Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 26, pp 27112–27127 | Cite as

Natural and non-toxic products from Fabaceae Brazilian plants as a replacement for traditional antifouling biocides: an inhibition potential against initial biofouling

  • Vanessa Ochi AgostiniEmail author
  • Alexandre José Macedo
  • Erik Muxagata
  • Márcia Vanusa da Silva
  • Grasiela Lopes Leães Pinho
Research Article

Abstract

In this study, we screened for the antifouling activity of 15 species plant extracts from Brazilian the Brazilian Caatinga Fabaceae against the initial colonization of natural marine bacterial biofilm. We also investigated the potential toxicity of extracts against planktonic and benthic non-target organisms. Aqueous extracts of plants collected in the Caatinga biome (PE, Brazil) were prepared and tested at different concentration levels (0, 0.5, 1, 2, 4, and 8 mg mL−1). Natural marine bacterial consortium was inoculated in multi-well plates and incubated with the different treatments for 48 h. The biofilm and planktonic bacterial density and biomass inhibition were evaluated along with biofilm biomass eradication. The extracts that showed the highest bacterial biofilm inhibition were evaluated for toxicity against microalgae and crustaceans. The biofilm and planktonic bacterial inhibition potential were evaluated through flow cytometry and spectrophotometry. The selected treatments were evaluated for their toxicity using the microalgae Chaetoceros calcitrans, the copepod Nitokra sp., and the brine shrimp Artemia salina as bioindicators. Our work demonstrates the biotechnological potential of Fabaceae plant compounds as a safe antifouling alternative. Anadenanthera colubrina var. cebil fruits and Apuleia leiocarpa leaf extracts showed antibiofilm activity (≥ 80%), while Myroxylon peruiferum and Dioclea grandiflora leaf extracts showed antibiotic activity. These extracts were safe to planktonic and benthic non-target organisms. The results of this study point to potential substitutes to highly toxic antifouling paints and shed light on the prospect of a yet to be explored biome for more sustainable alternatives in biofouling research.

Keywords

Aquatic environment, biotechnology Biofilm Caatinga biome Pelagic-benthic coupling 

Notes

Acknowledgments

The authors acknowledge the support of Universidade Federal of Rio Grande (FURG), Universidade Federal do Rio Grande do Sul (UFRGS), Universidade Federal de Pernambuco (UFPE), Centro de Microscopia Eletrônica do Sul (CEME-SUL), and PNPD-CAPES scholarship.

Funding

This work was supported by the PRONEM FAPERGS/CNPq (16/2551-000244-4).

Compliance with ethical standards

National ethical statement

The present research is in accordance with Brazilian legislation for the use of genetic patrimony and tradition-associated knowledge, under the record numbers: SisGen A08E18B and SisGen A50301E.

Competing interests

The authors declare that they have no competing interests.

