Abstract
Maerl beds are unique marine habitats hosting a great diversity of organisms while macroalgae are a major component of this diversity. The bay of Brest is one of the most studied coastal ecosystems in the world; in addition, it has a significant background concerning historical seaweeds check-lists associated to maerl beds. However, no recent work aimed at compiling and completing these data. In this study, a total of 7 subtidal and 3 intertidal maerl beds have been surveyed between 2020 and 2022. These data complete 4 previous inventories, giving the most accurate description of seaweeds colonizing maerl beds in the bay of Brest. The total number of macroalgal species reaches 170 among which 127 are Rhodophyta, 22 Phaeophyceae, and 21 Ulvophyceae, with 51 additions to the French and 19 additions to the European maerl beds check-list. A comparison with other maerl beds of the northeastern Atlantic coasts is compiled. It appears that the maerl beds from the bay of Brest are the most diverse in Atlantic France and among the most diverse in Europe. A description of the stratification of maerl beds and the associated macroalgal communities is proposed. It includes maerl species, encrusting species, maerl-entangling species, erect isolated species, and free-living species. In addition, specimens of the rarely recorded Rytiphlaea tinctoria, reaching its northernmost population in the bay, a possible introduced species/relict population, are described.
Similar content being viewed by others
References
Androuin T (2018) Ecologie trophique de l'espèce ingénieur Crepidula fornicata et implications pour le fonctionnement de son habitat, PhD thesis. Université de Bretagne occidentale-Brest, pp 225
Ardré F (1970) Contribution à l'étude des algues marines du Portugal. I. La flore. Port. Acta Biol (B) 10:1–423
Bárbara I, García-Redondo V, Díaz-Tapia P, García-Fernández A, Piñeiro-Corbeira C, Peña V, Lugilde J, Cremades J (2019) Adiciones y correcciones a la flora bentónica marina del Atlántico ibérico norte. Acta Bot Malac 44:51–60
Barbera C, Bordehore C, Borg JA, Glémarec M, Grall J, Hall-Spencer JM, De La Huz C, Lanfranco E, Lastra M, Moore P (2003) Conservation and management of northeast Atlantic and Mediterranean maerl beds. Aquat Conserv Mar Freshw Ecosyst 13:S65–S76
Basualdo CV (2011) Choosing the best non-parametric richness estimator for benthic macroinvertebrates databases. Rev Soc Entomol Argent 70:27–38
BIOMAERL (1999) Final Report, BIOMAERL project (Coordinator: PG Moore, University Marine Biological Station Millport, Scotland), EC Contract No. MAS3-CT95-0020, (in 2 vols.) pp 1–541, 542–973+ appendix
Blunden G, Farnham W, Jephson N, Fenn R, Plunkett B (1977) The composition of maerl from the Glenan Islands of Southern Brittany. Bot Mar 20:121–126
Boedeker C, Leliaert F, Zuccarello GC (2016) Molecular phylogeny of the Cladophoraceae (Cladophorales, Ulvophyceae), with the resurrection of Acrocladus Nägeli and Willeella Børgesen, and the description of Lurbica gen. nov. and Pseudorhizoclonium gen. nov. J Phycol 52:905–928
Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38
Brodie J, Wilbraham J, Pottas J, Guiry MD (2016) A revised check-list of the seaweeds of Britain. J Mar Biol Assoc U K 96:1005–1029
Burel T, Le Duff M, Gall EA (2019) Updated check-list of the seaweeds of the French coasts, Channel and Atlantic Ocean. An Aod-Les cahiers naturalistes de l’Observatoire marin 7:1-38
Cabioc'h J (1968) Quelques particularités anatomiques du Lithophyllum fasciculatum (Lamarck) Foslie. Bulletin de la Société botanique de France 115:173-186
Cabioc'h J (1969) Les fonds de maërl de la baie de Morlaix et leur peuplement végétal. Cahiers de Biologie Marine, Station biologique de Roscoff et Laboratoire de Biologie végétale marine, Faculté des Sciences de Paris 10:139-161
Cremades J, Barreiro R, Maneiro I, Saunders GW (2011) A new taxonomic interpretation of the type of Plocamium cartilagineum (Plocamiales, Florideophyceae) and its consequences. Eur J Phycol 46:125–142
