Marine Biodiversity. https://doi.org/10.1007/978-3-319-77779-5_4 Google Scholar
  51. Lopes RM (2009) Informe sobre as Espécies Exóticas Invasoras Marinhas no Brasil, Brasíilia, Ministério do Meio Ambiente, Série Biodiversidade doi: https://doi.org/10.1017/CBO9781107415324.004
  52. Lotze HK, Lenihan HS, Bourque BJ et al (2006) Depletion, degradation and recovery potential of estuaries and coastal seas. Science 312:1806–1809. https://doi.org/10.1126/science.1128035 CrossRefPubMedGoogle Scholar
  53. MacKay F, Cyrus D, Russell KL (2010) Macrobenthic invertebrate responses to prolonged drought in South Africa's largest estuarine lake complex. Estuar Coast Shelf Sci 86:553–567. https://doi.org/10.1016/j.ecss.2009.11.011 CrossRefGoogle Scholar
  54. Magalhães W, Barros F (2011) Structural and functional approaches to describe polychaete assemblages: ecological implications for estuarine ecosystems. Mar Fresh Res 62:918–922. https://doi.org/10.1071/MF10277 CrossRefGoogle Scholar
  55. Marengo JA, Ambrizzi T, da Rocha RP et al (2010) Future change of climate in Sotuh America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Clim Dyn 35:1073–1097. https://doi.org/10.1007/s00382-009-0721-6 CrossRefGoogle Scholar
  56. Mari X, Torréton JP, Trinh CBT et al (2012) Aggregation dynamics along a salinity gradient in the Bach dang estuary, North Vietnam. Estuar Coast Shelf Sci 96:151–158. https://doi.org/10.1016/j.ecss.2011.10.028 CrossRefGoogle Scholar
  57. Mariano DLS, Barros F (2015) Intertidal benthic macrofaunal assemblages: changes in structure along entire tropical estuarine salinity gradients. J Mar Biol Assoc UK 95:5–15. https://doi.org/10.1017/S002531541400126X CrossRefGoogle Scholar
  58. Mcleod E, Chmura GL, Bouillon S et al (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560. https://doi.org/10.1890/110004 CrossRefGoogle Scholar
  59. Miranda RJ, Costa Y, Lordes FL et al (2016a) New records of the alien cup-corals (Tubastraea spp.) within estuarine and reef systems in Todos os Santos Bay, southwestern Atlantic. Mar. Biodivers Rec 9:1–6. https://doi.org/10.1186/s41200-016-0053-2 CrossRefGoogle Scholar
  60. Miranda RJ, Cruz IC, Barros F (2016b) Effects of the alien coral Tubastraea tagusensis on native coral assemblages in a southwestern Atlantic coral reef. Mar Biol 163:1–12. https://doi.org/10.1007/s00227-016-2819-9 CrossRefGoogle Scholar
  61. Netto SA, Galluci F (2003) Meiofauna and macrofauna communities in a mangrove from the island of Santa Catarina, South Brazil. Hydrobiologia 505:159–170. https://doi.org/10.1023/B:HYDR.0000007304.22992.b2 CrossRefGoogle Scholar
  62. Netto SA, Lana PC (1999) The role of above-and belowground components of Spartina alterniflora (Loisel) and detritus biomass in structuring macrobenthic associations of Paranaguá Bay (SE, Brazil). Hydrobiologia 400:167–177. https://doi.org/10.1023/A:1003753001411 CrossRefGoogle Scholar
  63. Pendleton L, Donato DC, Murray BC et al (2012) Estimating global “blue carbon” emissions from conversion and degradation of vegetated coastal ecosystems. PLoS One 7:e43542. https://doi.org/10.1371/journal.pone.0043542 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pezy JP, Baffreau A, Dauvin JC (2017) What are the factors driving long-term changes of the suprabenthos in the seine estuary? Mar Pollut Bull 118:307. https://doi.org/10.1016/j.marpolbul.2017.03.008 CrossRefPubMedGoogle Scholar
  65. Pratt DR, Lohrer AM, Pilditch CA et al (2014) Changes in ecosystem function across sedimentary gradients in estuaries. Ecosystems 17:182–194. https://doi.org/10.1007/s10021-013-9716-6 CrossRefGoogle Scholar
  66. Queiroz HM, Nóbrega GN, Ferreira TO, Almeida LS, Romero TB, Santaella ST, Bernardino AF, Otero XL (2018) The Samarco mine tailing disaster: a possible time-bomb for heavy metals contamination? Sci Total Environ 637-638:498–506CrossRefPubMedGoogle Scholar
  67. Ribeiro LF, Eça GF, Barros F et al (2016) Impacts of shrimp farming cultivation cycles on macrobenthic assemblages and chemistry of sediments. Environ Pollut 211:307–315. https://doi.org/10.1016/j.envpol.2015.12.031 CrossRefPubMedGoogle Scholar
  68. Rigo D (2004) Análise do escoamento em regiões estuarinas com manguezais – Medições e modelagem na Baía de Vitória, ES. Thesis, Federal University of Rio de JaneiroGoogle Scholar
  69. RMA P, Barros F, Farias CO, Wagener AL, Hatje V et al (2017) Tropical bar as a reference área defined by multiple lines of evidence. Mar Pollut Bull 123:291–303. https://doi.org/10.1016/j.marpolbul.2017.08.041 CrossRefGoogle Scholar
