Is the distribution of the lancelet Branchiostoma caribaeum affected by sewage discharges? An analysis at multiple scales of variability

Marine Pollution Bulletin

Volumn 69, Issue 1-2, 2013, Pages 178-188

  Barboza, Carlos Alberto de Moura ^a,b   Hadlich, Heliatrice Louise ^a   Sandrini Neto, Leonardo ^a   Martins, César de Castro ^a   Lana, Paulo da Cunha ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Branchiostoma caribaeum; Fecal steroids; Lancelet; Paranagu Bay; Sewage contamination; Spatial scales

Indexed keywords

BRANCHIOSTOMA; FECAL STEROIDS; LANCELET; SEWAGE CONTAMINATION; SPATIAL SCALE;

CONTAMINATION;

LIPIDS;

STEROID;

BENTHOS; BIOINDICATOR; BIOMASS; CONCENTRATION (COMPOSITION); DISCHARGE; ESTUARY; FISH; GRADIENT ANALYSIS; POLLUTION EFFECT; SEWAGE; SPATIAL DISTRIBUTION; SPATIAL VARIATION; STEROID;

ARTICLE; BIOMASS; BRANCHIOSTOMA CARIBAEUM; BRAZIL; CEPHALOCHORDATA; ESTUARY; GEOGRAPHIC DISTRIBUTION; NONHUMAN; POLLUTION MONITORING; POPULATION DENSITY; SEA POLLUTION; SEDIMENT; SEWAGE; SPECIES DISTRIBUTION;

ANIMALS; BIOMASS; BRAZIL; CHORDATA, NONVERTEBRATE; ENVIRONMENTAL MONITORING; SEASONS; SEWAGE; WATER POLLUTANTS; WATER POLLUTION;

BRAZIL; PARANA [BRAZIL]; PARANAGUA BAY;

BRANCHIOSTOMA CARIBAEUM; INVERTEBRATA;

EID: 84876105207     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2013.01.040     Document Type: Article

References (100)

