DNA Barcode-Assisted Inventory of the Marine Macroalgae from the Azores, Including New Records
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling
2.2. DNA Extraction, PCR Amplification, and Sequencing
2.3. Compilation of Publicly Available Sequences for the Azores
2.4. Evaluation of Native Status in the Azores
3. Results
3.1. DNA-Barcoding of Newly Generated Sequences
3.2. Analyses of Publicly Available Sequences
3.3. DNA-Based Species Inventory
3.4. Updates to the Azorean Marine Flora
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Taxa | Genetic Marker | GenBank Accession Numbers | Top Matches | Comments |
---|---|---|---|---|
Ochrophyta | ||||
Colpomenia sinuosa | rbcL * | OR944643 OR944644 | Colpomenia sinuosa, 99.39% similarity, Hawaiian Islands (AB578988) and Korea (AY398468) | |
UPA * | OR961485 | Colpomenia sinuosa, 99.74% similarity, China (OR094252) and Hawaiian Islands (EF426596) | ||
Fucus spiralis | cox1 | OR944632 | Fucus spiralis, 100% similarity, the Atlantic USA coast (EU646722) Fucus vesiculosus, 100% similarity, Norway (MN184303) | Phylogeny reconstructions based on complete mitochondrion and chloroplast genomes support the recognition of Fucus spiralis var. vesiculosus [91], although this taxon is not currently recognized in Algaebase. Until further taxonomic decisions, and since the presence of F. vesiculosus in the Azores is not confirmed by morphological studies [7], F. spiralis is maintained as the identity of the Azorean voucher. |
UPA * | OR961486 OR961487 OR961488 | Fucus spiralis, 99.75% similarity, the Pacific USA coast (MG922855) Fucus vesiculosus, 99.75% similarity, Portugal (FM957154) | ||
Padina gymnospora | UPA * | OR961489 | Padina gymnospora, 99.20% similarity, Hawaiian Islands (EF426588) | UPA sequences from Padina pavonica, the only Padina species currently reported to the Azores, are not available for comparison. |
Scytosiphon lomentaria | UPA * | OR961490 | Scytosiphon promiscuous, 100% similarity, Japan (MK107984) Hapterophycus canaliculatus, 100% similarity, Korea (MF591718) Petalonia binghamiae (as Endarachne binghamiae), 100% similarity, Korea (MF460360) Scytosiphon lomentaria, 100% similarity, China (MK798154) Petalonia fascia, 100% similarity, the Atlantic USA coast (KF367780) and China (KC782886) | Phylogeny reconstructions based on a complete chloroplast genome show that Scytosiphon promiscuus and Petalonia binghamiae are different taxa [92], though UPA sequences retrieved from their complete chloroplast genome are 100% similar. |
Rhodophyta | ||||
Amphiroa beauvoisii | cox1 * | OR944633 OR944634 OR944635 OR944636 | Amphiroa beauvoisii, 100% similarity, Brazil (MG521348) | Phylogenetic reconstructions based on four genetic markers indicate that Amphiroa beauvoisii is a species complex [87], with the Azorean vouchers nested in “clade 2”. |
UPA * | OR961491 OR961492 | Amphiroa beauvoisii, 100% similarity, Brazil (MG521307) and the Atlantic USA coast (KF367784) | ||
Gelidium microdon | rbcL * | OR944645 | Gelidium microdon, 100% similarity, the Atlantic Spanish coast (KT920271) | |
UPA *+ | OR961493 | This is the first UPA sequence for Gelidium microdon | ||
Hypnea musciformis | cox1 * | OR944637 OR944638 | Hypnea musciformis, 99.85% similarity, Tunisia (MG030775) and Italy (MF597663) | A sequence from the complete chloroplast genome generated from a topotype of Hypnea musciformis was used for comparison (OL964154; [93]). |
rbcL * | OR944646 | Hypnea musciformis, 99.93% similarity, Italy (OL964154), France (EU346011), and the Mediterranean Spanish coast (KT428787) | ||
UPA * | OR961494 | Hypnea musciformis, 100% similarity, Italy (OL964154) and the Atlantic USA coast (KJ202096) | ||