References

  1. Agostini VO, Ritter MN, Macedo AJ, Muxagata E, Erthal F (2017) What determines sclerobiont colonization on marine mollusk shells? PLoS One 12:e0184745.  https://doi.org/10.1371/journal.pone.0184745 CrossRefGoogle Scholar
  2. Agostini VO, Macedo AJ, Muxagata E (2018) O papel do biofilme bacteriano no acoplamento bentopelágico, durante o processo de bioincrustação. Revista Liberato 19(31):1–134.  https://doi.org/10.31514/rliberato.2018v19n31.p23 Google Scholar
  3. Amara I, Miled W, Slama RB, Ladhari N (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A review. Environ Toxicol Pharmacol 57:115–130.  https://doi.org/10.1016/j.etap.2017.12.001 CrossRefGoogle Scholar
  4. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LS (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:D115–D119.  https://doi.org/10.1093/nar/gkw1099 CrossRefGoogle Scholar
  5. Araújo EL, Sampaio EVSB, Rodal MJN (1995) Composição florística e fitossociologia de três áreas de caatinga de Pernambuco. Rev Bras Biol 55(4):595–607Google Scholar
  6. Armstrong E, McKenzie JD, Goldsworthy GT (1999) Aquaculture of sponges on scallops for natural products research and antifouling. J Biotechnol 70:163–174CrossRefGoogle Scholar
  7. Armstrong E, Boyd KG, Pisacane A, Peppiatt CJ, Burgess JG (2000) Marine microbial natural products in antifouling coatings. Biofouling 16(2–4):215–224.  https://doi.org/10.1080/08927010009378446 CrossRefGoogle Scholar
  8. Bakus GJ, Wright M, Khan AK, Ormsby B, Gulko DA, Licuanan W, Carriazo E, Ortiz A, Chan DB, Lorenzana D, Huxley M (1994) Experiments seeking marine natural antifouling compounds. In: Thompson M-F, Nagabhushanam R, Sarojini R, Fingerman M (eds) Recent developments in biofouling control. A A Balkema, Rotterdam, pp 373–338Google Scholar
  9. Bejgarn S, MacLeod M, Bogdal C, Breitholtz M (2015) Toxicity of leachate from weathering plastics: an exploratory screening study with Nitocra spinipes. Chemosphere 132:114–119.  https://doi.org/10.1016/j.chemosphere.2015.03.010 CrossRefGoogle Scholar
  10. Bertram V (2000) Past, present and prospects of antifouling. Proc 32nd WEGEMT School on Marine Coatings, University of Plymouth, pp 85–97Google Scholar
  11. Brandelli CLC, Ribeiro VB, Zimmer KR, Barth AL, Tasca T, Macedo AJ (2015) Medicinal plants used by a Mbyá-Guarani tribe against infections: activity on KPC-producing isolates and biofilm-forming bacteria. Nat Prod Commun 10(11): 12 p):464–468.  https://doi.org/10.3109/13880209.2014.922587 Google Scholar
  12. Bugni TS, Richards B, Bhoite L, Cimbora D, Harper MK, Ireland CM (2008) Marine natural product libraries for high-throughput screening and rapid drug discovery. J Nat Prod 71(6):1095–1098.  https://doi.org/10.1021/np800184g CrossRefGoogle Scholar
  13. Calabrese EJ (2014) Hormesis: a fundamental concept in biology. Microb Cell 1(5):145–149.  https://doi.org/10.15698/mic2014.05.145 CrossRefGoogle Scholar
  14. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  15. Cresswell T, Richards JP, Glegg GA, Readman JW (2006) The impact of legislation on the usage and environmental concentrations of Irgarol 1051 in UK coastal waters. Mar Pollut Bull 52:1169–1175.  https://doi.org/10.1016/j.marpolbul.2006.01.014 CrossRefGoogle Scholar
  16. Da Gama BAP, Carvalho AGV, Weidner K, Soares AR, Coutinho R, Fleury BG, Teixeira VL, Pereira RC (2008) Antifouling activity of natural products from Brazilian seaweeds. Bot Mar 51:191–201.  https://doi.org/10.1515/BOT.2008.027 Google Scholar
  17. Desai DV (2008) Impact of Irgarol 1051 on the larval development and metamorphosis of Balanus amphitrite Darwin, the diatom Amphora coffeaformis and natural biofilm. Biofouling 24(5):393–403.  https://doi.org/10.1080/08927010802339764 CrossRefGoogle Scholar
