Insights into species diversity of associated crustose coralline algae (Corallinophycidae, Rhodophyta) with Atlantic European maerl beds using DNA barcoding
DOI:
https://doi.org/10.3989/ajbm.2459Keywords:
Brittany, COI-5P, Corallinales, crustose coralline algae, diversity, Galicia, Hapalidiales, Lithophyllum, Lithothamnion, maerl, Mesophyllum, morphology, Phymatolithon, reproduction, rhodolith, SEMAbstract
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.
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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
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