Jania pedunculata var. adhaerens | cox1 * | OR944639 | Jania sp., 100% similarity, the Indian South African coast (LC071780) Jania adhaerens, 99.85% similarity, China (OP168510) | Based on the lectotype, Jania pedunculata var. adhaerens should be referred to as a variety rather than a distinct species [52]. |
UPA *+ | OR961495 | This is the first UPA sequence for Jania pedunculata var. adhaerens | ||
Jania verrucosa | cox1 * | OR944640 | Jania verrucosa, 98.95% similarity, the Indian South African coast (LC071781) | Although the similarity between cox1 sequences was slightly beyond 99%, this match was used to discriminate the species due to the higher similarity observed between the rbcL sequences. |
rbcL * | OR944647 | Jania verrucosa, 99.89% similarity, New Zealand (KM369140) | ||
UPA *+ | OR961496 | This is the first UPA sequence for Jania verrucosa | ||
Laurencia pyramidalis | rbcL | OR944648 | Laurencia pyramidalis, 100% similarity, the Atlantic France (FJ785316), the Canary Islands (KF492791), the Azores (KF492787), and the Mediterranean Turkish coast (MZ153331) | |
UPA *+ | OR961497 | This is the first UPA sequence for Laurencia pyramidalis | ||
Lomentaria articulata | cox1 * | OR944641 | Lomentaria articulata, 100% similarity, the Atlantic French coast (KJ960811) | |
UPA *+ | OR961498 | This is the first UPA sequence for Lomentaria articulata | ||
Chlorophyta | ||||
Ulva australis | tufA * | OR944649 | Ulva australis, 100% similarity, the Atlantic French coast (MT160640), Italy (LR732070), the Netherlands (MZ272366), and Australia (MK125443) Ulva pertusa, 100% similarity, China (MN853875) | |
Ulva compressa | tufA * | OR944650 | Ulva compressa, 99.85% similarity, Australia (JN029285) | |
Ulva lacinulata | tufA * | OR944651 OR944652 | Ulva lacinulata, 100% similarity, Croatia (MW543061) and Portugal (MT160657) U. laetevirens, 100% similarity, Italy (MF544109), Tunisia (MF614791), and Korea (MT625105) | A sequence from the complete chloroplast genome generated from the lectotype of Ulva lacinulata was used for comparison (MW543061; [83]). |
Appendix B
Taxa | Genetic Marker | GenBank/ BOLD Accession Numbers | Top Matches | Comments |
---|---|---|---|---|
Ochrophyta | ||||
Colpomenia sinuosa | cox1 | PHAZO004-10 PHAZO117-10 PHAZO118-10 PHAZO119-10 PHAZO203-10 PHAZO204-10 | Colpomenia sinuosa, 99.6–100% similarity, Australia (MZ054832) | |
Cystoseira pustulata | cox1 | OL434655 (as Cystoseira pustulata) PHAZO043-10 (as Cystoseira compressa) | Cystoseira pustulata, 100% similarity, the Canary Islands (OK480304), the Azores (MF768044), and the Mediterranean Spanish coast (MF768042) | |
Fucus spiralis | cox1 | PHAZO060-10 PHAZO062-10 PHAZO063-10 | Fucus spiralis, 100% similarity, the Atlantic USA coast (EU646722) Fucus vesiculosus, 100% similarity, Norway (MN184303) | Phylogeny reconstructions based on complete mitochondrion and chloroplast genomes support the recognition of Fucus spiralis var. vesiculosus [91], although this taxon is not currently recognized in Algaebase. Until further taxonomic decisions, and since the presence of F. vesiculosus in the Azores is not confirmed by morphological studies [7], F. spiralis is maintained as the identity of the Azorean voucher. |
Gongolaria abies-marina | cox1 | PHAZO156-10 (as Cystoseira abies-marina) | Gongolaria abies-marina, 100% similarity, Azores (OK480429) | |
Halopteris filicina | cox1 | PHAZO003-10 PHAZO005-10 PHAZO008-10 PHAZO041-10 PHAZO042-10 PHAZO153-10 | Halopteris filicina, 99.8% similarity, Mediterranean French coast (EU579868) | |
Halopteris scoparia | LSU | OL434652 | Halopteris scoparia, 99.2% similarity, Tunisia (OK646025) | |
Petalonia binghamiae | cox1 | PHAZO002-10 (as Petalonia cf. fascia) | Petalonia binghamiae, 100% similarity, China (MF374731; as Endarachne binghamiae). | |
