Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-14T11:15:15.522Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity of intertidal marine sponges from the western coast of Portugal (North-east Atlantic)

Published online by Cambridge University Press:  07 June 2019

A. Regueiras ,
A. Alex ,
M. S. Costa ,
S. Pereira  and
V. Vasconcelos
A. Regueiras
Affiliation:
CIIMAR/CIMAR, Blue Biotechnology and Ecotoxicology, Centre of Environmental and Marine Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal Department of Biology, Sciences Faculty, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal
A. Alex
Affiliation:
CIIMAR/CIMAR, Blue Biotechnology and Ecotoxicology, Centre of Environmental and Marine Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal
M. S. Costa
Affiliation:
CIIMAR/CIMAR, Blue Biotechnology and Ecotoxicology, Centre of Environmental and Marine Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal Faculty of Pharmaceutical Sciences, University of Iceland, Hagi, Hofsvallagata 53, 107, Reykjavik, Iceland
S. Pereira
Affiliation:
CIIMAR/CIMAR, Blue Biotechnology and Ecotoxicology, Centre of Environmental and Marine Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal
V. Vasconcelos*
Affiliation:
CIIMAR/CIMAR, Blue Biotechnology and Ecotoxicology, Centre of Environmental and Marine Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal Department of Biology, Sciences Faculty, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal
*
Author for correspondence: V. Vasconcelos, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Sponges are important components of intertidal marine communities. There is a lack of information about intertidal marine sponge diversity in the western coast of Portugal (North-east Atlantic). In the present work we identified the most common intertidal sponges of the western coast of Portugal, and made a comprehensive list of the intertidal species described so far for this region. Sponges belonging to the Classes Calcarea and Demospongiae were identified, the former class for the first time at these locations. Demospongiae are the most common intertidal sponges, present in all sampling locations. We used an integrative approach for Demospongiae identification, using both morphological and molecular characters. Molecular identification, using a CO1 marker proved to be helpful in the identification to the genus level, despite some limitations, such as difficulty in amplification experienced for sponges as well as non-target organisms. A total of 170 specimens were collected. Seven specimens (five species) belonged to the Class Calcarea and 163 specimens (23 species) to the Class Demospongiae. The demosponge Hymeniacidon perlevis was present at all sample locations. Calcarean species were primarily found in samples taken along the south-western coast.

