Skip to main content

Macroalgal responses to coastal urbanization: relative abundance of indicator species

Abstract

This study aimed to evaluate and compare the intertidal macroalgae community from reef structures subject to different urbanization degrees. Samplings were made in 11 beaches from the Pernambuco coast, northeastern Brazil. The sites were classified according to the level of urbanization into three classes of increasing urbanization pressure: non urbanized (NU), in urbanization process (UP), and consolidated urbanization (UC). Macroalgae were identified in situ non-destructively. A total of 53 taxa were identified, 41 of these were macroalgae. Significant differences were observed in the composition of macroalgae according to the urbanization levels, with Palisada perforata, Gelidiella acerosa, and Caulerpa spp. dominating NU and UP sites, whereas Chondracanthus acicularis, Bryopsis sp., and Ulva spp. dominated UC sites. This work shows that urbanization can have a strong effect on the structure of rocky intertidal macroalgal assemblages and highlights some macroalgae species that can be used as bioindicators for assessing the impact of urbanization on coastal shores.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Airoldi L (2003) The effects of sedimentation on rocky coast assemblages. Oceanogr Mar Biol 41:161–236

    Google Scholar 

  2. Airoldi L, Beck WM (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405

    Google Scholar 

  3. Ambrose RF (2002) Transects, quadrats, and other sampling units. In: Murray SN, Ambrose RF, Dethier MN (eds) Methods for performing monitoring, impact, and ecological studies on rocky shores. Coastal Research Center, Marine Science Institute, University of California, Santa Barbara, pp 98–122

    Google Scholar 

  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for Primer. Primer-E, Plymouth

    Google Scholar 

  5. Areces A (2001) La ficoflora intermareal como bioindicadora de calidad ambiental. Estudio de caso: El litoral habanero. In: Alveal K, Antezana T (eds) Sustentabilidad de la biodiversidade. Um problema actual, bases científico-técnicas, teorizaciones y perspectivas. Trama Impresores S.A, Concepción, pp 569–589

    Google Scholar 

  6. Balata D, Piazzi L, Rindi F (2011) Testing a new classification of morphological functional groups of marine macroalgae for the detection of responses to stress. Mar Biol 158:2459–2469

    Article  Google Scholar 

  7. Benedetti-Cecchi L (2001) Variability in abundance of algae and invertebrates at different spatial scales on rocky sea shores. Mar Ecol Prog Ser 215:79–92

    Article  Google Scholar 

  8. Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser 214:137–150

    Article  Google Scholar 

  9. Borowitzka MA (1972) Intertidal algal species diversity and the effects of pollution. Aust J Mar Freshwat Res 25:73–84

    Article  Google Scholar 

  10. Branner JC (1904) The stone reefs of Brazil, their geological and geographical relations, with a chapter on the coral reefs, vol 54. Bulletin of the Museum of Comparative Zoology, Cambridge, pp 1–285

    Google Scholar 

  11. Cabrera R, Moreira A, Primelles J, Suárez AM (2005) Variación de la biomasa de Chondrophycus papillosus (C. Agardh) Garbary et Harper (Ceramiales: Rhodophyta) y su epifitismo en la bahía de Nuevitas. Cuba Rev Invest Mar 26:15–20

    Google Scholar 

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

    Google Scholar 

  13. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial (Plymouth routines in multivariate ecological research). Primer-E Ltd, Plymouth

    Google Scholar 

  14. Clarke KR, Warwick RM (2005) Primer-6 computer program. Natural Environment Research Council, Plymouth

    Google Scholar 

  15. Coelho SM, Rijstenbil JW, Brown MT (2000) Impacts of anthropogenic stresses on the early development stages of seaweed. J Aquat Ecosyst Stress Recov 7:317–333

    Article  CAS  Google Scholar 

  16. Connell SD, Russell BD, Turner DJ, Shepherd SA, Kildea T, Miller D, Airoldi L, Cheshire A (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol Prog Ser 360:63–72

    Article  Google Scholar 

  17. CPRH (2003) Agência estadual de meio ambiente e recursos hídricos. Diagnóstico Sócioambiental do Litoral Sul de Pernambuco Avaiable at: http://wwwcprhpegovbr. Acessed 26 June 2015

  18. Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Article  Google Scholar 

  19. Dominguez JML, Bittencourt ACSP, Leão ZMAN, Azevedo AEG (1990) Geologia do quaternário costeiro do Estado de Pernambuco. Rev Bras Geociênc 20:208–215

    Article  Google Scholar 

  20. Fonseca AC, Villaça R, Knoppers B (2012) Reef flat community structure of Atol das Rocas, Northeast Brazil and Southwest Atlantic. J Mar Biol 2012:1–10

    Article  Google Scholar 

  21. Goatley CH, Bellwood DR (2013) Ecological consequences of sediment on high-energy coral reefs. PLoS One 8(10):e77737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Google Earth® (2013) Google Inc.