  70. Rocha RM, Bonnet NY, Baptista MS et al (2012) Introduced and native Phlebobranch and Stolidobranch solitary ascidians (Tunicata: Ascidiacea) around Salvador, Bahia, Brazil. Zoologia (Curitiba) 29:39–53. https://doi.org/10.1590/S1984-46702012000100005 CrossRefGoogle Scholar
  71. Rondinelli SF, Barros F (2010) Evaluating shellfish gathering (Lucina pectinata) in a tropical mangrove system. J Sea Res 64:401–407. https://doi.org/10.1016/j.seares.2010.06.002 CrossRefGoogle Scholar
  72. Sabeel RAO, Ingels J, Pape E et al (2015) Macrofauna along the Sudanese Red Sea coast: potential effect of mangrove clearance on community and trophic structure. Mar Ecol 36:794–809. https://doi.org/10.1111/maec.12184 CrossRefGoogle Scholar
  73. Schaeffer-Novelli Y, Cintrón-Molero G, Adaime RR et al (1990) Variability of mangrove ecosystems along the Brazilian coast. Estuaries 13:204–218. https://doi.org/10.2307/1351590 CrossRefGoogle Scholar
  74. Semeniuk V (2013) Predicted response of coastal wetlands to climate changes: a western Australian model. Hydrobiologia 708:23–43. https://doi.org/10.1007/s10750-012-1159-0 CrossRefGoogle Scholar
  75. Servino RN, Gomes LEO, Bernardino AF (2018) Extreme weather impacts on mangrove forests in the eastern Brazil marine ecoregion. Sci Total Environ 628-629:233–240. https://doi.org/10.1016/j.scitotenv.2018.02.068 CrossRefPubMedGoogle Scholar
  76. Silva EC (2016). Efeito das espécies invasoras Charybdis hellerii (Crustacea; Portunidae) e Melanoides tuberculatus (Gastropoda; Thiaridae) sobre a estrutura das assembleias macrobentônicas em dois ambientes aquático, Bahia, Brasil. Thesis, Federal University of BahiaGoogle Scholar
  77. Silva EC, Barros F (2011) Macrofauna bentônica introduzida no brasil: lista de espécies marinhas e dulcícolas e distribuição atual. Oecol Aust 15:326–344. https://doi.org/10.4257/oeco.2011.1502.10 CrossRefGoogle Scholar
  78. Sjoling S, Mohammed SM, Lyimo TJ et al (2005) Benthic bacterial diversity and nutrient processes in mangroves: impact of deforestation. Estuar Coast Shelf Sci 63:397–406. https://doi.org/10.1016/j.ecss.2004.12.002 CrossRefGoogle Scholar
  79. Spalding MD, Fox HE, Allen GR et al (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583. https://doi.org/10.1641/B570707 CrossRefGoogle Scholar
  80. Sweetman AK, Middelburg JJ, Berle AM et al (2010) Impacts of exotic mangrove forests and mangrove deforestation on carbon remineralization and ecosystem functioning in marine sediments. Biogeosciences 7:2129–2145. https://doi.org/10.5194/bg-7-2129-2010 CrossRefGoogle Scholar
  81. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci U S A 105:15452–15457. https://doi.org/10.1073/pnas.0803833105 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Vinebrooke RD, Cottingham KL, Norberg J et al (2004) Implications of multiple stressors on biodiversity and ecosystem functioning. Oikos 104:451–451. https://doi.org/10.1111/j.0030-1299.2004.13255.x CrossRefGoogle Scholar
  83. Whitfield AK, Elliott M, Basset A et al (2012) Paradigms in estuarine ecology - a review of the Remane diagram with a suggested revised model for estuaries. Estuar Coast Shelf Sci 97:78–90. https://doi.org/10.1016/j.ecss.2011.11.026 CrossRefGoogle Scholar
  84. Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279e338. https://doi.org/10.2307/1943563 CrossRefGoogle Scholar
  85. Ysebaert T, Herman PMJ (2002) Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Mar Ecol Prog Ser 244:105–124. https://doi.org/10.3354/meps244105 CrossRefGoogle Scholar
  86. Ysebaert T, Herman PMJ, Meire P et al (2003) Large-scale spatial patterns in estuaries: estuarine macrobenthic communities in the Schelde estuary, NW Europe. Estuar Coast Shelf Sci 57:335–555. https://doi.org/10.1016/S0272-7714(02)00359-1 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Angelo Fraga Bernardino
    • 1
  • Alice Reis
    • 2
  • Antônio Carlos Dórea Pereira Filho
    • 2
  • Luiz Eduardo de Oliveira Gomes
    • 1
  • Lorena Bonno Bissoli
    • 1
  • Francisco Carlos Rocha de BarrosJr
    • 2
  1. 1.Grupo de Ecologia Bêntica, Departamento de Oceanografia e EcologiaCCHN, Universidade Federal do Espírito SantoEspírito SantoBrazil
  2. 2.Laboratório de Ecologia Bentônica, Programa de Pós-Graduação em Ecologia e BiomonitoramentoInstituto de Biologia, Centro Interdisciplinar de Energia e Ambiente, Universidade Federal da BahiaSalvadorBrazil

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