Sargassum cymosum | cox1 | OL434657 PHAZO044-10 PHAZO045-10 PHAZO116-10 (as Sargassum sp.) | Sargassum natans, 100% similarity, Curaçao (OM460646), from the Northwestern Atlantic Ocean and the Caribbean Sea (KY084907—KY084908, KY084912 Sargassum fluitans, 100% similarity, from the Gulf of Mexico (MT470904) | Phylogenetic reconstructions based on cox1, ITS-2, and rbcL [94] indicate that both species should be regarded as synonyms of S. cymosum. This name is used despite the lack of a formal amendment to S. cymosum since the species is reported to the Azores [7], unlike S. natans and S. fluitans. |
Scytosiphon lomentaria | cox1 | PHAZO060-10 PHAZO062-10 PHAZO063-10 | Scytosiphon lomentaria, 99.8–100% similarity, Argentina (ON568311) | |
Zonaria tournefortii | cox1 | OL434658 | Zonaria tournefortii, 100% similarity, the Canary Island (MW224392) and the Atlantic USA coast (KF367749) | |
Rhodophyta | ||||
Asparagopsis armata | cox1 | OL434653 | Asparagopsis armata, 100% similarity, the Atlantic French coast (KJ960344) and the UK (AB774223) | |
Asparagopsis taxiformis | cox1 | OL434654 | Asparagopsis taxiformis, 100% similarity, Italy (KJ398158) and the Mediterranean Spanish coast (AB774217) | |
Corallina berteroi | cox1 * | HQ919507 | Corallina caespitosa, 100% similarity, the Atlantic Spanish coast (KF460944) | Reappraisal of Corallina species based on type material [95] suggested that the cosmopolitan species C. caespitosa should be referred to as C. berteroi. |
HQ919508 | Corallina caespitosa, 100% similarity, the Atlantic Spanish coast (KF460946) and the Atlantic French coast (KJ960596) | |||
HQ919502 HQ919503 HQ919504 HQ919505 HQ919506 HQ919509 HQ919510 HQ919511 | Corallina caespitosa, 99.2–99.6% similarity, the Azores (KP834357) | |||
Olokunia boudouresquei | rbcL | EU349143 (as Cruoriopsis crucialis) | Olokunia boudouresquei, 100% similarity, New Zealand (KC998949; as Peyssonnelia boudouresquei) | This sequence is reported as included in Krayesky et al. [60], but no reference to the sequence is found in this article. |
Osmundea pinnatifida | rbcL | KU647694/ REDEU882-13 | Osmundea pinnatifida, 100% similarity, Ireland (AF281875) | |
Pterocladiella capillacea | cox1 | OL434656 | Pterocladiella capillacea, 100% similarity, Tunisia (MG030796) and the Mediterranean French coast (OL809719) | |
Chlorophyta | ||||
Caulerpa webbiana f. disticha | tufA | FM956073 | Caulerpa webbiana, 100% similarity, Red Sea (AJ417958), Australia (KF314152), and the Hawaiian Islands (KJ957133) | Further studies of the different formae within the species are needed to confirm the subspecific rank of the Azorean voucher. |
References
- Seubert, M.; von Hochstetter, C. Übersicht Der Flora Der Azorischen Inseln. Arch. Naturgeschichte 1843, 9, 1–24. [Google Scholar]
- Gabriel, D.; Ferreira, A.I.; Micael, J.; Fredericq, S. Non-Native Marine Macroalgae of the Azores: An Updated Inventory. Diversity 2023, 15, 1089. [Google Scholar] [CrossRef]
- Neto, A.I.; Cacabelos, E.; Prestes, A.C.L.; Díaz-Tapia, P.; Moreu, I. New Records of Marine Macroalgae for the Azores. Bot. Mar. 2022, 65, 105–120. [Google Scholar] [CrossRef]
- Faria, J.; Prestes, A.C.L.; Moreu, I.; Martins, G.M.; Neto, A.I.; Cacabelos, E. Arrival and Proliferation of the Invasive Seaweed Rugulopteryx okamurae in NE Atlantic Islands. Bot. Mar. 2022, 65, 45–50. [Google Scholar] [CrossRef]
- Gabriel, D.; Martins, B.; Ribeiro, C.; Vilizzi, L.; Ferreira, A.I.; Fredericq, S.; Calado, H. Quantification of the Invasiveness Risk of Non-Native Macroalgae in the Azores to Support Conservation Measures. Aquat. Conserv. 2024, 1–5. [Google Scholar] [CrossRef]
- Micael, J.; Parente, M.I.; Costa, A.C. Tracking Macroalgae Introductions in North Atlantic Oceanic Islands. Helgol. Mar. Res. 2014, 68, 209–219. [Google Scholar] [CrossRef]
- Neto, A.I.; Moreu, I.; Cacabelos, E.; Parente, M.I. Checklist of the Benthic Marine Algae of the Azores Archipelago. Available online: https://www.gbif.org/ (accessed on 21 December 2023).