1. Antoniadou C., Krestenitis Y., Chintiroglou C. Structure of the "lancelets sand" community in Thermaikos Bay (East Mediterranean). Fresenius Environ. Bull. 2004, 13(11):1122-1128.
2. Borja A., Franco J., Pérez V. A marine biotic index to establish the ecological quality of soft bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 2000, 40:1100-1114.
3. Borja A., Dauer D.M. Assessing the environmental quality status in estuarine and coastal systems: comparing methodologies and indices. Ecol. Ind. 2008, 8:331-337.
4. Camargo M.G. SysGran: um sistema de código aberto para análises granulométricas do sedimento. Rev. Bras. Geol. 2006, 36:345-352.
5. Carreira R.S., Wagener A.L.R., Readman J.W. Sterols as markers of sewage contamination in a tropical urban estuary (Guanabara Bay, Brazil): space-time variations. Estuar. Coast. Shelf Sci. 2004, 60:587-598.
6. Carvalho S., Pereira P., Pereira F., Pablo H., Vale C., Gaspar M.B. Factors structuring temporal and spatial dynamics of macrobenthic communities in a eutrophic coastal lagoon (óbidos lagoon, Portugal). Mar. Environ. Res. 2011, 71:97-110.
7. Chapman M.G., Tolhurst T., Murphy R., Underwood A.J. Complex and inconsistent patterns of variation in benthos, micro-algae and sediment over multiple spatial scales. Mar. Ecol. Prog. Ser. 2010, 398:33-47.
8. Choi M., Moon H.Y., Yu J., Kim S.S., Pait A.S., Choi H.G. Nationwide monitoring of nonylphenolic compounds and coprostanol in sediments from Korean coastal waters. Mar. Pollut. Bull. 2009, 58:1078-1095.
9. Chen Y., Cheung S.G., Shin P.K.S. The diet of lancelets in subtropical Hong Kong as indicated by fatty acid and stable isotopic analyses. J. Mar. Biol. Assoc. UK 2008, 88:1487-1491.
10. Choueri R.B., Cesar A., Torres R.J., Abessa D.M.S., Morais R.D., Pereira C.D.S., Nascimento M.R.L., Mozeto A.A., Riba I., DelValls T.A. Integrated sediment quality assessment in Paranaguá Estuarine System, Southern Brazil. Ecotoxicol. Environ. Saf. 2009, 72:1824-1831.
11. Choueri R.B., Cesar A., Abessa D.M.S., Torres R.J., Riba I., Pereira C.D.S., Nascimento M.R.L., Morais R.D., Mozeto A.A., DelValls T.A. Harmonised framework for ecological risk assessment of sediments from ports and estuarine zones of North and South Atlantic. Ecotoxicology 2010, 19:678-696.
12. Clarke K.R., Ainsworth M.A. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 1993, 92:205-219.
13. Cloern J.E. Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 2001, 210:223-253.
14. Combi T., Taniguchi S., Ferreira P.A.L., Mansur A.V., Figueira R.C.L., Mahiques M.M., Montone R.C., Martins C.C. Sources and temporal patterns of polychlorinated biphenyls around a large South American grain shipping port (Paranaguá Estuarine System, Brazil). Arch. Environ. Contam. Toxicol 2013, 10.1007/s00244-012-9872-2.
15. Cory R.L., Pierce L. Distribution and ecology in lancelets over the continental shelf of the southeastern United States. Limnol. Oceanogr. 1967, 12(4):650-656.
16. Costa O.S., Leão Z.M.A.N., Nimmo M., Attrill M. Nutrification impacts on coral reefs from northern Bahia, Brazil. Hydrobiologia 2000, 440:307-315.
17. Costa O.S., Nimmo M., Atrill M.J. Coastal nutrification in Brazil: a review of the role of nutrient excess on coral reef demise. J. South Am. Earth Sci. 2008, 25:257-270.
18. Dauvin J.-C. Paradox of estuarine quality: benthic indicators and indices, consensus or debate for the future. Mar. Pollut. Bull. 2007, 55:271-281.
19. Dauvin J.-C., Ruellet T. The estuarine quality paradox: is it possible to define an ecological quality status for specific modified and naturally stressed estuarine ecosystems?. Mar. Pollut. Bull. 2009, 59:38-47.