  23. Halpern BS, Longo C, Hardy D, McLeod KL, Samhouri JF, Katona SK et al (2012) An index to assess the health and benefits of the global ocean. Nature 488:615–620

    Article  CAS  PubMed  Google Scholar 

  24. Horta PA, Amancio E, Coimbra CS, Oliveira EC (2001) Considerações sobre a distribuição e origem da flora de macroalgas marinhas brasileiras. Hoehnea 28:243–265

    Google Scholar 

  25. IBGE (2010) Instituto Brasileiro de Geografia e Estatística Censo Demográfico. http://www.censo2010.ibge.gov.br. Acessed 26 June 2015

  26. ITEP (2012) Instituto de Tecnologia de Pernambuco. Relatório de impacto ambiental. Recuperação da orla marítima. Municípios de Jaboatão dos Guararapes, Recife, Olinda e Paulista (Pernambuco). Instituto de Tecnologia de Pernambuco, Recife, pp 1–98

    Google Scholar 

  27. Johnston EL, Roberts DA (2009) Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. Environ Pollut 157:1745–1752

    Article  CAS  PubMed  Google Scholar 

  28. Juanes JA, Guinda X, Puente A, Revilla JA (2008) Macroalgae, a suitable indicator of the ecological status of coastal rocky communities in the NE Atlantic. Ecol Indic 8:351–359

    Article  Google Scholar 

  29. Köppen W (1948) Climatologia: con un estudio de los climas de la tierra. Fondo de Cultura Econômica, Mexico, pp 1–479

    Google Scholar 

  30. Krause-Jensen D, Sagert S, Schubert H, Bostrom C (2008) Empirical relationships linking distribution and abundance of marine vegetation to eutrophication. Ecol Indic 8:515–529

    Article  Google Scholar 

  31. Laborel JL (1969) Madreporaires et hidrocoralliaires recifaux dês cotes brésiliennes. Systematíque, ecologie, repartition verticale et geographic. Ann Inst Oceanogr Paris 47:171–226

    Google Scholar 

  32. Lapointe BE (1989) Macroalgal production and nutrient relations in oligotrophic areas of Florida bay. Bull Mar Sci 44:312–323

    Google Scholar 

  33. Loffler Z, Hoey AS (2018) Canopy-forming macroalgal beds (Sargassum) on coral reefs are resilient to physical disturbance. J Ecol 106:1156–1164

    Article  Google Scholar 

  34. Mangialajo L, Chiantore M, Cattaneo-Vietti R (2008) Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Mar Ecol Prog Ser 358:63–74

    Article  Google Scholar 

  35. Manso VAV, Coutinho PN, Guerra NC, Soares CFA (2006) Pernambuco. In: Muehe D (ed) Erosão e Progradação no Litoral Brasileiro. Ministério do Meio Ambiente, Brasília, pp 179–196

    Google Scholar 

  36. Martins CD, Arantes N, Faveri C, Batista MB, Oliveira EC, Pagliosa PR, Fonseca AL, Nunes JMC, Chow F, Pereira SB, Horta PA (2012) The impact of coastal urbanization on the structure of phytobenthic communities in southern Brazil. Mar Pollut Bull 64:772–778

    Article  CAS  PubMed  Google Scholar 

  37. Moreira AR, Armenteros M, Gómez M, Leon AR, Cabrera R, Castellanos ME, Munoz A, Suarez AM (2006) Variation of macroalgae biomass in Cienfuegos bay, Cuba. Rev Investig Mar 27:3–12

    Google Scholar 

  38. Orfanidis S, Panayotidis P, Stamatis N (2003) An insight to the ecological evaluation index (EEI). Ecol Indic 3:27–33

    Article  Google Scholar 

  39. Orlandi L, Bentivogli F, Carlino P, Calizza E, Rossi D, Costantini ML, Rossi L (2014) δ15 N variation in Ulva lactuca as a proxy for anthropogenic nitrogen inputs in coastal areas of gulf of Gaeta (Mediterranean Sea). Mar Pollut Bull 84:76–82

    Article  CAS  PubMed  Google Scholar 

  40. Ortega JLG (2000) Algas. In: Espino GL, Pulido J, Pérez JLC (eds) Organismos indicadores de la calidad del água y de la contaminación (Bioindicadores). Playa y Valdés, Mexico, pp 109–193

    Google Scholar 

  41. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685

    Article  Google Scholar 

  42. Peckol P, Rivers JS (1996) Contribution by macroalgal mats to primary production of a shallow embayment under high and low nitrogen-loading rates. Estuar Coast Shelf Sci 43:311–325

    Article  CAS  Google Scholar 

  43. Pereira SMB, Carvalho MFO, Angeiras JA, Pedrosa MEB, Oliveira NMB, et al (2002) Algas marinhas bentônicas do estado de Pernambuco. In: Tabarelli M, Silva JMC (ed) Diagnóstico da biodiversidade de Pernambuco. Secretaria de Ciência, Tecnologia e Meio Ambiente, Massangana, Recife, 1, p 97–124

