Insights into species diversity of associated crustose coralline algae (Corallinophycidae, Rhodophyta) with Atlantic European maerl beds using DNA barcoding

Authors

DOI:

https://doi.org/10.3989/ajbm.2459

Keywords:

Brittany, COI-5P, Corallinales, crustose coralline algae, diversity, Galicia, Hapalidiales, Lithophyllum, Lithothamnion, maerl, Mesophyllum, morphology, Phymatolithon, reproduction, rhodolith, SEM

Abstract


DNA barcoding in combination with morpho-anatomical analysis was applied to study the diversity of crustose coralline algae associated to two maerl beds from two protected Atlantic European areas from Brittany and Galicia —France and Spain, respectively—. Given the records of gametophytes of the maerl species Phymatolithon calcareum under crustose growth-forms, and that associated crustose coralline algae appear to be involved in the recruitment of new maerl plants, we compared the species composition between the associated crustose coralline algae to Breton and Galician maerl beds with the maerl species identified in these beds in previous DNA barcoding surveys. Our molecular results revealed higher species diversity in associated crustose coralline algae than in maerl-forming species. Nine taxa of crustose coralline algae were found in both study areas: four in Brittany and five in Galicia. Three species from Brittany were identified as Phymatolithon calcareum, Phymatolithon lamii, and Lithophyllum hibernicum. The remaining six ones were assigned to the genera Phymatolithon and Mesophyllum, along with Lithothamnion and Lithophyllum. Morpho-anatomical examination of diagnostic characters corroborated our molecular identification. Our results showed that the most representative genus of crustose coralline algae in Brittany was Phymatolithon, while in Galicia was Mesophyllum. In Brittany, Phymatolithon calcareum was found under both growth-forms, maerl and crustose coralline algae, the latter assigned to the gametophyte stage by the presence of uniporate conceptacles. The recruitment of new maerl plants involving associated crustose coralline algae with maerl beds may occur, but only we can affirm it for Phymatolithon calcareum in Brittany. By contrast, the different species composition between both growth-forms in the Galician maerl beds would indicate that the fragmentation of own free-living maerl species appears to be the most common propagation mechanism.

Downloads

Download data is not yet available.

References

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. https://doi.org/10.1515/botm.1970.13.2.100

Adey W., Halfar J., Humphreys A., Suskiewicz T., Belanger D., Gagnon P. & Fox M. 2015. Subartic rhodolith beds promote longevity of crustose coralline algal buildups and their climate archiving potential. Palaios 30: 281-293. https://doi.org/10.2110/palo.2014.075

Basso D., Nalin R. & Nelson C. 2009. Shallow-water Sporolithon rhodoliths from North Island (New Zealand). Palaios 24: 92-103. https://doi.org/10.2110/palo.2008.p08-048r

Bosence D.W. 1976. Ecological studies on two unattached coralline algae from western Ireland. Palaeontology 19: 365-395.

Cabioch J. 1969. Les fonds de maerl de la Baie de Morlaix et leur peuplement végétal. Cahiers de Biologie Marine 10: 139-161.

Cabioch J. 1970. Le maërl des côtes de Bretagne et le problème de sa survie. Penn ar Bed 7: 421-429.

Carro B., López L., Pe-a V., Bárbara I. & Barreiro R. 2014. DNA barcoding allows the accurate assessment of European maerl diversity: a proof-of-concept study. Phytotaxa 190: 176-189. https://doi.org/10.11646/phytotaxa.190.1.12

Chamberlain Y.M. 1991. Observations on Phymatolithon lamii (Lemoine) Y. Chamberlain comb. nov. (Rhodophyta, Corallinales) in the British Isles with an assessment of its relationship to P. rugulosum, Lithophyllum lamii and L. melobesioides. British Phycological Journal 26: 219-233. https://doi.org/10.1080/00071619100650201

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772-772. https://doi.org/10.1038/nmeth.2109 PMid:22847109 PMCid:PMC4594756

Freiwald A. 1995. Sedimentological and biological aspects in the formation of branched rhodoliths in northern Norway. Beiträge zur Paläontologie 20: 7-19.

Guiry M.D. & Guiry G.M. [2016]. AlgaeBase. Galway, Ireland. Website: http://www.algaebase.org [Accessed: 4 November 2016].

Hall-Spencer J.M., Kelly J. & Maggs C.A. 2010. Background document for maërl beds. OSPAR Commission Biodiversity Series, OSPAR Commission: 1-36. PMid:21141665

Hernández-Kantún J.J., Rindi F., Adey W.H., Heesch S., Pe-a V., Le Gall L. & Gabrielson P.W. 2015a. Sequencing type material resolves the identity and distribution of the generitype Lithophyllum incrustans, and related European species L. hibernicum and L. bathyporum (Corallinales, Rhodophyta). Journal of Phycology 51: 791–807. https://doi.org/10.1111/jpy.12319 PMid:26986797

Hernández-Kantún J.J., Riosmena-Rodríguez R., Hall-Spencer J.M., Pe-a V., Maggs C.A. & Rindi F. 2015b. Phylogenetic analysis of rhodolith formation in the Corallinales (Rhodophyta). European Journal of Phycology 50: 46-61. https://doi.org/10.1080/09670262.2014.984347

Hernández-Kantún J.J., Riosmena-Rodríguez R., Adey W.H. & Rindi F. 2014. Analysis of the cox2?3 spacer region for population diversity and taxonomic implications in rhodolith-forming species (Rhodophyta: Corallinales). Phytotaxa 190: 331-354. https://doi.org/10.11646/phytotaxa.190.1.20

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

Lemoine M.P. 1910. Répartition et mode de vie du Maërl (Lithothamnium calcareum) aux environs de Concarneau (Finistère). Annales de Institut Océanographique. Fondation Albert Ier, Prince de Monaco 1: 1-28.

