DOI: http://dx.doi.org/10.11646/phytotaxa.190.1.12

DNA barcoding allows the accurate assessment of European maerl diversity: a Proof-of-Concept study

Belén Carro, Lua Lopez, Viviana Peña, Ignacio Bárbara, Rodolfo Barreiro

Abstract


Two non-geniculate coralline red algae (Lithothamnion corallioides and Phymatolithon calcareum) are partially protected under the assumption that they are the main components of maerl beds in Atlantic Europe. However, what we know about the composition of maerl relies mainly on morphology-based identifications that are notoriously difficult due to a lack of diagnostic features, convergence, and widespread phenotypic plasticity. Now, this state of affairs can be improved with new alternatives that, unlike morphology, allow the unambiguous partition of a large number of rhodoliths into species regardless of their size, shape, and condition (fertile or sterile). Here, we report the first DNA barcoding assessment of the relative abundance of maerl-forming algae. The plastidial gene psbA was sequenced for 1140 rhodoliths from 15 maerl beds scattered along 2000 km from the British Isles to South Portugal; rhodoliths were randomly collected along linear transects to obtain quantitative estimates of species composition. Most (97%) of our collections belonged to three, rather than two, species that often appeared intermixed along a single transect. Lithothamnion corallioides and P. calcareum dominated in the British Isles and Brittany (NW France), but they were gradually replaced by Phymatolithon sp3 in Galicia (NW Spain) and became extremely rare in Algarve (S Portugal). Morphology (rhodolith size and shape, branch diameter, habit) varied considerably between and within beds but the three species converged to a remarkably similar habit when living in sympatry. Still, P. calcareum and L. corallioides seemed to perform best in Brittany while Phymatolithon sp3 produced the largest rhodoliths with thickest branches in Algarve. Altogether, our study shows that the replacement of species of maerl seen in northern latitudes continues to the south along the coasts of Iberia. It also serves as a proof-of-concept of the benefits of DNA barcoding for ecological and biogeographic research of these taxonomically challenging taxa.


Keywords


algae, Lithothamnion corallioides, Phymatolithon calcareum

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References


Adey, W.H. (1966) Distribution of saxicolous crustose corallines in the Northwestern North Atlantic. Journal of Phycology 2: 49–54.
http://dx.doi.org/10.1111/j.1529-8817.1966.tb04593.x

Adey, W.H. & Adey, P.J. (1973) Studies on the biosystematics and ecology of epilithic crustose Corallinaceae of the British Isles. British Phycological Journal 8: 343–407.
http://dx.doi.org/10.1080/00071617300650381

Adey, W.H. & McKibbin, D.L. (1970) Studies on the maerl species Phymatolithon calcareum (Pallas) nov. comb. and Lithothamnium coralloides Crouan in the Ría de Vigo. Botanica Marina 13: 100–106.
http://dx.doi.org/10.1515/botm.1970.13.2.100

Amado-Filho, G.M., Maneveldt, G.W., Manso, R., Marins-Rosa, B., Pacheco, M. & Guimarães, S. (2007) Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil. Ciencias Marinas 33: 399–410.

Bahía, R.G., Abrantes, D.P., Brasileiro, P.S., Pereira Filho, G.H. & Amado Filho, G.M. (2010) Rhodolith bed structure along a depth gradient on the northern coast of Bahía State, Brazil. Brazilian Journal of Oceanography 58: 232–327.
http://dx.doi.org/10.1590/s1679-87592010000400007

Barbera, C., Bordehore, C., Borg, J.A., Glémarec, M., Grall, J., Hall-Spencer, J.M., Huz, C.D.L., Lanfranco, E., Lastra, M., Moore, P.G., Mora, J., Pita, M.E., Ramos-Esplá, A.A., Rizzo, M., Sánchez-Mata, A., Seva, A., Schembri, P.J. & Valle, C. (2003) Conservation and management of northeast Atlantic and Mediterranean maerl beds. Aquatic Conservation: Marine and Freshwater Ecosystems 13: S65–S76.
http://dx.doi.org/10.1002/aqc.569

Basso, D. (1996) Adaptive strategies and convergent morphologies in some Mediterranean coralline algae. Bollettino della Societa Paleontologica Italiana 3: 1–8.