20. Dolbeth M., Cardoso P.G., Ferreira S.M., Verdelhos T., Raffaelli D., Pardal M.A. Anthropogenic and natural disturbance effects on a macrobenthic estuarine community over a 10-year period. Mar. Pollut. Bull. 2007, 54:585-676.
21. Egres A.G., Martins C.C., Oliveira V.M., Lana P.C. Effects of an experimental in situ diesel oil spill on the benthic community of unvegetated tidal flats in a subtropical estuary (Paranaguá Bay, Brazil). Mar. Pollut. Bull. 2012, 64:2681-2691.
22. Elliot Q., Quintino V. The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar. Pollut. Bull. 2007, 54:640-645.
23. Fernandes M.B., Sicre M.-A., Cardoso J.N., Macedo S.J. Sedimentary 4-desmethyl sterols and n-alkanols in an eutrophic urban estuary. Capibaribe River Brazil. Sci. Total Environ. 1999, 231:1-16.
24. Fletcher D.J., Underwood A.J. How to cope with negative estimates of components of variance in ecological field studies. J. Exp. Mar. Biol. Ecol. 2002, 273:89-95.
25. Folk R.L., Ward W.C. Brazos river bar: a study in the significance of grain size parameters. J. Sediment. Petrol. 1957, 27:3-26.
26. Fortin, M.-J., Dale, M., 2005. Spatial Analysis. A Guide for Ecologists. Cambridge University Press, New York.
27. Froehner S., Maceno M., Da Luz E.C., Souza D.B., Machado K.S. Distribution of polycyclic aromatic hydrocarbons in marine sediments and their potential toxic effects. Environ. Monit. Assess. 2010, 168:205-213.
28. Gamito S., Furtado R. Feeding diversity in macroinvertebrate communities: a contribution to estimate the ecological status in shallow waters. Ecol. Ind. 2009, 9:1009-1019.
29. Gaspar M.B., Carvalho S., Constantino R., Tata-Regala J., Cúrdia J., Monteiro C.C. Can we infer dredge fishing effort from macrobenthic community structure?. J. Mar. Sci. 2009, 66:2121-2132.
30. Gonzalez-Oreja J.A., Saiz-Salinas J.I. Short-term spatio-temporal changes in urban pollution by means of faecal sterols analysis. Mar. Pollut. Bull. 1998, 36:868-875.
31. Graham M.H., Edwards M.S. Statistical significance versus fit: estimating the importance of individual factors in ecological analysis of variance. Oikos 2001, 93:505-513.
32. Grasshoff K., Ehrhardt M., Kremling K. Methods of Seawater Analysis 1983, VerlagChemie, Weinheim. second ed.
33. Gray J.S. Pollution-induced changes in populations. Phil. Trans. R. Soc (B) 1979, 286:545-561.
34. Hatje V., Barros F., Figueiredo D.G., Santos V.L.C.S., Peso-Aguiar M.C. Trace metal contamination and benthic assemblages in Subaé estuarine system. Brazil. Mar. Pollut. Bull. 2006, 52:969-987.
35. Hudson E.D., Parrish C.C., Helleur R.J. Biogeochimistry of sterols in plankton, settling particles and recent sediments in cold ocean ecosystem (Tinity Bay, Newfound-land). Mar. Chem. 2001, 76:253-270.
36. IBGE, 2007. Instituto Brasileiro de Geografia e Estatística. Available at (accessed on 01.11). http://www.ibge.gov.br/home/.
37. Jeng W.L., Han B.C. Sedimentary coprostanol in Kaoshiung Harbour and the Tan-Shui Estuary. Taiwan. Mar. Poll. Bull. 1994, 28:494-499.
38. Kawakami S.K., Montone R.C. An efficient ethanol-based analytical protocol to quantify fecal steroids in marine sediments. J. Braz. Chem. Soc. 2002, 13:226-232.
39. Kolm H.E., Schoenenberger M.F., Piemonte M.D., Souza P.S.D., Scuhli G.S.E., Mucciatto M.B., Mazzuco R. Spatial variation of bacteria in surface waters of Paranaguá and Antonina Bays, Parana. Brazil. Braz. Arch. Biol. Technol. 2002, 45:27-34.
40. Kolm H.E., Santos P.R.N.M., Sauutter K.D. Bacteria in water and sediments of Guaratuba Bay, Paraná. Brazil. Trop. Oceanogr. 2007, 35:51-69.