Crouan PL, Crouan HM (1852) Algues marines du Finistère, comments to exsiccata
Crouan PL, Crouan HM (1867) Florule du Finistère. Contenant les descriptions de 360 espèces nouvelles de Sporogames, de nombreuses observations et une synonymie des plantes cellulaires et vasculaires. Klincksieck; Lefournier, Paris & Brest, pp 406
Diaz-Tapia P, Barbara I, Cremades J, Verbruggen H, Maggs CA (2017) Three new cryptogenic species in the tribes Polysiphonieae and Streblocladieae (Rhodomelaceae, Rhodophyta). Phycologia 56:605–623
Díaz-Tapia P, Baldock L, Maggs C (2020) Discovery of Flabellia petiolata (Halimedaceae, Chlorophyta) in the southern British Isles: a relict population or a new introduction? Aquat Bot 160:103160
Dinter WP (2001) Biogeography of the OSPAR maritime area. Federal Agency for Nature Conservation, Bonn, Germany, p 167
Dizerbo A, Herpe E (2007) Liste et répartition des algues marines des côtes françaises de la Manche et de l’Atlantique. Iles Normandes incluses, Éditions Anaximandre, Landernau, 351 p
Foster MS (2001) Rhodoliths: between rocks and soft places. J Phycol 37:659–667
Foster M, McConnico L, Lundsten L, Wadsworth T, Kimball T, Brooks L, Medina-López M, Riosmena-Rodríguez R, Hernández-Carmona G, Vásquez-Elizondo R (2007) Diversity and natural history of a Lithothamnion muelleri-Sargassum horridum community in the Gulf of California. Cienc Mar 33:367–384
Fredericq S, Krayesky-Self S, Sauvage T, Richards J, Kittle R, Arakaki N, Hickerson E, Schmidt WE (2019) The critical importance of rhodoliths in the life cycle completion of both macro-and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Front Mar Sci 5:502
Geoffroy A (2012) Diversité génétique et délimitation d'espèces par des approches conjointes de barcoding et de génétique des populations: application à l'identification d'espèces d'algues marines nouvellement cultivées. Paris 6, pp 175
Grall J (2002) Biodiversité spécifique et fonctionnelle du maerl: réponses à la variabilité de l'environnement côtier, PhD Thesis. Brest Université de Bretagne Occidentale, pp 302
Grall J (2003) Fiche de synthèse sur les biocénoses: les bancs de maërl. Rapport IUEM (UBO)/LEMAR (http://www.rebent.org/documents/), 20 p
Grall J, Chauvaud L (2002) Marine eutrophication and benthos: the need for new approaches and concepts. Glob Chang Biol 8:813–830
Grall J, Hall-Spencer J (2003) Problems facing maerl conservation in Brittany. Aquat Conserv Mar Freshw Ecosyst 13:10
Grall J, Le Loc'h F, Guyonnet B, Riera P (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J Exp Mar Biol Ecol 338:1–15
Guillou M, Grall J, Connan S (2002) Can low sea urchin densities control macro-epiphytic biomass in a north-east Atlantic maerl bed ecosystem (Bay of Brest, Brittany, France)? J Mar Biol Assoc U K 82:867–876
Guiry MD (2012) A catalogue of Irish seaweeds, A.R.G. Gantner Verlag K.G, Ruggell, pp 250
Guiry MD, Freamhainn MT (1985) Biosystematics of Gracilaria foliifera (Gigarthales, Rhodophyta). Nord J Bot 5:629–637
Guiry MD, Guiry GM (2022) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed 2 Sept 2022
Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D'Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE (2008) A global map of human impact on marine ecosystems. Science 319:948–952
Hardy FG, Guiry MD (2003) A check-list and atlas of the seaweeds of Britain and Ireland. British Phycological Society, London, pp 435
Hernandez-Kantun JJ, Rindi F, Adey WH, Heesch S, Peña V, Le Gall L, Gabrielson PW (2015) Sequencing type material resolves the identity and distribution of the generitype Lithophyllum incrustans, and related European species L. hibernicum and L. bathyporum (Corallinales, Rhodophyta). J Phycol 51:791–807
Hily C, Potin P, Floc'h J-Y (1992) Structure of subtidal algal assemblages on soft-bottom sediments: fauna/flora interactions and role of disburbances in the Bay of Brest, France. Mar Ecol Prog Ser 85:115–130
Hiscock S (1986) A field key to the British red seaweeds (Rhodophyta). Field Studies Council Occasional Publication