Maggs C.A. 1983. A phenological study of the epiflora of two maerl beds in Galway Bay. PhD thesis, National University of Ireland, Galway.

Mendoza M.L. & Cabioch J. 1998. Étude comparée de la reproduction de Phymatolithon calcareum (Pallas) Adey & McKibbin et Lithothamnion corallioides (P. & H. Crouan) P. & H. Crouan (Corallinales, Rhodophyta), et reconsidérations sur le définition des genres. Canadian Journal of Botany 76: 1433-1445. https://doi.org/10.1139/b98-116

Pardo C., López L., Pe-a V., Hernández-Kantún J., Le Gall L., Bárbara I. & Barreiro R. 2014. A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area. PLoS ONE 9: e104073. https://doi.org/10.1371/journal.pone.0104073 PMid:25111057 PMCid:PMC4128821

Pardo C., Pe-a V., Barreiro R. & Bárbara I. 2015. A molecular and morphological study of Corallina sensu lato (Corallinales, Rhodophyta) in the Atlantic Iberian Peninsula. Cryptogamie, Algologie 36: 31-54. https://doi.org/10.7872/crya.v36.iss1.2015.31

Pe-a 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.

Pe-a 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.

Pe-a V., Adey W.H., Riosmena-Rodríguez R., Jung M.-Y., Afonso-Carrillo J., Choi H.G. & Bárbara I. 2011. Mesophyllum sphaericum sp. nov. (Corallinales, Rhodophyta): a new maërl-forming species from the northeast Atlantic. Journal of Phycology 47: 911-927. https://doi.org/10.1111/j.1529-8817.2011.01015.x PMid:27020026

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

Peña V., De Clerck O., Afonso-Carrillo J., Ballesteros E., Bárbara I., Barreiro R. & Le Gall L. 2015a. An integrative systematic approach to species diversity and distribution in the genus Mesophyllum (Corallinales, Rhodophyta) in Atlantic and Mediterranean Europe. European Journal of Phycology 50: 20-36. https://doi.org/10.1080/09670262.2014.981294

Pe-a V., Pardo C., López L., Carro B., Hernández-Kantún J., Adey W.H., Bárbara I., Barreiro R. & Le Gall L. 2015b. Phymatolithon lusitanicum sp. nov. (Hapalidiales, Rhodophyta): the third most abundant maerl-forming species in the Atlantic Iberian Peninsula. Cryptogamie, Algologie 36: 1-31.

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. https://doi.org/10.1098/rstb.2005.1719 PMid:16214745 PMCid:PMC1609223

Saunders G.W. & McDevit D.C. 2012. Methods for DNA barcoding photosynthetic protists emphasizing the macroalgae and diatoms. Methods in Molecular Biology 858: 207-222. https://doi.org/10.1007/978-1-61779-591-6_10 PMid:22684958

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729. https://doi.org/10.1093/molbev/mst197 PMid:24132122 PMCid:PMC3840312

Thiers B. [2016]. Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden's Virtual Herbarium. Website: http://sweetgum.nybg.org/science/ih/ [Accessed: 4 November 2016].

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. https://doi.org/10.1111/j.1529-8817.2008.00637.x PMid:27033664

Woelkerling W.J. 1988. The Coralline Red Algae: An Analysis of the Genera and Subfamilies of Nongeniculate Corallinaceae. Oxford University Press, London.

Woelkerling W.J. & Irvine L.M. 1986. The typification and status of Phymatolithon (Corallinaceae, Rhodophyta). British Phycological Journal 21: 55-80. https://doi.org/10.1080/00071618600650071

Published

2017-12-30

How to Cite

Pardo, C., Bárbara, I., Barreiro, R., & Peña, V. (2017). Insights into species diversity of associated crustose coralline algae (Corallinophycidae, Rhodophyta) with Atlantic European maerl beds using DNA barcoding. Anales Del Jardín Botánico De Madrid, 74(2), e059. https://doi.org/10.3989/ajbm.2459

Issue

Section

Articles

Most read articles by the same author(s)