- Guiry, M.D. How Many Species of Algae Are There? J. Phycol. 2012, 48, 1057–1063. [Google Scholar] [CrossRef]
- Saunders, G.W. Applying DNA Barcoding to Red Macroalgae: A Preliminary Appraisal Holds Promise for Future Applications. Philos. Trans. R. Soc. B Biol. Sci. 2005, 360, 1879–1888. [Google Scholar] [CrossRef]
- Bhattacharya, D.; Elwood, H.J.; Goff, L.J.; Sogin, M.L. Phylogeny of Gracilaria lemaneiformis (Rhodophyta) Based on Sequence Analysis of ITS Small Subunit Ribosomal RNA Coding Region. J. Phycol. 1990, 26, 181–186. [Google Scholar] [CrossRef]
- Bird, C.J.; Rice, E.L.; Murphy, C.A.; Ragan, M.A. Phylogenetic Relationships in the Gracilariales (Rhodophyta) as Determined by 18S RDNA Sequences. Phycologia 1992, 31, 510–522. [Google Scholar] [CrossRef]
- Hommersand, M.H.; Fredericq, S.; Freshwater, D.W. Phylogenetic Systematics and Biogeography of the Gigartinaceae (Gigartinales, Rhodophyta) Based on Sequence Analysis of RbcL. Bot. Mar. 1994, 37, 193–203. [Google Scholar] [CrossRef]
- De Clerck, O.; Guiry, M.D.; Leliaert, F.; Samyn, Y.; Verbruggen, H. Algal Taxonomy: A Road to Nowhere? J. Phycol. 2013, 49, 215–225. [Google Scholar] [CrossRef] [PubMed]
- Bartolo, A.G.; Zammit, G.; Peters, A.F.; Küpper, F.C. The Current State of DNA Barcoding of Macroalgae in the Mediterranean Sea: Presently Lacking but Urgently Required. Bot. Mar. 2020, 63, 253–272. [Google Scholar] [CrossRef]
- Silva, L.B.; Sardos, J.; de Sequeira, M.M.; Silva, L.; Crawford, D.; Moura, M. Understanding Intra and Inter-Archipelago Population Genetic Patterns within a Recently Evolved Insular Endemic Lineage. Plant Syst. Evol. 2016, 302, 367–384. [Google Scholar] [CrossRef]
- Draisma, S.G.A.; Prud’Homme van Reine, W.F.; Stam, W.T.; Olsen, J.L. A Reassessment of Phylogenetic Relationships within the Phaeophyceae Based on Rubisco Large Subunit and Ribosomal DNA Sequences. J. Phycol. 2001, 37, 586–603. [Google Scholar] [CrossRef]
- Lin, S.; Fredericq, S.; Hommersand, M.H. Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) Based on Large Subunit RDNA and RbcL Sequences, Including the Phycodryoideae, subfam. nov. J. Phycol. 2001, 37, 881–899. [Google Scholar] [CrossRef]
- Bittner, L.; Payri, C.; Couloux, A.; Cruaud, C.; Dereviers, B.; Rousseau, F. Molecular Phylogeny of the Dictyotales and Their Position within the Phaeophyceae, Based on Nuclear, Plastid and Mitochondrial DNA Sequence Data. Mol. Phylogenet. Evol. 2008, 49, 211–226. [Google Scholar] [CrossRef]
- Gabriel, D.; Draisma, S.G.A.; Sauvage, T.; Schmidt, W.E.; Schils, T.; Lim, P.-E.; Harris, D.J.; Fredericq, S. Multilocus Phylogeny Reveals Gibsmithia hawaiiensis (Dumontiaceae, Rhodophyta) to Be a Species Complex from the Indo-Pacific, with the Proposal of G. eilatensis sp. nov. Phytotaxa 2016, 277, 1–20. [Google Scholar] [CrossRef]
- Famà, P.; Wysor, B.; Kooistra, W.H.C.F.; Zuccarello, G.C. Molecular Phylogeny of the Genus Caulerpa (Caulerpales, Chlorophyta) Inferred from Chloroplast TufA Gene. J. Phycol. 2002, 38, 1040–1050. [Google Scholar] [CrossRef]
- Händeler, K.; WÄGELE, H.; Wahrmund, U.; Rüdinger, M.; Knoop, V. Slugs’ Last Meals: Molecular Identification of Sequestered Chloroplasts from Different Algal Origins in Sacoglossa (Opisthobranchia, Gastropoda). Mol. Ecol. Resour. 2010, 10, 968–978. [Google Scholar] [CrossRef]
- Sherwood, A.R.; Presting, G.G. Universal Primers Amplify a 23S RDNA Plastid Marker in Eukaryotic Algae and Cyanobacteria. J. Phycol. 2007, 43, 605–608. [Google Scholar] [CrossRef]