Hsieh T, Ma K, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456
Jardim VL, Gauthier O, Toumi C, Grall J (2022) Quantifying maerl (rhodolith) habitat complexity along an environmental gradient at regional scale in the Northeast Atlantic. Mar Environ Res 105768
Kamenos N, Moore P, Hall-Spencer J (2003) Substratum heterogeneity of dredged vs un-dredged maerl grounds. J Mar Biol Assoc U K 83:411–413
L’Hardy-Halos M-T, Castric-Fey A, Girard-Descatoire A, Lafargue F (1973) Recherches en scaphandre autonome sur le peuplement végétal du substrat rocheux: l’Archipel de Glénan. Bulletin de la Société scientifique de Bretagne 48:103-128
Legrand E, Riera P, Lutier M, Coudret J, Grall J, Martin S (2017) Species interactions can shift the response of a maerl bed community to ocean acidification and warming. Biogeosciences 14:5359–5376
Leliaert F, Boedeker C, Peña V, Bunker F, Verbruggen H, De Clerck O (2009) Cladophora rhodolithicola sp. nov. (Cladophorales, Chlorophyta), a diminutive species from European maerl beds. Eur J Phycol 44:155–169
Maggs C, Guiry M (1981) Le Cladophora pygmaea Reinke, espece nouvelle pour les côtes de France. Trav Stat Biol Roscoff NS 27:11-13
Maggs C, Guiry M (1987) Gelidiella calcicola sp. nov. (Rhodophyta) from the British Isles and Northern France. Br Phycol J 22:417–434
Maggs C, Hommersand MH (1993) Seaweeds of the British Isles. Volume 1 Rhodophyta, Part 3A Ceramiales, Natural History Museum, London, pp 444
Martin S, Hall-Spencer JM (2017) Effects of ocean warming and acidification on rhodolith/maërl beds. In: Riosmena-Rodríguez R, Nelson W, Aguirre J, Rhodolith/maerl beds: A global perspective. Springer International Publishing, Switzerland, pp 55–85
Peña V (2010) Estudio ficológico de los fondos de maërl y cascajo en el noroeste de la Península Ibérica, PhD thesis. A Coruña, Universidade da Coruña, pp 635
Peña V, Bárbara I (2008) Maërl community in the north-western Iberian Peninsula: a review of floristic studies and long-term changes. Aquat Conserv Mar Freshw Ecosyst 18:339–366
Peña V, Bárbara I (2010a) New records of crustose seaweeds associated with subtidal maërl beds and gravel bottoms in Galicia (NW Spain). Bot Mar 53:41–61
Peña V, Bárbara I (2010b) Seasonal patterns in the maerl community of shallow European Atlantic beds and their use as a baseline for monitoring studies. Eur J Phycol 45:327–342
Peña V, Bárbara I (2013) Non-coralline crustose algae associated with maerl beds in Portugal: a reappraisal of their diversity in the Atlantic Iberian beds. Bot Mar 56:481–493
Peña V, Adey WH, Riosmena-Rodríguez R, Jung MY, Afonso-Carrillo J, Choi HG, Barbara I (2011) Mesophyllum sphaericum sp. nov. (Corallinales, Rhodophyta): a new maerl-forming species from the northeast Atlantic. J Phycol 47:911–927
Peña V, Barreiro R, Hall-Spencer JM, Grall J (2013) Lithophyllum spp. form unusual maerl beds in the North East Atlantic: the case study of L. fasciculatum (Lamarck) Foslie, 1898, in Brittany. An Aod-Les cahiers naturalistes de l’Observatoire marin 2(2):11–21
Peña V, Bárbara I, Grall J, Maggs CA, Hall-Spencer J (2014) The diversity of seaweeds on maerl in the NE Atlantic. Mar Biodivers 44:533–551
Peña V, Pardo C, López L, Carro B, Hernandez-Kantun J, Adey WH, Bárbara I, Barreiro R, Le Gall L (2015) Phymatolithon lusitanicum sp. nov.(Hapalidiales, Rhodophyta): the third most abundant maerl-forming species in the Atlantic Iberian Peninsula. Cryptogam Algol 36:429–459
Phillips LE, De Clerck O (2005) The terete and sub-terete members of the red algal tribe Amansieae (Ceramiales, Rhodomelaceae). Cryptogam Algol 26:5–33
Piñeiro-Corbeira C, Maggs CA, Rindi F, Bunker F, Baldock L, Díaz-Tapia P (2020) Molecular assessment of the tribes Streblocladieae and Polysiphonieae (Rhodomelaceae, Rhodophyta) in the British Isles reveals new records and species that require taxonomic revision. Cryptogam Algol 41:55–72