  18. Devi P, Solimabi W, D’Souza L, Sonak S, Kamat SY, Singbai SYS (1997) Screening of some marine plants for activity against marine fouling bacteria. Bot Mar 40:87–91Google Scholar
  19. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefGoogle Scholar
  20. Eldeen IMS, Van Heerden FR, Van Staden J (2010) In vitro biological activities of niloticane, a new bioactive cassane diterpene from the bark of Acacia nilotica subsp. Kraussiana. J Ethnopharmacol 128:555–560.  https://doi.org/10.1016/j.jep.2010.01.057 CrossRefGoogle Scholar
  21. Fantz PR (1991) Ethnobotany of Clitoria (Leguminosae). Econ Bot 45:511–520CrossRefGoogle Scholar
  22. Fernández-Alba R, Piedra L, Mezcua M, Hernando MD (2002) Toxicity of single and mixed contaminants in seawater measured with acute toxicity bioassays. Sci World J 2:1115–1120.  https://doi.org/10.1100/tsw.2002.221 CrossRefGoogle Scholar
  23. Gamarra-Rojas CFL, Sampaio EVDSB (2002) Espécies de caatinga no banco de dados do CNIP. In: Sampaio EVDSB, Giuletti AM, Virgínio J, Gamarra-Rojas CFL (eds) Vegetação e flora da caatinga. APNE-CNIP, Recife, pp 50–91Google Scholar
  24. Garaventa F, Gambardella C, Di Fino A, Pittore M, Faimali M (2010) Swimming speed alteration of Artemia sp. and Brachionus plicatilis as a sub-lethal behavioural end-point for ecotoxicological surveys. Ecotoxicology 19(3):512–519.  https://doi.org/10.1007/s10646-010-0461-8 CrossRefGoogle Scholar
  25. Gopikrishnan V, Radhakrishnan M, Pazhanimurugan R, Shanmugasundaram T, Balagurunathan R (2015) Natural products: potential and less explored source for antifouling compounds. J Chem Pharm Res 7(7):1144–1153Google Scholar
  26. Göransson U, Sjogren M, Svangard E, Claeson P, Bohlin L (2004) Reversible antifouling effect of the cyclotide cycloviolacin O2 against barnacles. J Nat Prod 67:1287–1290.  https://doi.org/10.1021/np0499719 CrossRefGoogle Scholar
  27. Gotelli NJ, Ellison AM (2013) A primer of ecological statistics, 2nd edn. Sinauer Associates, Inc. Publishers, Sunderland, p 576Google Scholar
  28. Grasland B, Mitalane J, Briandet R, Quemener E, Meylheuc T, Linossier I, Vallee-Rehel K, Haras D (2003) Bacterial biofilm in seawater: cell surface properties of early-attached marine bacteria. Biofouling 19(5):307–313.  https://doi.org/10.1080/0892701031000121041 CrossRefGoogle Scholar
  29. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239.  https://doi.org/10.1139/bcb-2014-0144 CrossRefGoogle Scholar
  30. Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000km salinity gradient of the Baltic Sea. ISME J 5:1571–1579.  https://doi.org/10.1038/ismej.2011.41 CrossRefGoogle Scholar
  31. ICRAM (2001) Metodologie analitiche di riferimento. Ministero dell’Ambiente e dela Tutela del Territorio. Servizio Difesa Mare, RomaGoogle Scholar
  32. International Organization for Standardization (ISO) (2006) Water quality and marine algal growth inhibition test with Skeletonema costatum and Phaeodactylum tricornutum, 2nd edn. ISO 10253, Geneva, p 12Google Scholar
  33. Karlsson J, Breitholtz M, Eklund B (2006) A practical ranking system to compare toxicity of anti-fouling paints. Mar Pollut Bull 52:1661–1667.  https://doi.org/10.1016/j.marpolbul.2006.06.007 CrossRefGoogle Scholar
  34. Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30:235–248.  https://doi.org/10.1016/S0160-4120(03)00176-4 CrossRefGoogle Scholar
  35. Koutsaftis A, Aoyama I (2006) The interactive effects of binary mixtures of three antifouling biocides and three heavy metals against the marine algae Chaetoceros gracilis. Environ Toxicol 21:432–439.  https://doi.org/10.1002/tox.20202 CrossRefGoogle Scholar
  36. Koutsaftis A, Aoyama I (2007) Toxicity of four antifouling biocides and their mixtures on the brine shrimp Artemia salina. Sci Total Environ 387:166–174.  https://doi.org/10.1016/j.scitotenv.2007.07.023 CrossRefGoogle Scholar