41. Konsulova Ts. Seasonal structure and ecological status of Varna Bay (Black Sea) sandy and muddy macrozoobenthiccoenoses. Rapp. Comm. Int. Mer Medit. 1992, 33:42.
42. Lampadariou N., Karakassis I., Pearson T.H. Cost/benefit analysis of a benthic monitoring programme of organic benthic enrichment using different sampling and analysis methods. Mar. Poll. Bull. 2005, 90:1606-1618.
43. Lana P.C., Marone E., Lopes R.M., Machado E.C. The subtropical estuarine complex of paranaguá bay. Brazil. Ecol. Study 2001, 144:132-145.
44. Legendre P., Legendre L. Numerical Ecology: Developments in Environmental Modelling 1998, Elsevier Science, Amsterdam. second ed.
45. Levin S.A. The problem of pattern and scale in ecology. Ecology 1992, 73(6):1943-1967.
46. Loh A.N., Canuel E.A., Bauer J.E. Potential source and diagenetic signatures of oceanic solved and particulate organic matter as distinguished by lipid biomarker distributions. Mar. Chem. 2008, 112:189-202.
47. Lorenzen C.J. Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnol. Oceanogr. 1967, 12:343-346.
48. Maldonado, C., Venkatesan, M.I., Phillips, C.R., Bayona, J.M., 2000. Distribution of trialkylamines and coprostanol in San Pedro shelf sediments adjacent to a sewage outfall. Mar. Pollut. Bull. 40, 680-687.
49. Marone E., Machado E.C., Lopes R.M., Silva E.T. Land-ocean fluxes in the paranaguá bay southern brazil. Braz. J. Oceanogr. 2005, 53:169-181.
50. Martins C.C., Ferreira J.A., Taniguchi S., Mahiques M.M., Bícego M.C., Montone R.C. Spatial distribution of sedimentary linear alkylbenzenes and faecal steroids of Santos Bay and adjoining continental shelf, SW Atlantic, Brazil: origin and fate of sewage contamination in the shallow coastal environment. Mar. Pollut. Bull. 2008, 56:1353-1376.
51. Martins C.C., Gomes F.B.A., Ferreira J.A., Montone R.C. Organic markers of sewage contamination in surface sediments from Santos Bay, São Paulo. Quim. Nova 2008, 31:1008-1014.
52. Martins C.C., Braun J.A.F., Seyffert B.H., Machado E.C., Filmann G. Anthropogenic organic matter inputs indicated by sedimentary fecal steroids in a large South American tropical estuary (Paranaguá estuarine system, Brazil). Mar. Pollut. Bull. 2010, 60:2137-2143.
53. Martins C.C., Seyffert B.H., Braun J.A.F., Fillmann G. Input of organic matter in a large South American tropical estuary (Paranaguá Estuarine System, Brazil) indicated by sedimentary sterols and multivariate statistical approach. J. Braz. Chem. Soc. 2011, 22:1585-1594.
54. Martins C.C., Bícego M.C., Figueira R.C.L., Angelli J.F.L., Combi T., Gallice W.C., Mansur A.V., Rocha M.L., Wisnieski E., Ceschim L.M.M., Ribeiro A.P. Multi-molecular markers and metals as tracers of organic matter inputs and contamination status from an Environmental Protection Area in the SW Atlantic (Laranjeiras Bay, Brazil). Sci. Total Environ. 2012, 417-418:158-168.
55. Montone R.C., Martins C.C., Bícego M.C., Taniguchi S., Silva D.A.M., Campos L.S., Weber R.R. Distribution of sewage input in marine sediments around a maritime Antarctic research station indicated by molecular geochemical indicators. Sci. Total Environ. 2010, 408:4665-4671.
56. Morrisey D.J., Howitt I., Underwood A.J., Stark J.S. Spatial variation in soft-sediment benthos. Mar. Ecol. Prog. Ser. 1992, 81:197-204.
57. Moure J.S., Björnberg T.K.S., Loureiro T.S. Protochordata ocorrentes na entrada da Baía de Paranaguá. Dusenia 1954, 5:233-242.
58. Mudge S.M., Lintern D.G. Comparison of sterol biomarkers for sewage with other measures in Victoria Harbor, B.C, Canada. Estuar. Coast. Shelf Sci. 1999, 48:27-38.