Qui-Minet ZN, Delaunay C, Grall J, Six C, Cariou T, Bohner O, Legrand E, Davoult D, Martin S (2018) The role of local environmental changes on maerl and its associated non-calcareous epiphytic flora in the Bay of Brest. Estuar, Coast Shelf Sci 208:140–152
Qui-Minet ZN, Coudret J, Davoult D, Grall J, Mendez-Sandin M, Cariou T, Martin S (2019) Combined effects of global climate change and nutrient enrichment on the physiology of three temperate maerl species. Ecol Evol 9:13787–13807
Qui-Minet ZN, Davoult D, Grall J, Martin S (2022) The relative contribution of fleshy epiphytic macroalgae to the production of temperate maerl (rhodolith) beds. Mar Ecol Prog Ser 693:69–82
R Development core team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL, Available at: https://www.R-project.org/. Accessed 2 Sept 2022
Rodríguez-Prieto C, Ballesteros E, Boisset F, Afonso-Carrillo J (2013) Guía de las macroalgas y fanerógamas marinas del Mediterráneo occidental. Ediciones Omega S.A., Barcelona
Rico J, Guiry M (1998) Life history and reproduction of Gelidium maggsiae sp. nov.(Rhodophyta, Gelidiales) from Ireland. Oceanogr Lit Rev 3:525
Saunders GW, Virginia Lehmkuhl* K (2005) Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in northern Europe. Eur J Phycol 40:293-312
Savoie AM, Saunders GW (2019) A molecular assessment of species diversity and generic boundaries in the red algal tribes Polysiphonieae and Streblocladieae (Rhodomelaceae, Rhodophyta) in Canada. Eur J Phycol 54:1–25
Sjøtun K, Husa V, Peña V (2008) Present distribution and possible vectors of introductions of the alga Heterosiphonia japonica (Ceramiales, Rhodophyta) in Europe. Aquat Invasions 3:377–394
Steentoft M, Irvine L, Farnham W (1995) Two terete species of Gracilaria and Gracilariopsis (Gracilariales, Rhodophyta) in Britain. Phycologia 34:113–127
Steinhagen S, Düsedau L, Weinberger F (2021) DNA barcoding of the German green supralittoral zone indicates the distribution and phenotypic plasticity of Blidingia species and reveals Blidingia cornuta sp. nov. Taxon 70:229–245
Tauran A, Dubreuil J, Guyonnet B, Grall J (2020) Impact of fishing gears and fishing intensities on maerl beds: an experimental approach. J Exp Mar Biol Ecol 533:151472
Verlaque M, Ruitton S, Mineur F, Boudouresque CF (2007) CIESM Atlas of exotic macrophytes in the Mediterranean Sea. Rapp Comm Int Mer Médit 38:14
Acknowledgements
The authors would like to thank the crew of the Albert-Lucas, M. Maguer and L. Pinsivy for sampling in the bay, as well as the crew of the Saint-Guénolé. Thanks are due to V. Peña and S. Connan for sharing their data. Thanks are due to the divers from the GMAP (Groupe Manche Atlantique de Plongée) and particularly P. Praud, U. Cadour, S. Carlo, J.C. Jézequel, and F. Ferellec. Thanks are due to M. Le Duff for reviewing the manuscript. The authors would like to thank the two anonymous reviewers for their valuable comments. The authors are indebted to J. Grall for his advices and the preliminary concept of the study.
Funding
This study was supported by the REBENT program.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
This article does not contain any studies with animals performed by any of the authors.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities. The study is compliant with the REBENT protocols.
Data availability
The datasets generated during and/or analyzed during the current study are available in the IUEM repository, https://www-iuem.univ-brest.fr/observatoire.
Author contribution
M.H. and T.B. conceived the ideas, collected the field data; M.H. analyzed the data with substantial contributions from T.B.; M.H. led the writing with contributions from T.B. All authors gave final approval for publication.
Additional information
Communicated by H. Hillebrand
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Helias, M., Burel, T. Maerl-associated macroalgae in the bay of Brest (Brittany, France). Mar. Biodivers. 53, 14 (2023). https://doi.org/10.1007/s12526-022-01322-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-022-01322-z