  37. Lee YK, Kwon KK, Cho KH, Kim HW, Park JH, Lee HK (2003) Culture and identification of Bacteria from marine biofilms. J Microbiol 41(3):183–188Google Scholar
  38. Lee JW, Nam JH, Kim YH, Lee KH, Lee DH (2008) Bacterial communities in the initial stage of marine biofilm formation on artificial surfaces. J Microbiol 46(2):174–182.  https://doi.org/10.1007/s12275-008-0032-3 CrossRefGoogle Scholar
  39. Lee J-H, Cho MH, Lee J (2011) 3-Indolylacetonitrile decreases Escherichia coli O157:H7 biofilm formation and Pseudomonas aeruginosa virulence. Environ Microbiol 13(1):62–73.  https://doi.org/10.1111/j.1462-2920.2010.02308.x CrossRefGoogle Scholar
  40. Libralato G, Losso C, Volpi Ghirardini A (2007) Toxicity of untreated wood leachates towards two saltwater organisms (Crassostrea gigas and Artemia franciscana). J Hazard Mater 144:590–593.  https://doi.org/10.1016/j.jhazmat.2006.10.082 CrossRefGoogle Scholar
  41. Lopes LFP, Agostini VO, Muxagata E (2018) Could some procedures commonly used in bioassays with the copepod Acartia tonsa Dana 1849 distort results? Ecotoxicol Environ Saf 150:353–365.  https://doi.org/10.1016/j.ecoenv.2017.12.004 CrossRefGoogle Scholar
  42. Malafaia CB, Jardelino ACS, Silva AGS, Souza EB, Macedo AJ, Correia MTS, Silva MV (2017) Effects of Caatinga plant extracts in planktonic growth and biofilm formation in Ralstonia solanacearum. Microb Ecol 75(3):555–561CrossRefGoogle Scholar
  43. Maréchal J-F, Hellio C (2009) Challenges for the development of new non-toxic antifouling challenges for the development of new non-toxic antifouling solutions. Int J Mol Sci 10:4623–4637.  https://doi.org/10.3390/ijms10114623 CrossRefGoogle Scholar
  44. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10CrossRefGoogle Scholar
  45. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618.  https://doi.org/10.1038/ismej.2011.139 CrossRefGoogle Scholar
  46. Muthusamy S, Lundin D, Branca RMM, Baltar F, Gonzalez JM, Lehtio J, Pinhassi J (2017) Comparative proteomics reveals signature metabolisms of exponentially growing and stationary phase marine bacteria. Environ Microbiol 19(6):2301–2319CrossRefGoogle Scholar
  47. Nandakumar K, Yano T (2003) Biofouling and its prevention: a comprehensive overview. Biocontrol Sci 8(4):133–144CrossRefGoogle Scholar
  48. Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL (2000) Fate and ecotoxicity of the new antifouling compound Irgarol 1051 in the aquatic environment. Water Res 34:3523–3530.  https://doi.org/10.1016/S0043-1354(00)00095-6 CrossRefGoogle Scholar
  49. Oliveira SS, Wasielesky Junior WFB, Ballester ELC, Abreu PCOV (2006) Caracterização da assembléia de bactérias nitrificantes pelo método “Fluorescent in situ Hybridization” (FISH) no biofilme e água de larvicultura do Camarão-rosa Farfantepenaeus paulensis. Atlântica 28(1):33–45Google Scholar
  50. Omae I (2003) General aspects of tin free antifouling paints. Chem Rev 103:3431–3488.  https://doi.org/10.1021/cr030669z CrossRefGoogle Scholar
  51. Ozkan A, Berberoglu H (2013) Adhesion of algal cells to surfaces. Biofouling 29(4):469–482.  https://doi.org/10.1080/08927014.2013.782397 CrossRefGoogle Scholar
  52. Poth AG, Colgrave ML, Philip R, Kerenga B, Daly NL, Anderson MA, Craik DJ (2011) Discovery of cyclotides in the Fabaceae plant family provides new insights into the cyclization, evolution, and distribution of circular proteins. ACS Chem Biol 6:345–355.  https://doi.org/10.1021/cb100388j CrossRefGoogle Scholar
  53. Price RR, Patchan M, Clare A, Rittschof D, Bonaventura J (1994) Performance enhancement of natural antifouling compounds and their analogs through microencapsulation and controlled release. In: Thompson M-F, Nagabhushanam R, Sarojini R, Fingerman M (eds) Recent developments in biofouling control. A A Balkema, Rotterdam, pp 321–334Google Scholar