- Vieira, C.; De Ramon N’Yeurt, A.; Rasoamanendrika, F.A.; D’Hondt, S.; Tran, L.-A.T.; Van den Spiegel, D.; Kawai, H.; De Clerck, O. Marine Macroalgal Biodiversity of Northern Madagascar: Morpho-Genetic Systematics and Implications of Anthropic Impacts for Conservation. Biodivers. Conserv. 2021, 30, 1501–1546. [Google Scholar] [CrossRef]
- Tronholm, A.; Steen, F.; Tyberghein, L.; Leliaert, F.; Verbruggen, H.; Antonia Ribera Siguan, M.; De Clerck, O. Species Delimitation, Taxonomy, and Biogeography of Dictyota in Europe (Dictyotales, Phaeophyceae). J. Phycol. 2010, 46, 1301–1321. [Google Scholar] [CrossRef]
- Vieira, C.; Steen, F.; D’hondt, S.; Bafort, Q.; Tyberghein, L.; Fernandez-García, C.; Wysor, B.; Tronholm, A.; Mattio, L.; Payri, C.; et al. Global Biogeography and Diversification of a Group of Brown Seaweeds (Phaeophyceae) Driven by Clade-specific Evolutionary Processes. J. Biogeogr. 2021, 48, 703–715. [Google Scholar] [CrossRef]
- Schmidt, O.C. Die Marine Vegetation Der Azoren. Hedwigia 1928, 68, 327–346. [Google Scholar]
- Agardh, J. Om de under Korvetten Josephines Expedition, Sistliden Sommar, Insamlade Algerne. R. Swed. Acad. Sci. 1870, 4, 359–366. [Google Scholar]
- Vieira, C.; Henriques, F.; D’hondt, S.; Neto, A.; Almada, C.H.; Kaufmann, M.; Sansón, M.; Sangil, C.; De Clerck, O. Lobophora (Dictyotales) Species Richness, Ecology and Biogeography Across the North-Eastern Atlantic Archipelagos and Description of Two New Species. J. Phycol. 2020, 56, 346–357. [Google Scholar] [CrossRef]
- Trelease, W. Botanical Observations on the Azores. Mo. Bot. Gard. Annu. Rep. 1897, 1897, 77–220. [Google Scholar] [CrossRef]
- Faria, J.; Prestes, A.C.L.; Moreu, I.; Cacabelos, E.; Martins, G.M. Dramatic Changes in the Structure of Shallow-Water Marine Benthic Communities Following the Invasion by Rugulopteryx okamurae (Dictyotales, Ochrophyta) in Azores (NE Atlantic). Mar. Pollut. Bull. 2022, 175, 113358. [Google Scholar] [CrossRef]
- Santiañez, W.J.E.; Lee, K.M.; Uwai, S.; Kurihara, A.; Geraldino, P.J.L.; Ganzon-Fortes, E.T.; Boo, S.M.; Kogame, K. Untangling Nets: Elucidating the Diversity and Phylogeny of the Clathrate Brown Algal Genus Hydroclathrus, with the Description of a New Genus Tronoella (Scytosiphonaceae, Phaeophyceae). Phycologia 2018, 57, 61–78. [Google Scholar] [CrossRef]
- Tittley, I.; Neto, A.I. “Expedition Azores 1989”: Benthic Marine Algae (Seaweeds) Recorded from Faial and Pico. Arquipélago-Life Mar. Sci. 1994, 12, 1–13. [Google Scholar]
- Gain, L. Algues Provenant Des Campagnes de l’Hirondelle II (1911–1912). Bull. L’institut Océanographique Monaco 1914, 279, 1–23. [Google Scholar]
- Greuter, W.; Barrie, F.R.; Burdet, H.M.; Demoulin, V.; Nicolson, D.H.; Silva, P.C.; Trehane, P.; McNeill, J.; Filgueiras, T.S.; Skog, J.E.; et al. International Code of Botanical Nomenclature (Saint Louis Code); Koeltz Scientific Books: Koenigstein, Germany, 2000; ISBN 3-904144-22-7. [Google Scholar]
- Bruno de Sousa, C.; Cox, C.J.; Brito, L.; Pavão, M.M.; Pereira, H.; Ferreira, A.; Ginja, C.; Campino, L.; Bermejo, R.; Parente, M.; et al. Improved Phylogeny of Brown Algae Cystoseira (Fucales) from the Atlantic-Mediterranean Region Based on Mitochondrial Sequences. PLoS ONE 2019, 14, e0210143. [Google Scholar] [CrossRef] [PubMed]
- Neiva, J.; Bermejo, R.; Medrano, A.; Capdevila, P.; Milla-Figueras, D.; Afonso, P.; Ballesteros, E.; Sabour, B.; Serio, D.; Nóbrega, E.; et al. DNA Barcoding Reveals Cryptic Diversity, Taxonomic Conflicts and Novel Biogeographical Insights in Cystoseira s.l. (Phaeophyceae). Eur. J. Phycol. 2023, 58, 351–375. [Google Scholar] [CrossRef]