Basso, D., Nalin, R. & Campbell, N. (2009) Shallow-water Sporolithon rhodoliths from North Island (New Zealand). Palaios 24: 92–103.

Birkett, D.A., Maggs, C.A. & Dring, M.J. (1998) Maerl. An overview of dynamics and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project), Scotland, 116 pp.

Bittner, L., Halary, S., Payri, C., Cruaud, C., Reviers, B.d., Lopez, P. & Bapteste, E. (2010) Some considerations for analyzing biodiversity using integrative metagenomics and gene networks. Biology Direct 5: 47.
http://dx.doi.org/10.1186/1745-6150-5-47

Bittner, L., Payri, C.E., Maneveldt, G.W., Couloux, A., Cruaud, C., de Reviers, B. & Le Gall, L. (2011) Evolutionary history of the Corallinales (Corallinophycidae, Rhodophyta) inferred from nuclear, plastidial and mitochondrial genomes. Molecular Phylogenetics and Evolution 61: 697–713.
http://dx.doi.org/10.1016/j.ympev.2011.07.019

Bosellini, A. & Ginsburg, R.N. (1971) Form and internal structure of recent algal nodules (Rhodolites) from Bermuda. Journal of Geology 79: 669–682.
http://dx.doi.org/10.1086/627697

Bosence, D.W.J. (1976) Ecological studies on two unattached coralline algae from western Ireland. Palaeontology 19: 365–395.

Bosence, D.W.J. (1983) The Occurrence and Ecology of Recent Rhodoliths — A Review. In: Peryt, T.M. (Ed.) Coated Grains. Springer-Verlag, Berlin Heidelberg, pp. 225–242.

Bosence, D.W.J. (1991) Coralline algae: mineralization, taxonomy and palaeoecology. In: Riding, R. (Ed.) Calcareous Algae and Stromatolites. Springer-Verlag, Berlin Heidelberg, pp. 98–113.
http://dx.doi.org/10.1007/978-3-642-52335-9_5

Cabioch, J. (1966) Contribution à l'étude morphologique, anatomique et systématique de deux Mélobésiées: Lithothamnium calcareum (Pallas) Areschoug et Lithothamniun corallioides Crouan. Botanica Marina 9: 33–53.
http://dx.doi.org/10.1515/botm.1966.9.1-2.33

Crouan, P. & Crouan, H. (1867) Florule du Finistére. Klincksieck, F. & Lefournier, J. B. & A., Paris & Brest, 262 pp.

Foster, M., Riosmena-Rodríguez, R., Steller, D.L. & Woelkerling, W.J. (1997) Living rhodolith beds in the Gulf of California and their implications for paleoenvironmental interpretation. In: Johnson, M.E. & Ledesma-Vázquez, J. (Eds.) Pliocene Carbonates and Related Facies Flanking the Gulf of California, Baja California, Mexico. The Geological Society of America, Boulder, Colorado, pp. 127–139.

Gagnon, P., Matheson, K. & Stapleton, M. (2012) Variation in rhodolith morphology and biogenic potential of newly discovered rhodolith beds in Newfoundland and Labrador (Canada). Botanica Marina 55: 85–99.
http://dx.doi.org/10.1515/bot-2011-0064

Goldberg, N. (2006) Age estimates and description of rhodoliths from Esperance Bay, Western Australia. Journal of the Marine Biological Association of the United Kingdom 86: 1291–1296.

Graham, D. & Midgley, N. (2000) Graphical representation of particle shape using triangular diagrams: an Excel spreadsheet method. Earth Surface Processes and Landforms 25: 1473–1477.