  • Ignacio Bárbara, Javier Cremades, Grateloupia lanceola versus Grateloupia turuturu (Gigartinales, Rhodophyta): en la Península Ibérica , Anales del Jardín Botánico de Madrid: Vol. 61 No. 2 (2004)
  • María Dalila Espíritu Santo, Paloma Cubas, Mario F. Lousá, Cristina Pardo, J. Carlos Costa, Ulex parviflorus sensu lato (Genisteae, Leguminosae) from Central Portugal , Anales del Jardín Botánico de Madrid: Vol. 55 No. 1 (1997)
  • Ignacio Bárbara, Marysol Vilas Rama, Javier Cremades, M.ª Carmen López Rodríguez, Graciela Paz Bermúdez, Francisco Pando, Miguel Oltra, Ginés López González, Vicente J. Aran Redó, Gonzalo Mateo Sanz, Antoni Sánchez-Cuxart, José Luis Fernández-Alonso, Santiago Castroviejo, Paulo Cardoso da Silveira, Joao Domingues de Almeida, Pedro Sánchez Gómez, Miguel Ángel Carrión Vilches, Antonio Hernández González, Juan Bautista Vera Pérez, Luis Serra Laliga, Joan Pérez Botella, Juanjo Izquierdo, Marcos Perille Seoane, Manuel Pimentel Pereira, David Romero Pedreira, Elvira Sahuquillo Balbuena, Enrique Rico, Joaquín Ascaso, Lorenzo Ortas, Notas breves , Anales del Jardín Botánico de Madrid: Vol. 59 No. 1 (2001)
  • Javier Cremades, Ignacio Bárbara, Alberto Granja, Alfredo José Veiga, Alberto Santolaria, José María Gorostiaga, Antonio Secilla, Isabel Díez, María Luisa Castro, Ana Soliño, Luis Freiré, Gregorio Aragón Rubio, Isabel Martínez Moreno, María José Sánchez-Biezma Serrano, Graciela Paz Bermúdez, Regina Carballal Durán, María Eugenia López de Silanes Vázquez, José Antonio Navarro Cano, Carlos Barcia González, Enrique Sánchez Gullón, José Antonio Ortega Expósito, Miguel Allué, Juan José Lastra Menéndez, Matías Mayor López, Vicente Pastor, José Luis Carretero, Mario Sanz Elorza, José Vicente Ferrández Palacio, Josep Antoni Conesa Mor, Mario Sanz Elorza, Mikel Lorda López, José Mario Arguelles, Alejandro Díez Riol, Antonio Guillen, Manuel Laínz, Fragmenta Chorologica Occidentale , Anales del Jardín Botánico de Madrid: Vol. 55 No. 2 (1997)
  • Alfredo J. Veiga, Javier Cremades, Ignacio Bárbara, Ginés López González, Santiago Silvestre, Antonio Guillen Uterino, Manuel Laínz, S.J., Juan José Lastra Menéndez, Matías Mayor, Santos Cirujano, Leopoldo Medina, Gerardo Stübing, Juan Bautista Peris, Carlos J. Martín Blanco, María A. Carrasco, Gonzalo Mateo, Manuel Benito Crespo, Hamilton Beltrán Santiago, Antonio Galán de Mera, Juan Bautista Peris, Amparo Olivares, Joan Martin, F. Javier Fernández Casas, Pablo García Murillo, Arturo Sousa, Santos Llatas Quiros, José Alfredo Vicente Orellana, Antonio Galán de Mera, Francisco José González, Pilar Candau, Julio A. Camargo, Notas Breves , Anales del Jardín Botánico de Madrid: Vol. 55 No. 1 (1997)
  • Silvia Calvo, Ignacio Barbara, Juan Luis Menéndez Valderrey, José Manuel Rico Ordás, Carlos J. Martín Blanco, María A. Carrasco, Pedro Sánchez Gómez, José Sebastían Carrión, Miguel Ángel Carrión Vilches, J. A. Alejandre, Modesto Luceño, J. Martín Martín, Carlos Aedo, Joao Marcelo Alvarenga Braga, Pablo Vargas, Félix Muñoz Garmendia, Jochen Hess, Joachim Kadereit, Omar Fiz, Virginia Valcarcel, Jorge Martínez, Ernst Vitek, Christoph Dobes, Francisco Gómiz García, Paulo C. Silveira, Notas Breves , Anales del Jardín Botánico de Madrid: Vol. 58 No. 2 (2000)
  • Javier Cremades, Ignacio Bárbara, Alfredo José Veiga, M.ª Carmen López Rodríguez, Antonia D. Asencio, Marina Aboal, César López Várela, Javier Dosil, Silvia Calvo, Viviana Peña, Mª Carmen López Rodríguez, Jaime Bernardo Blanco-Dios, Marcos Lago, María Luisa Castro, José Rodríguez Vázquez, Teresa Agreda Cabo, Marina Fernández Toirán, Mª Inmaculada López-Prada, Simón Fos, Eva Barreno, Fina Méndez Anta, Montserrat Freiré Dopazo, Aida García Molares, Sergio Pérez Ortega, David Gómez, Fernando Fernández Mendoza, Fragmenta chorologica occidentalia, Algae 7776-7892; Fungi, 7893-8141; Lichenes, 8142-8248; Bryophyta, 8249-8391 , Anales del Jardín Botánico de Madrid: Vol. 59 No. 2 (2001)
<< < 1 2