- South, G.; Tittley, I. A Checklist and Distributional Index of the Benthic Marine Algae of the North Atlantic Ocean; British Museum (Natural History) and Huntsman Marine Laboratory: London, UK; St. Andrews, NB, Canada, 1986; ISBN 0969254202. [Google Scholar]
- Neto, A.I.; Parente, M.; Cacabelos, E.; Costa, A.; Botelho, A.; Ballesteros, E.; Monteiro, S.; Resendes, R.; Afonso, P.; Prestes, A.; et al. Marine Algal Flora of Santa Maria Island, Azores. Biodivers. Data J. 2021, 9, e61909. [Google Scholar] [CrossRef]
- Seubert, M. Flora Azorica Quam Ex Collectionibus Schedisque Hochstetteri Patris et Flii Elaborativit et Tabulis XV Propria Manu Aeri Incisis Ilustravit Mauritius Seubert; Apud Adolphum Marcum: Bonn, Germany, 1844. [Google Scholar]
- Parente, M.I.; Fletcher, R.L.; Costa, F.O.; Saunders, G.W. Taxonomic Investigation of Ralfsia-like (Ralfsiales, Phaeophyceae) Taxa in the North Atlantic Ocean Based on Molecular and Morphological Data, with Descriptions of Pseudoralfsiaceae fam. nov., Pseudoralfsia azorica gen. et sp. nov. and Nuchella vesicularis gen. et sp. nov. Eur. J. Phycol. 2021, 56, 12–23. [Google Scholar] [CrossRef]
- Neto, A.I. Algas Marinhas Do Litoral Da Ilha Graciosa. Relatórios Comun. Dep. Biol. Univ. Açores 1989, 17, 61–65. [Google Scholar]
- Neto, A.I. Checklist of the Benthic Marine Macroalgae of the Azores. Arquipélago-Life Mar. Sci. 1994, 12, 15–34. [Google Scholar]
- Dijoux, L.; Viard, F.; Payri, C. The More We Search, the More We Find: Discovery of a New Lineage and a New Species Complex in the Genus Asparagopsis. PLoS ONE 2014, 9, e103826. [Google Scholar] [CrossRef]
- Schmidt, O.C. Beitrage Zur Kenntnis Der Meeresalgen Der Azoren II. Hedwigia 1929, 69, 165–172. [Google Scholar]
- Machín-Sánchez, M.; Le Gall, L.; Neto, A.I.; Rousseau, F.; Cassano, V.; Sentíes, A.; Fujii, M.T.; Díaz-Larrea, J.; Prud’homme van Reine, W.F.; Bonillo, C.; et al. A Combined Barcode and Morphological Approach to the Systematics and Biogeography of Laurencia pyramidalis and Laurenciella marilzae (Rhodophyta). Eur. J. Phycol. 2014, 49, 115–127. [Google Scholar] [CrossRef]
- Gil-Rodríguez, M.C.; Haroun, R. Laurencia viridis sp. nov. (Ceramiales, Rhodomelaceae) from the Macaronesian Archipelagos. Bot. Mar. 1992, 35, 227–238. [Google Scholar] [CrossRef]
- Rodríguez-Buján, I.; Pimentel, M.; Díaz-Tapia, P. Melanothamnus macaronesicus Rodríguez-Buján Díaz-Tapia, sp. nov. (Rhodomelaceae, Rhodophyta): A New Turf-Forming Species from the Azores and the Canary Islands. Cryptogam. Algol. 2021, 42, 77–91. [Google Scholar] [CrossRef]
- Machín-Sánchez, M.; Rousseau, F.; Le Gall, L.; Cassano, V.; Neto, A.I.; Sentíes, A.; Fujii, M.T.; Gil-Rodríguez, M.C. Species Diversity of the Genus Osmundea (Ceramiales, Rhodophyta) in the Macaronesian Region. J. Phycol. 2016, 52, 664–681. [Google Scholar] [CrossRef] [PubMed]
- Díaz-Tapia, P.; Muñoz-Luque, L.; Piñeiro-Corbeira, C.; Maggs, C.A. Phylogenetic Analyses of Macaronesian Turf-Forming Species Reveal Cryptic Diversity and Resolve Stichothamnion in the Vertebrata Clade (Rhodomelaceae, Rhodophyta). Eur. J. Phycol. 2021, 56, 444–454. [Google Scholar] [CrossRef]
- Williamson, C.J.; Walker, R.H.; Robba, L.; Yesson, C.; Russell, S.; Irvine, L.M.; Brodie, J. Toward Resolution of Species Diversity and Distribution in the Calcified Red Algal Genera Corallina and Ellisolandia (Corallinales, Rhodophyta). Phycologia 2015, 54, 2–11. [Google Scholar] [CrossRef]