Keywords

CalcareaCO1Demospongiaeintertidal diversityPoriferaPortugal
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 6 , September 2019 , pp. 1253 - 1265
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alex, A and Antunes, A (2015) Pyrosequencing characterization of the microbiota from Atlantic intertidal marine sponges reveals high microbial diversity and the lack of co-occurrence patterns. PLoS ONE 10, e0127455.Google Scholar
Alex, A, Vasconcelos, V, Tamagnini, P, Santos, A and Antunes, A (2012) Unusual symbiotic cyanobacteria association in the genetically diverse intertidal marine sponge Hymeniacidon perlevis (Demospongiae, Halichondrida). PLoS ONE 7, e51834.Google Scholar
Alex, A, Silva, V, Vasconcelos, V and Antunes, A (2013) Evidence of unique and generalist microbes in distantly related sympatric intertidal marine sponges (Porifera: Demospongiae). PLoS ONE 8, e80653.Google Scholar
Alvizu, A, Eilertsen, MH, Xavier, JR and Rapp, HT (2018) Increased taxon sampling provides new insights into the phylogeny and evolution of the subclass Calcaronea (Porifera, Calcarea). Organisms Diversity & Evolution 18, 279–290.Google Scholar
Appeltans, W, Ahyong, ST, Anderson, G, Angel, MV, Artois, T, Bailly, N, Bamber, R, Barber, A, Bartsch, I, Berta, A, Błażewicz-Paszkowycz, M, Bock, P, Boxshall, G, Boyko, CB, Brandão, SN, Bray, RA, Bruce, NL, Cairns, SD, Chan, T-Y, Cheng, L, Collins, AG, Cribb, T, Curini-Galletti, M, Dahdouh-Guebas, F, Davie, PJF, Dawson, MN, De Clerck, O, Decock, W, De Grave, S, de Voogd, NJ, Domning, DP, Emig, CC, Erséus, C, Eschmeyer, W, Fauchald, K, Fautin, DG, Feist, SW, Fransen, CHJM, Furuya, H, Garcia-Alvarez, O, Gerken, S, Gibson, D, Gittenberger, A, Gofas, S, Gómez-Daglio, L, Gordon, DP, Guiry, MD, Hernandez, F, Hoeksema, BW, Hopcroft, RR, Jaume, D, Kirk, P, Koedam, N, Koenemann, S, Kolb, JB, Kristensen, RM, Kroh, A, Lambert, G, Lazarus, DB, Lemaitre, R, Longshaw, M, Lowry, J, Macpherson, E, Madin, LP, Mah, C, Mapstone, G, McLaughlin, PA, Mees, J, Meland, K, Messing, CG, Mills, CE, Molodtsova, TN, Mooi, R, Neuhaus, B, Ng, PKL, Nielsen, C, Norenburg, J, Opresko, DM, Osawa, M, Paulay, G, Perrin, W, Pilger, JF, Poore, GCB, Pugh, P, Read, GB, Reimer, JD, Rius, M, Rocha, RM, Saiz-Salinas, JI, Scarabino, V, Schierwater, B, Schmidt-Rhaesa, A, Schnabel, KE, Schotte, M, Schuchert, P, Schwabe, E, Segers, H, Self-Sullivan, C, Shenkar, N, Siegel, V, Sterrer, W, Stöhr, S, Swalla, B, Tasker, ML, Thuesen, EV, Timm, T, Todaro, MA, Turon, X, Tyler, S, Uetz, P, van der Land, J, Vanhoorne, B, van Ofwegen, LP, van Soest, RWM, Vanaverbeke, J, Walker-Smith, G, Walter, TC, Warren, A, Williams, GC, Wilson, SP and Costello, MJ (2012) The magnitude of global marine species diversity. Current Biology 22, 2189–2202.Google Scholar
Barnes, DKA and Bell, JJ (2002) Coastal sponge communities of the West Indian Ocean: morphological richness and diversity. African Journal of Ecology 40, 350–359.Google Scholar
Bell, JJ (2008) The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79, 341–353.Google Scholar
Bell, JJ and Barnes, DKA (2000) The influences of bathymetry and flow regime upon the morphology of subtidal sponge communities. Journal of the Marine Biological Association of the United Kingdom 80, 707–718.Google Scholar
Boaventura, D, Ré, P, da Fonseca, LC and Hawkins, SJ (2002) Intertidal rocky shore communities of the continental Portuguese coast: analysis of distribution patterns. Marine Ecology–Pubblicazioni Della Stazione Zoologica Di Napoli I 23, 69–90.Google Scholar
Boury-Esnault, N (2006) Systematics and evolution of Demospongiae. Canadian Journal of Zoology 84, 205–224.Google Scholar
Boury-Esnault, N, Lavrov, DV, Ruiz, CA and Pérez, T (2013) The integrative taxonomic approach applied to Porifera: a case study of the Homoscleromorpha. Integrative and Comparative Biology 53, 416–427.Google Scholar
Cárdenas, P, Menegola, C, Rapp, HT and Diaz, MC (2009) Morphological description and DNA barcodes of shallow-water Tetractinellida (Porifera: Demospongiae) from Bocas del Toro, Panama, with description of a new species. Zootaxa 2276, 1–39.Google Scholar
Cárdenas, P, Pérez, T and Boury-Esnault, N (2012) Sponge systematics facing new challenges. Advances in Marine Biology 61, 79–209.Google Scholar
Carter, HJ (1876) Descriptions and figures of deep-sea sponges and their spicules, from the Atlantic Ocean, dredged up on board H.M.S. ‘Porcupine’, chiefly in 1869 (concluded). Annals and Magazine of Natural History 18, 226–240.Google Scholar
Cebrian, E, Uriz, MJ and Turon, X (2007) Sponges as biomonitors of heavy metals in spatial and temporal surveys in northwestern Mediterranean: multispecies comparison. Environmental Toxicology and Chemistry 26, 2430–2439.Google Scholar