  54. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P (1999) Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181:5993–6002Google Scholar
  55. Qi SH, Xu Y, Xiong HR, Qian PY, Zhang S (2009) Antifouling and antibacterial compounds from a marine fungus Cladosporium sp. F14. World J Microbiol Biotechnol 25:399–406.  https://doi.org/10.1007/s11274-008-9904-2 CrossRefGoogle Scholar
  56. Queiroz LP (2006) The Brazilian Caatinga: phytogeographical pattern inferred from distribution data of the Leguminosae. In: Pennington RT, Lewis GP, Ratter JA (eds) Neotropical savannas and dry forests: plant diversity, biogeography, and conservation. Taylor & Francis CRC Press, Oxford, pp 113–149.  https://doi.org/10.1201/9781420004496.ch6 Google Scholar
  57. R Core Team: R [Internet]. Auckland: a language and environment for statistical computing; [accessed 2018]. Available from: https://www.R-project.org/
  58. Ralston E, Swain G (2009) Bioinspiration—the solution for biofouling control? Bioinsp Biomim 4:1–9.  https://doi.org/10.1088/1748-3182/4/1/015007 CrossRefGoogle Scholar
  59. Rodrigue JP (2006a) Transportation and the geographical and functional integration of global production networks. Growth Chang 37:510–525.  https://doi.org/10.1111/j.1468-2257.2006.00338.x CrossRefGoogle Scholar
  60. Rodrigue JP (2006b) Challenge the derived transport-demand thesis: geographical issues in freight distribution. Environ Plann A 38:1419–1462CrossRefGoogle Scholar
  61. Sanchez-Fortún S, Sanz F, Barahona MV (1996) Acute toxicity of several organophosphorous insecticides and protection by cholinergic antagonists and 2-PAM on Artemia salina larvae. Arch Environ Contamin Toxicol 31:391–398.  https://doi.org/10.1007/BF01700957 CrossRefGoogle Scholar
  62. Sanchez-Fortún S, Sanz F, Santa-Maria A, Ros JM, De Vicente ML, Encinas MT, Vinagre E, Barahona MV (1997) Acute sensitivity of three age classes of Artemia salina larvae to seven chlorinated solvents. Bull Environ Contamin Toxicol 59:445–451.  https://doi.org/10.1007/s10661-005-6029-z CrossRefGoogle Scholar
  63. Satheesh S, Ba-akdah MA, Al-Sofyani AA (2016) Natural antifouling compound production by microbes associated with marine macroorganisms. Electron J Biotechnol 21:26–35.  https://doi.org/10.1016/j.ejbt.2016.02.002 CrossRefGoogle Scholar
  64. Sbrilli G, Limberti A, Caldini G, Corsini A (1998) Metodologia di saggioalgale per il controllo dei corpi idrici e delle acque di scarico. ARPATFirenze, pp 1–191Google Scholar
  65. Schultz MP (2007) Effects of coating roughness and biofouling on ship resistance and powering. Biofouling 23:331–341CrossRefGoogle Scholar
  66. Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27(1):87–98.  https://doi.org/10.1080/08927014.2010.542809 CrossRefGoogle Scholar
  67. Silva LN, Trentin DS, Zimmer KR, Treter J, Brandelli CLC, Frasson AP, Tasca T, Silva AG, Silva MV, Macedo AJ (2015) Anti-infective effects of Brazilian Caatinga plants against pathogenic bacterial biofilm formation. Pharm Biol 53(3):464–468.  https://doi.org/10.3109/13880209.2014.922587 CrossRefGoogle Scholar
  68. Silva LN, Zimmer KR, Macedo AJ, Trentin DS (2016) Plant natural products targeting bacterial virulence factors. Chem Rev 116:9162–9236.  https://doi.org/10.1021/acs.chemrev.6b00184 CrossRefGoogle Scholar
  69. SIS (1991) Determination of acute lethal toxicity of chemical substances and effluents to Nitocra spinipes Boeck — static procedure (in Swedish.). Standardiserings kommissionen i Sverige (SIS), Stockholm, SwedenGoogle Scholar
  70. Soroldoni S, Abreu F, Castro ÍB, Duarte FA, Pinho GL (2017) Are antifouling paint particles a continuous source of toxic chemicals to the marine environment? J Hazard Mater 15(330):76–82.  https://doi.org/10.1016/j.jhazmat.2017.02.001 CrossRefGoogle Scholar