59. Mudge S.M., Seguel C.G. Organic contamination of San Vicente Bay. Chile. Mar. Pollut. Bull. 1999, 38:1011-1021.
60. Mudge S.M., Duce C.E. Identifying the source, transport path and sinks of sewage derived organic matter. Environ. Pollut. 2005, 136:209-220.
61. Muniz P., Venturini N., Pires-Vanin A.M.S., Tommasi L.R., Borja A. Testing the applicability of a Marine Biotic Index (AMBI) to assessing the ecological quality of soft-bottom benthic communities, in the South America Atlantic region. Mar. Pollut. Bull. 2005, 50:624-663.
62. Muniz, P., Pires-Vanin, A.M.S., 2005. More about taxonomic sufficiency: a case study using polychaete communities in a subtropical bay moderately affected by urban sewage. Ocean Sci. J., Korea 40 (3), 127-143.
63. Nohara M., Nishida M., Manthacitra V., Nishikawa T. Ancient phylogenetic separation between Pacific and Atlantic cephalochordates as revealed by mitochondrial genome analysis. Zool. Sci. 2004, 21:203-210.
64. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2012. Vegan: Community Ecology Package. R Package version 2.0-3.
65. Oulion S., Bertrand S., Belgacem M.R., Le Petillon Y., Escriva H. Sequencing and analysis of the mediterranean amphioxus (Branchiostoma lanceolatum) transcriptome. PLoS ONE 2012, 7(5):e36554.
66. Paerl H.W. Assessing and managing nutrient-enhanced eutrophication in estuarine and coastal waters: interactive effects of human and climatic perturbations. Ecol. Eng. 2006, 26:40-54.
67. Pagliosa P.R., Barbosa F.A.R. Assessing the environment-benthic fauna coupling in protected and urban areas of southern Brazil. Biol. Conserv. 2006, 129:408-417.
68. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., 2009. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-96. Avaible at. http://www.R-project.
69. Poss S., Boschung H.T. Lancelets (Cephalocordata: Branchiostomatidae): how many species are valid. Isr. J. Zool. 1996, 42:13-60.
70. R Development Core Team, 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
71. Rabalais N.N., Turner R.E., Díaz R.J., Justić D. Global change and eutrophication of coastal waters. J. Mar. Sci. 2009, 66:1528-1537.
72. Readman J.W., Fillmann G., Tolosa I., Bartocci J., Mee L.D. The use of steroid markers to assess sewage contamination of the Black Sea. Mar. Pollut. Bull. 2005, 50:310-318.
73. Riisgrad H.U., Svane I. Filter feeding in lancelets (lancelets), Branchiostoma lancelotum. Invertebr. Biol. 1999, 118(4):423-432.
74. Rota E., Perra G., Focardi S. The European lancelet Branchiostoma lanceolatum (Pallas) as an indicator of environmental quality of Tuscan Archipelago (Western Mediterranean Sea). Chem. Ecol. 2009, 25:61-69.
75. Rosenberg R., Magnusson M., Nilsson H.C. Temporal and spatial changes in marine benthic habitats in relation to the EU Water Framework Directive: the use of sediment profile imagery. Mar. Pollut. Bull. 2009, 58:565-572.
76. Ruppert E.E., Nash T.R., Smith A.J. The size range of suspended particles trapped and ingested by the filter-feeding lancelet Branchiostima floridae (Cephalocordata: Acrania). J. Mar. Biol. Assoc. UK 2000, 80:329-332.
77. Sá F., Machado E.C., Aangulo R.J., Veiga F.A., Brandini N. Arsenic and heavy metals in Sediments near Paranaguá Port, Southern Brazil. J. Coast. Res. Spec. Issue 2006, 39:1066-1068.
78. Sandrini-Neto, L., Camargo, M. G., 2011. GAD: analysis of variance from general principles. R package version 1.1.1. Avaible at. http://www.R-project.
79. Sarkar, D., 2009. lattice: Lattice Graphics. R package version 0.18-8. Available at http://www.R-project.