Grall, J. & Hall-Spencer, J.M. (2003) Problems facing maerl conservation in Brittany. Aquatic Conservation: Marine and Freshwater Ecosystems 13: S55–S64.
http://dx.doi.org/10.1002/aqc.568

Hall-Spencer, J.M., Kelly, J. & Maggs, C.A. (2010) Background document for maërl beds. In: OSPAR Commission Biodiversity Series. OSPAR Commission, London, UK, pp. 1–36.

Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 313–321.
http://dx.doi.org/10.1098/rspb.2002.2218

Hebert, P.D.N., Ratnasingham, S. & de Waard, J.R. (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B-Biological Sciences 270: S96–S99.

Hind, K.R. & Saunders, G.W. (2013) A Molecular Phylogenetic Study of the Tribe Corallineae (Corallinales, Rhodophyta) with an Assessment of Genus-Level Taxonomic Features and Descriptions of Novel Genera. Journal of Phycology 49: 103–114.
http://dx.doi.org/10.1111/jpy.12019

Irvine, L.M. & Chamberlain, Y.M. (1994) Seaweeds of the British Isles: Volume 1: Rhodophyta, Part 2B: Corallinales, Hildenbrandiales. The Natural History Museum, London, 276 pp.

Kjellman, F.R. (1883) The algae of the Artic Sea. A survey of the species, together with an exposition of the general characters and the development of the flora. Kungliga Svenska Vetenskapsakademiens Handlingar 20: 1–351.

Maggs, C.A., Verbruggen, H. & De Clerck, O. (2007) Molecular systematics of red algae: building future structures on firm foundations. In: Brodie, J. & Lewis, J. (eds) Unravelling the algae: the past, present, and future of algal systematics. Taylor and Francis, Boca Raton, pp. 103–121.

Marrack, E. (1999) The relationship between water motion and living rhodolith beds in the Southwestern Gulf of California, Mexico. Palaios 14: 159–171.

Miranda, F. (1934) Materiales para una flora marina de las rías bajas gallegas. Boletín de la Real Sociedad Española de Historia Natural, Sección Biología 34: 165–180.

Pardo, C., López, L., Peña, V., Hernández-Kantún, J., Le Gall, L., Bárbara, I. & Barreiro, R. (submitted) A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR area. PLoSONE.

Peña, V. & Bárbara, I. (2004) Diferenciación morfológica y anatómica entre Lithothamnion corallioides y Phymatolithon calcareum (Corallinales, Rhodophyta) en dos bancos de maërl de la Ría de Arousa (N. O. Península Ibérica). Anales de Biología 26: 21–27.

Peña, V. & Bárbara, I. (2008) Biological importance of an Atlantic European maerl bed off Benencia Island (northwest Iberian Peninsula). Botanica Marina 51: 493–505.
http://dx.doi.org/10.1515/bot.2008.057

Peña, V. & Bárbara, I. (2009) Distribution of the Galician maerl beds and their shape classes (Atlantic Iberian Peninsula): proposal of areas in future conservation actions. Cahiers de Biologie Marine 50: 353–368.

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. Botanica Marina 56: 481–493.
http://dx.doi.org/10.1515/bot-2013-0083

Peña, V., Bárbara, I., Berecibar, E. & Santos, R. (2009) Present distribution of maerl beds in the Atlantic Iberian Peninsula. Museologia Scientifica e Naturalistica volumen speciale IFAA: 46.

Peña, V., Bárbara, I., Grall, J., Maggs, C.A. & Hall-Spencer, J.M. (2014a) The diversity of seaweeds on maerl in the NE Atlantic. Marine Biodiversity 44(4): 533–551 .