  71. Srinivasan M, Swain GW (2007) Managing the use of copper-based antifouling paints. Environ Manag 39:423–441.  https://doi.org/10.1007/s00267-005-0030-8 CrossRefGoogle Scholar
  72. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  73. Teixeira VL (2010) Caracterização do Estado da Arte em Biotecnologia Marinha no Brasil. Ministério da Saúde, Organização Pan-Americana da Saúde, Ministério da Ciência e Tecnologia. – Brasília: Ministério da Saúde, (Série B. Textos Básicos de Saúde), p 134Google Scholar
  74. Telegdi J, Trif L, Románszki L (2016) Smart anti-biofouling composite coatings for naval applications. Transport, structural, environmental and energy applications. Woodhead Publishing Series in Composites Science and Engineering. pp. 123–155. doi:  https://doi.org/10.1016/B978-1-78242-283-9.00005-1
  75. Trentin DS, Giordani RB, Zimmer KR, Silva AG, Silva MV, Correia MTS, Baumvol IJR, Macedo AJ (2011) Potential of medicinal plants from the Brazilian semi-arid region (Caatinga) against Staphylococcus epidermidis planktonic and biofilm lifestyles. J Ethnopharmacol 137:327–335.  https://doi.org/10.1016/j.jep.2011.05.030 CrossRefGoogle Scholar
  76. Trentin DS, Zimmer KR, Silva MV, Giordani RB, Macedo AJ (2014) Medicinal plants from brazilian caatinga: antibiofilm and antibacterial activities against Pseudomonas aeruginosa. Revista Caatinga, Mossoró 27(3):264–271Google Scholar
  77. Trovão DMBM, Fernandes PD, Andrade LA, Dantas Neto J (2007) Seazonal variations of physiological aspects of Caatinga species. Rev Bras Eng Agríc Ambient 11:307–311CrossRefGoogle Scholar
  78. Videla HA (2002) Prevention and control of biocorrosion. International Biodeterioration and Biodegradation, Barking 49:259–270CrossRefGoogle Scholar
  79. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  80. Wang K-L, Wu Z-H, Wang Y, Wang C-Y, Xu Y (2017) Mini-review: antifouling natural products from marine microorganisms and their synthetic analogs. Mar Drugs 15:266.  https://doi.org/10.3390/md15090266 CrossRefGoogle Scholar
  81. Warnken J, Dunn RJK, Teasdale PR (2004) Investigation of recreational boats as a source of copper at anchorage sites using time-integrated diffusive gradients in thin film and sediment measurements. Mar Pollut Bull 49:833–843.  https://doi.org/10.1016/j.marpolbul.2004.06.012 CrossRefGoogle Scholar
  82. WHOI (Woods Hole Oceanographic Institution) (1952) Marine fouling and its prevention. US Naval Institute, Annapolis, Maryland. http://hdl.handle.net/1912/191
  83. Yang J-L, Shen P-J, Liang X, Li Y-F, Bao W-Y, Li J-L (2013) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 29(3):247–259.  https://doi.org/10.1080/08927014.2013.764412 CrossRefGoogle Scholar
  84. Yerly J, Hu Y, Martinuzzi RJ (2008) Biofilm structure differentiation based on multi-resolution analysis. Biofouling 24(5):323–337.  https://doi.org/10.1080/08927010802209892 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Microcontaminantes Orgânicos e Ecotoxicologia Aquática - Instituto de Oceanografia da Universidade Federal do Rio Grande (FURG)Rio GrandeBrazil
  2. 2.Programa de Pós-graduação em Oceanologia (PPGO)Programa Nacional de Pós-Doutorado da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (PNPD-CAPES)Rio GrandeBrazil
  3. 3.Laboratório de Biofilmes e Diversidade Microbiana - Faculdade de Farmácia e Centro de Biotecnologia da Universidade Federal do Rio Grande do Sul (UFRGS)Porto AlegreBrazil
  4. 4.Laboratório de Zooplâncton - Instituto de Oceanografia da Universidade Federal do Rio Grande (FURG)Rio GrandeBrazil
  5. 5.Laboratório de Produtos Naturais - Departamento de Bioquímica da Universidade Federal de Pernambuco (UFPE)RecifeBrazil

Personalised recommendations