- Brodie, J.; Walker, R.H.; Williamson, C.; Irvine, L.M. Epitypification and Redescription of Corallina officinalis L., the Type of the Genus, and C. Elongata Ellis et Solander (Corallinales, Rhodophyta). Cryptogam. Algol. 2013, 34, 49–56. [Google Scholar] [CrossRef]
- Harvey, A.S.; Woelkerling, W.J.; de Reviers, B. A Taxonomic Analysis of Jania (Corallinaceae, Rhodophyta) in South-Eastern Australia. Aust. Syst. Bot. 2020, 33, 221–277. [Google Scholar] [CrossRef]
- Neto, A.I. Observations on the Biology and Ecology of Selected Macroalgae from the Littoral of São Miguel (Azores). Bot. Mar. 2000, 43, 483–499. [Google Scholar] [CrossRef]
- Woelkerling, W.J.; Harvey, A.S.; de Reviers, B. Jania pedunculata (Rhodophyta: Corallinaceae): Typification, Nomenclature, and Taxonomic Status Relative to J. crassa, J. verrucosa Sensu Johansen & Womersley, and J. ungulata. Taxon 2015, 64, 1280–1293. [Google Scholar] [CrossRef]
- Piccone, A. Alghe Della Crociera Del ‘Corsaro’ Alle Azzorre. Nuovo G. Bot. Ital. 1989, 21, 171–214. [Google Scholar]
- Gabriel, D.; Schils, T.; Neto, A.I.; Paramio, L.; Fredericq, S. Predaea feldmannii subsp. azorica (Nemastomataceae, Nemastomatales), a New Subspecies of Red Algae (Rhodophyta) from the Azores. Cryptogam. Algol. 2009, 33, 251–270. [Google Scholar]
- Fredericq, S.; Serrão, E.; Norris, J.N. New Records of Red Algae from the Azores. Arquipélago-Life Mar. Sci. 1992, 10, 1–4. [Google Scholar]
- Gavio, B.; Hickerson, E.; Fredericq, S. Platoma chrysymenioides sp. nov. (Schizymeniaceae), and Sebdenia integra sp. nov. (Sebdeniaceae), Two New Red Algal Species from the Northwestern Gulf of Mexico, with a Phylogenetic Assessment of the Cryptonemiales Complex (Rhodophyta). Gulf Mex. Sci. 2005, 23, 38–57. [Google Scholar] [CrossRef]
- Gabriel, D.; Parente, M.I.; Neto, A.I.; Raposo, M.; Schils, T.; Fredericq, S. Phylogenetic Appraisal of the Genus Platoma (Nemastomatales, Rhodophyta), Including Life History and Morphological Observations on P. cyclocolpum from the Azores. Phycologia 2010, 49, 2–21. [Google Scholar] [CrossRef]
- Krayesky, D.M.; Norris, J.N.; Gabrielson, P.W.; Gabriel, D.; Fredericq, S. A New Order of Red Algae Based on the Peyssonneliaceae, with an Evaluation of the Ordinal Classification of the Florideophyceae (Rhodophyta). Proc. Biol. Soc. Wash. 2009, 122, 364–391. [Google Scholar] [CrossRef]
- Gabriel, D.; Schils, T.; Parente, M.I.; Draisma, S.G.A.; Neto, A.I.; Fredericq, S. Taxonomic Studies in the Schizymeniaceae (Nemastomatales, Rhodophyta): On the Identity of Schizymenia sp. in the Azores and the Generic Placement of Nemastoma confusum. Phycologia 2011, 50, 109–121. [Google Scholar] [CrossRef]
- Pestana, E.M.D.S.; Lyra, G.D.M.; Santos, G.D.N.; Santos, C.C.D.; Cassano, V.; Nunes, J.M.D.C. Integrative Approach Reveals Underestimated Peyssonneliales Diversity in Brazil: Registering the First Occurrence of Ramicrusta and Incendia, with the Description of Three New Species. Phytotaxa 2020, 439, 39–55. [Google Scholar] [CrossRef]
- Pestana, E.M.d.S.; Nunes, J.M.d.C.; Cassano, V.; Lyra, G.d.M. Taxonomic Revision of the Peyssonneliales (Rhodophyta): Circumscribing the Authentic Peyssonnelia Clade and Proposing Four New Genera and Seven New Species. J. Phycol. 2021, 57, 1749–1767. [Google Scholar] [CrossRef]
- Gabriel, D.; Schmidt, W.E.; Krayesky, D.M.; Harris, D.J.; Fredericq, S. The Crustose Red Algal Genus Peyssonnelia (Peyssonneliales, Rhodophyta) in the Azores: From Five to One Species. Arquipélago-Life Mar. Sci. 2015, 32, 1–9. [Google Scholar]