  44. Pereira SMB, Oliveira-Carvalho MF, Burgos DC, Araújo EL (2008) Caracterização estrutural das macroalgas de ambiente recifal da praia de Enseada dos Corais. In: Congresso Brasileiro de Ficologia, XI, Itajaí-SC. Anais de trabalho completos. Série Livros do Museu Nacional. Rio de Janeiro, p 231–242

  45. Portugal AB, Carvalho FL, de Macedo Carneiro PB, Rossi S, de Oliveira Soares M (2016) Increased anthropogenic pressure decreases species richness in tropical intertidal reefs. Mar Environ Res 120:44–54

    Article  CAS  PubMed  Google Scholar 

  46. Projeto Orla (2002) Projeto Orla: fundamentos para gestão integrada. Brasília: MMA/SQA; Brasília: MP/SPU, p 78

  47. Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133

    Article  Google Scholar 

  48. Santos GS, Lira SMA, Schwamborn R (2015) Análise das comunidades macrobentônicos sésseis, com ênfase na interação entre o cnidário Zoanthus sociatus (Ellis, 1768) e macroalgas, no topo de um recife de águas rasas do nordeste do Brasil. Trop Oceanogr 43:1–8

    Article  Google Scholar 

  49. Scherner F, Horta PA, Oliveira EC, Simonassi JC, Hall-Spencer JM, Chow F, Nunes JM, Prereira SM (2013) Coastal urbanization leads to remarkable seaweed species loss and community shifts along the SW Atlantic. Mar Pollut Bull 76:106–115

    Article  CAS  PubMed  Google Scholar 

  50. Schiel DR (2006) Rivets or bolts? When single species count in the function of temperate rocky reef communities. J Exp Mar Biol Ecol 338:233–252

    Article  Google Scholar 

  51. Shanmugam P, Neelamani S, Ahn YH, Philip L, Hong GH (2007) Assessment of the levels of coastal marine pollution of Chennai city, southern India. Water Resour Manag 21:1187–1206

    Article  Google Scholar 

  52. SNIS (2011) Sistema Nacional de Informações sobre Saneamento: Diagnóstico dos serviços de água e esgotos. Ministério das cidades SNSA, Brasília, p 432

    Google Scholar 

  53. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57:573–583

    Article  Google Scholar 

  54. Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal dominated communities. Oikos 69:476–498

    Article  Google Scholar 

  55. Tait LW, Schiel DR (2011) Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages. PLoS One 6:e26986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Thibaut T, Pinedo S, Torras X, Ballesteros E (2005) Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albéres coast (France, North-Western Mediterranean). Mar Pollut Bull 50:1472–1489

    Article  CAS  PubMed  Google Scholar 

  57. Tsai C, Chang J, Sheu F, Shyu Y, Yu A, Wong S, Dai C, Lee T (2005) Seasonal growth dynamics of Laurencia papillosa and Gracilaria coronopifolia and from a highly eutrophic reef in southern Taiwan: temperature limitation and nutrient availability. J Exp Mar Biol Ecol 315:49–69

    Article  Google Scholar 

  58. Turra A, Croquer A, Carranza A, Mansilla A, Areces AJ, Werlinger C et al (2013) Global environmental changes: setting priorities for Latin American coastal habitats. Glob Chang Biol 19:1965–1969

    Article  PubMed  Google Scholar 

  59. Vasconcelos ERTPP, Reis TNV, Guimarães-Barros NC, Bernardi J, Areces-Mallea AJ, Cocentino ALM, Fujii MT (2013) Padrão espacial da comunidade de macroalgas de mesolitoral em ambiente recifal do nordeste brasileiro. Trop Oceanogr 41:84–92

    Google Scholar 

  60. Villaça R, Fonseca AC, Jensen VK, Knoppers B (2010) Species composition and distribution of macroalgae on Atol das Rocas, Brazil, SW Atlantic. Bot Mar 53:113–122

    Article  Google Scholar 

  61. Worm B, Lotze HK, Boström C, Engkvist R, Labanauskas V, Sommer U (1999) Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Mar Ecol Prog Ser 185:309–314

    Article  Google Scholar 

Download references

Acknowledgments

The first author thanks the Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE) for the PhD Scholarship and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Science without Frontier Scholarship. MTF thanks CNPq for the Productivity Fellowship (Proc. 303915/2013-7). The authors thank Souza-Filho JS, Neumann-Leitão S, Feitosa FA, Rosa-Filho JS for helpful advice and comments.

Funding

This work was supported by research grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Proc. 484647/2012-1).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Edson Régis Tavares Pessoa Pinho de Vasconcelos.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Vasconcelos, E.R.T.P.P., Vasconcelos, J.B., Reis, T.N.d. et al. Macroalgal responses to coastal urbanization: relative abundance of indicator species. J Appl Phycol 31, 893–903 (2019). https://doi.org/10.1007/s10811-018-1639-3

Download citation

Keywords

  • Coast occupation
  • Bioindicators
  • Phytobenthos
  • Coastal reefs