Costa, ACC (2012) Caracterização e cartografia da fauna intertidal das praias rochosas de Matosinhos. MSc degree, Universidade do Porto.Google Scholar
Costa, M, Costa-Rodrigues, J, Fernandes, MH, Barros, P, Vasconcelos, V and Martins, R (2012) Marine cyanobacteria compounds with anticancer properties: a review on the implication of apoptosis. Marine Drugs 10, 2181–2207.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Erpenbeck, D, Breeuwer, JAJ, van der Velde, HC and van Soest, RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Marine Biology 141, 377–386.Google Scholar
Erpenbeck, D, Hooper, JNA and Wörheide, G (2006) CO1 phylogenies in diploblasts and the ‘Barcoding of Life’ – are we sequencing a suboptimal partition? Molecular Ecology Notes 6, 550–553.Google Scholar
Erpenbeck, D, Voigt, O, Al-Aidaroos, AM, Berumen, ML, Büttner, G, Catania, D, Guirguis, AN, Paulay, G, Schätzle, S and Wörheide, G (2016) Molecular biodiversity of Red Sea demosponges. Marine Pollution Bulletin 105, 507–514.Google Scholar
Felsenstein, J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hall, T (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hanitsch, R (1895) Notes on a collection of sponges from the west coast of Portugal. Transactions of the Liverpool Biological Society 9, 205–219.Google Scholar
Hill, MS, Hill, AL, Lopez, J, Peterson, KJ, Pomponi, S, Diaz, MC, Thacker, RW, Adamska, M, Boury-Esnault, N, Cárdenas, P, Chaves-Fonnegra, A, Danka, E, De Laine, B-O, Formica, D, Hajdu, E, Lobo-Hajdu, G, Klontz, S, Morrow, CC, Patel, J, Picton, B, Pisani, D, Pohlmann, D, Redmond, NE, Reed, J, Richey, S, Riesgo, A, Rubin, E, Russell, Z, Rützler, K, Sperling, EA, di Stefano, M, Tarver, JE and Collins, AG (2013) Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes. PLoS ONE 8, e50437.Google Scholar
Hooper, JNA and van Soest, RWM (2002) Systema Porifera. A Guide to the Classification of Sponges. New York, NY: Springer-Verlag.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Kottek, M, Grieser, J, Beck, C, Rudolf, B and Rubel, F (2006) World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15, 259–263.Google Scholar
Leal, MC, Puga, J, Serôdio, J, Gomes, NC and Calado, R (2012) Trends in the discovery of new marine natural products from invertebrates over the last two decades – where and what are we bioprospecting? PLoS ONE 7, e30580.Google Scholar
Lévi, C and Vacelet, J (1958) Éponges récoltées dans l'Atlantique Oriental par le ‘‘Président Théodore Tissier’’ (1955–1956). Recueil des Travaux de l'Institut des Pêches maritimes 22, 225–246.Google Scholar
Lopes, MT (1989) Demosponjas intertidais da Costa Portuguesa (PhD thesis). Universidade de Lisboa.Google Scholar
Lopes, MT (1995) Colheita, preparação e identificação de espongiários. Lisbon: Museu Nacional de História Natural. Lisboa, Portugal.Google Scholar
Lopes, MT and Boury-Esnault, N (1981) Contribution à la connaissance des éponges cornées de la côte de l'Arrábida de de l'Algarve. Arquivos do Museu Bocage 1, 95–110.Google Scholar
Mahaut, M-L, Basuyaux, O, Baudinière, E, Chataignier, C, Pain, J and Caplat, C (2013) The Porifera Hymeniacidon perlevis (Montagu, 1818) as a bioindicator for water quality monitoring. Environmental Science and Pollution Research 20, 2984–2992.Google Scholar
Maldonado, M, Ribes, M and van Duyl, FC (2012) Nutrient fluxes through sponges: biology, budgets, and ecological implications. Advances in Marine Biology 62, 113–182.Google Scholar
Meyer, CP, Geller, JB and Paulay, G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59, 113–125.Google Scholar
Monteiro Marques, V, Reis, CS, Calvario, J, Marques, JC, Melo, R and Santos, R (1982) Contribuição para o estudo dos povoamentos bentónicos (substrato rochoso) da costa ocidental portuguesa. Oecologia Aquatica 6, 119–145.Google Scholar
Morrow, C and Cárdenas, P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Frontiers in Zoology 12, 7.Google Scholar
Morrow, CC, Redmond, NE, Picton, BE, Thacker, RW, Collins, AG, Maggs, CA, Sigwart, JD and Allcock, AL (2013) Molecular phylogenies support homoplasy of multiple morphological characters used in the taxonomy of heteroscleromorpha (Porifera: Demospongiae). Integrative and Comparative Biology 53, 428–446.Google Scholar
Naveiro, A (2002) Poriferos de la costa da Arrábida (Portugal): Classe Demospongiae. MSc Thesis, University of Santiago de Compostela, Santiago de Compostela, Spain.Google Scholar
Nylander, J (2004) MrAic.pl. Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.Google Scholar
Pereira, TR (2007) As comunidades porifera do litoral norte (MSc Thesis). Universidade de Aveiro.Google Scholar