80. Sawaya P., Paiva Carvalho J. On the Branchiostoma of the coast of São Paulo. Bolm. Fac. Fil. Ciênc. Univ. S Paulo, Zool. 1950, 15:235-237.
81. Silva L.F.B., Tavares M., Soares-Gomes A. Population structure of the lancelet Branchiostoma caribaeum (Cephalochordata: Branchiostomidae) in the Baía de Guanabara, Rio de Janeiro. Southeastern Brazil. Rev. Bras. Zoo. 2008, 25:617-623.
82. Simboura N., Zenetos A. Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new Biotic Index. Mediterr. Mar. Sci. 2002, 3:77-111.
83. Stokes M.D. Larval settlement, post-settlement growth and secondary production of the Florida lancelet (=amphioxus) Branchiostoma floridae. Mar. Ecol. Prog. Ser. 1996, 130:71-84.
84. Strickland J.L.H., Parsons T.R. A practical handbook of seawater analysis. Bull. Fish. Res. Board Canada 1972, 167:267-278.
85. Suguio K. Introdução à Sedimentologia 1973, Edgard BlucherLtda, São Paulo.
86. Tommasi L.R., Valente M.T.M., Acedo R. Cephalochordata da região de Ilha Grande (RJ). Bolm Inst. Oceanogr. S Paulo 1972, 21:149-162.
87. Thrush S.F., Hewitt J.E., Herman P.M.J., Ysebaert T. Multi-scale analysis of species-environment relationships. Mar. Ecol. Prog. Ser. 2005, 302:13-26.
88. Underwood A.J. Experiments in ecology: their logical design and interpretation using analysis of variance 1997, Cambridge University Press, Cambridge.
89. Valença A.P., Santos P.J. Macrobenthic community for assessment of estuarine health in tropical areas (Northeast, Brazil): review of macrofauna classification in ecological groups and application of AZTI Marine Biotic Index. Mar. Pollut. Bull. 2012, 64(9):1809-1820.
90. Veloso V.G., Neves G., Capper L.A. Sensitivity of a cirolanid isopod to human pressure. Ecol. Ind. 2010, 11(3):782-788.
91. Venturini N., Tommasi L.R. Polycyclic aromatic hydrocarbons and changes in the trophic structure of polychaete assemblages in sediments of Todosos Santos Bay, Northeastern. Brazil. Mar. Pollut. Bull. 2004, 48:97-107.
92. Venturini N., Muniz P., Bícego M.C., Martins C.C., Tommasi L.R. Petroleum contamination impact on macrobenthic communities under the influence of an oil refinery: integrating chemical and biological multivariate data. Estuar. Coast. Shelf Sci. 2008, 78:457-467.
93. Vivan J.M., Di Domenico M., Almeida T.C.M. Effects of dredged material disposal on benthic macrofauna near ItajaíHarbour (Santa Catarina, South Brazil). Ecol. Eng. 2009, 35:1435-1443.
94. Volkman J.K., Barret S.M., Blackburn S.I., Mansour M.P., Sikes E.L., Gelin F. Microalgal biomarkers: a review of recent research developments. Org. Geocem. 1998, 29:1163-1179.
95. Volkman J.K. Sterols and other triterpenoids: source specificity and evolution of biosynthetic pathways. Org. Geochem. 2005, 36:139-159.
96. Wakeham, S.G., Canuel, E.A., 2006. Degradation and preservation of organic matter in sediments. In: Volkman, J.K. (Ed), Handbook of environmental chemistry, vol. 2: reactions and processes 2 (N). Springer, Berlin, pp. 295-321.
97. Warwick R.M. A new method for detecting pollution effects on marine macrobenthic communities. Mar. Biol. 1986, 92:557-562.
98. Weisberg, S.B., Ranasinghe, J.A., Dauer, J.A., Schaffner, L.C., Diaz, R.J., Frithsen, J.B., 1997. An estuarine benthic index of bioticintegrity (B-IBI) for Chesapeake Bay. Estuaries 20(l), 149-158.
99. Writer J.H., Leenheer J.A., Barber L.B., Amy G.L., Chapra S.C. Sewage contamination in the upper Mississippi River as measured by the faecal sterol, coprostanol. Water Res. 1995, 29:1427-1436.
100. Ysebaert T., Herman P.M.J. Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Mar. Ecol. Prog. Ser. 2002, 244:105-124.