Peña, V., Hernández-Kantún, J., Grall, J., Pardo, C., López, L., Bárbara, I., Le Gall, L. & Barreiro, R. (2014b) Detection of gametophytes in the maerl-forming species Phymatolithon calcareum (Melobesioideae, Corallinales) assessed by DNA barcoding. Cryptogamie, Algologie 35: 15–25.
http://dx.doi.org/10.7872/crya.v35.iss1.2014.15

Pons, J., Barraclough, T., Gómez-Zurita, J., Cardoso, A., Duran, D., Hazell, S., Kamoun, S., Sumlin, W. & Vogler, A. (2006) Sequence-Based Species Delimitation for the DNA Taxonomy of Undescribed Insects. Systematic Biology 55: 595–609.

Prager, E.J. & Ginsburg, R.N. (1989) Carbonate nodule growth on Florida´s outer shelf and its implications for fossil interpretations. Palaios 4: 310–317.

Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.
http://dx.doi.org/10.1111/j.1365-294x.2011.05239.x

Robba, L., Russell, S.J., Barker, G. L. & Brodie, J. (2006) Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). American Journal of Botany 93: 1101–1108.
http://dx.doi.org/10.3732/ajb.93.8.1101

Rosas-Alquicira, E.F., Riosmena-Rodríguez, R., Couto, R.P. & Neto, A.I. (2009) New additions to the Azorean algal flora, with ecological observations on rhodolith formations. Cahiers de Biologie Marine 50: 143–151.

Saunders, G.W. (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical Transactions of the Royal Society B-Biological Sciences 360: 1879–1888.
http://dx.doi.org/10.1098/rstb.2005.1719

Saunders, G.W. & McDevit, D.C. (2012) Methods for DNA barcoding photosynthetic protists emphasizing the macroalgae and diatoms. In: Kress, W.J. & Erickson, D.L. (Eds.) DNA Barcodes: Methods and Protocols. Humana Press, Totowa, NJ, pp. 207–222.

Saunders, G.W. & Moore, T.E. (2013) Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28: 31–43.

http://dx.doi.org/10.4490/algae.2013.28.1.031

Seoane-Camba, J.A. & Campo Sancho, J. (1968) Resultados de una primera exploración algológica con escafandra autónoma en la Ría de Vigo. Publicaciones Técnicas de la Junta de Estudios de Pesca 7: 333–344.

Sneed, E.D. & Folk, R.L. (1958) Pebbles in the lower Colorador river, Texas. A study in particle morphogenesis. Journal of Geology 66: 114–150.

Steller, D.L. & Foster, M.S. (1995) Environmental factors influencing distribution and morphology of rhodoliths in Bahía Concepción, B.C.S., México. Journal of Experimental Marine Biology and Ecology 194: 201–212.
http://dx.doi.org/10.1016/0022-0981(95)00086-0

Teichert, S., Woelkerling, W., Rüggeberg, A., Wisshak, M., Piepenburg, D., Meyerhöfer, M., Form, A., Büdenbender, J. & Freiwald, A. (2012) Rhodolith beds (Corallinales, Rhodophyta) and their physical and biological environment at 80°31′N in Nordkappbukta (Nordaustlandet, Svalbard Archipelago, Norway). Phycologia 51: 371–390.
http://dx.doi.org/10.2216/11-76.1

Unger, F. (1858) Beiträge zur näheren Kenntniss des Leithakalkes, namentlich der vegetabilischen Einschlüsse und der Bildungsgeschichte desselben. Denkschriften der Kaiserlichen Akademie der Wissenschaften [Wein], Mathematisch-naturwissenschaftliche Klasse 14: 13–35.

Walker, R.H., Brodie, J., Russell, S., Irvine, L.M. & Orfanidis, S. (2009) Biodiversity of Coralline algae in the Northeastern Atlantic including Corallina caespitosa sp. nov. (Corallinoideae, Rhodophyta). Journal of Phycology 45: 287–297.
http://dx.doi.org/10.1111/j.1529-8817.2008.00637.x

Yoon, H.S., Hackett, J.D. & Bhattacharya, D. (2002) A single origin of the peridinin- and fucoxanthin- containing plastids in dinoflagellates through tertiary endosymbiosis. PNAS 99: 11724–11729.
http://dx.doi.org/10.1073/pnas.172234799


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