Pereira, SG, Lima, FP, Queiroz, NC, Ribeiro, PA and Santos, AM (2006) Biogeographic patterns of intertidal macroinvertebrates and their association with macroalgae distribution along the Portuguese coast. Hydrobiologia 555, 185.Google Scholar
Pérès, JM (1959) Aperçu bionomique sur les communautés bentiques des côtes sud du Portugal. Resultats Scientifiques de la campagne du N.R.P. “Faial” dans les eaux cotieres du Portugal (1957) 1, 1–35.Google Scholar
Pires, FR (2007) Padrões de distribuição e taxonomia para os Porifera da região central do Algarve. Mestrado em Biologia Marinha com especialização em Ecologia e Conservação Marinha, Universidade do Algarve, Faro, Portugal.Google Scholar
Pöppe, J, Sutcliffe, P, Hooper, JN, Wörheide, G and Erpenbeck, D (2010) CO1 barcoding reveals new clades and radiation patterns of Indo-Pacific sponges of the family Irciniidae (Demospongiae: Dictyoceratida). PLoS ONE 5, e9950.Google Scholar
Regueiras, A, Alex, A, Pereira, S, Costa, MS, Antunes, A and Vasconcelos, V (2017) Cyanobacterial diversity in the marine sponge Hymeniacidon perlevis from a temperate region (Portuguese coast, Northeast Atlantic). Aquatic Microbial Ecology 79, 259–272.Google Scholar
Rützler, K (2012) The role of sponges in the Mesoamerican barrier-reef ecosystem, Belize. Advances in Marine Biology 61, 211–271.Google Scholar
Saldanha, L (1974) Estudo do povoamento dos horizontes superiores da rocha litoral da costa da Arrábida (Portugal) (PhD Thesis). Arquivos Museu Bocage, 2ª Série, 1.Google Scholar
Sarà, M and Vacelet, J (1973) Ecologie des démosponges. In Grassé, PP (ed.), Traité de Zoologie, Vol. III, Fasc. 1. Paris: Masson Cie, pp. 462–576.Google Scholar
Spalding, MD, Fox, HE, Allen, GR, Davidson, N, Ferda, xAZA, Finlayson, MAX, Halpern, BS, Jorge, MA, Lombana, AL, Lourie, SA, Martin, KD, McManus, E, Molnar, J, Recchia, CA and Robertson, J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583.Google Scholar
Thacker, RW, Hill, AL, Hill, MS, Redmond, NE, Collins, AG, Morrow, CC, Spicer, L, Carmack, CA, Zappe, ME, Pohlmann, D, Hall, C, Diaz, MC and Bangalore, PV (2013) Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integrative and Comparative Biology 53, 373–387.Google Scholar
Topsent, E (1928) Spongiaires de l'Atlantique et de la Méditerranée provenant des croisières du Prince Albert ler de Monaco. Résultats des campagnes scientifiques accomplies par le Prince Albert I. Monaco 74, 71–376.Google Scholar
Van Soest, RW, Boury-Esnault, N, Vacelet, J, Dohrmann, M, Erpenbeck, D, De Voogd, NJ, Santodomingo, N, Vanhoorne, B, Kelly, M and Hooper, JN (2012) Global diversity of sponges (Porifera). PLoS ONE 7, e35105.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, Ríos, P and Downey, R (2017) World Porifera Database. http://www.marinespecies.org/porifera.Google Scholar
Vargas, S, Schuster, A, Sacher, K, Büttner, G, Schätzle, S, Läuchli, B, Hall, K, Hooper, JNA, Erpenbeck, D and Wörheide, G (2012) Barcoding sponges: an overview based on comprehensive sampling. PLoS ONE 7, e39345.Google Scholar
Voigt, O and Wörheide, G (2016) A short LSU rRNA fragment as a standard marker for integrative taxonomy in calcareous sponges (Porifera: Calcarea). Organisms Diversity and Evolution 16, 53–64.Google Scholar
Wörheide, G, Solé-Cava, AM and Hooper, JNA (2005) Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks. Integrative and Comparative Biology 45, 377–385.Google Scholar
Wörheide, G, Erpenbeck, D and Menke, C (2007) The sponge barcoding project. In Custódio, MR, Lobo-Hajdu, G, Hajdu, E and Muricy, G (eds), Porifera Research: Biodiversity, Innovation and Sustainability. Rio de Janeiro: Série Livros 28, Museu Nacional, pp. 123–128.Google Scholar
Wulff, J (2012) Ecological interactions and the distribution, abundance, and diversity of sponges. Advances in Marine Biology 61, 273–344.Google Scholar
Xavier, JR and van Soest, RWM (2012) Diversity patterns and zoogeography of the Northeast Atlantic and Mediterranean shallow-water sponge fauna. Hydrobiologia 687, 107–125.Google Scholar
Xavier, JR, Rachello-Dolmen, PG, Parra-Velandia, F, Schönberg, CHL, Breeuwer, JAJ and van Soest, RWM (2010) Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Molecular Phylogenetics and Evolution 56, 13–20.Google Scholar
Supplementary material: File

Regueiras et al. supplementary material

Regueiras et al. supplementary material 1

Download Regueiras et al. supplementary material(File)
File 94.6 KB
Supplementary material: File

Regueiras et al. supplementary material

Regueiras et al. supplementary material 2

Download Regueiras et al. supplementary material(File)
File 45.1 KB
Supplementary material: File

Regueiras et al. supplementary material

Regueiras et al. supplementary material 3

Download Regueiras et al. supplementary material(File)
File 23.8 KB