- Bullock, R.C.; Turner, R.D.; Fralick, R.A. Species Richness and Diversity of Algal-Associated Micromolluscan Communities from São Miguel, Açores. Açoreana 1990, Suplemento I, 39–58. [Google Scholar]
- Cacabelos, E.; Faria, J.; Martins, G.M.; Mir, C.; Parente, M.I.; Gabriel, D.; Sánchez, R.; Altamirano, M.; Costa, A.C.; Prud’homme van Reine, W.; et al. First Record of Caulerpa prolifera in the Azores (NE Atlantic). Bot. Mar. 2019, 62, 155–160. [Google Scholar] [CrossRef]
- Cardigos, F.; Tempera, F.; Fontes, J.; Ribeiro, P.; Sala, I.; Caldeira, R.; Santos, R.S. Relatório Sobre a Presença de Uma Nova Espécie No Norte Da Ilha Do Faial; Departamento de Oceanografia e Pescas da Universidade dos Açores: Horta, Portugal, 2013. [Google Scholar]
- Amat, J.N. The Recent Northern Introduction of the Seaweed Caulerpa Webbiana (Caulerpales, Chlorophyta) in Faial, Azores Islands (North-Eastern Atlantic). Aquat. Invasions 2008, 3, 417–422. [Google Scholar] [CrossRef]
- Cardigos, F.; Monteiro, J.; Fontes, J.; Parretti, P.; Serrão Santos, R. Fighting Invasions in the Marine Realm, a Case Study with Caulerpa webbiana in the Azores. In Biological Invasions in Changing Ecosystems; Canning-Clode, J., Ed.; De Gruyter Open: Warsaw, Poland, 2015; pp. 279–300. [Google Scholar]
- Verbruggen, H.; Leliaert, F.; Maggs, C.A.; Shimada, S.; Schils, T.; Provan, J.; Booth, D.; Murphy, S.; De Clerck, O.; Littler, D.S.; et al. Species Boundaries and Phylogenetic Relationships within the Green Algal Genus Codium (Bryopsidales) Based on Plastid DNA Sequences. Mol. Phylogenet. Evol. 2007, 44, 240–254. [Google Scholar] [CrossRef] [PubMed]
- Hayden, H.S.; Waaland, J.R. A Molecular Systematic Study of Ulva (Ulvaceae, Ulvales) from the Northeast Pacific. Phycologia 2004, 43, 364–382. [Google Scholar] [CrossRef]
- Couceiro, L.; Cremades, J.; Barreiro, R. Evidence for Multiple Introductions of the Pacific Green Alga Ulva australis Areschoug (Ulvales, Chlorophyta) to the Iberian Peninsula. Bot. Mar. 2011, 54, 391–402. [Google Scholar] [CrossRef]
- Hanyuda, T.; Heesch, S.; Nelson, W.; Sutherland, J.; Arai, S.; Boo, S.M.; Kawai, H. Genetic Diversity and Biogeography of Native and Introduced Populations of Ulva pertusa (Ulvales, Chlorophyta). Phycol. Res. 2016, 64, 102–109. [Google Scholar] [CrossRef]
- Gittenberger, A.; Rensing, M.; Stegenga, H.; Hoeksema, B.W. Native and Non-Native Species of Hard Substrata in the Dutch Wadden Sea. Ned. Faun. Meded. 2010, 33, 21–75. [Google Scholar]
- Coat, G.; Dion, P.; Noailles, M.-C.; De Reviers, B.; Fontaine, J.-M.; Berger-Perrot, Y.; Loiseaux-De Goér, S. Ulva armoricana (Ulvales, Chlorophyta) from the Coasts of Brittany (France). II. Nuclear RDNA ITS Sequence Analysis. Eur. J. Phycol. 1998, 33, 81–86. [Google Scholar] [CrossRef]
- López, S.B.; Fernández, I.B.; Lozano, R.B.; Ugarte, J.C. Is the Cryptic Alien Seaweed Ulva pertusa (Ulvales, Chlorophyta) Widely Distributed along European Atlantic Coasts? Bot. Mar. 2007, 50, 267–274. [Google Scholar] [CrossRef]
- Chainho, P.; Fernandes, A.; Amorim, A.; Ávila, S.P.; Canning-Clode, J.; Castro, J.J.; Costa, A.C.; Costa, J.L.; Cruz, T.; Gollasch, S.; et al. Non-Indigenous Species in Portuguese Coastal Areas, Coastal Lagoons, Estuaries and Islands. Estuar. Coast. Shelf Sci. 2015, 167, 199–211. [Google Scholar] [CrossRef]
- Verlaque, M.; Belsher, T.; Deslous-Paoli, J.M. Morphology and Reproduction of Asiatic Ulva pertusa (Ulvales, Chlorophyta) in Thau Lagoon (France, Mediterranean Sea). Cryptogam. Algol. 2002, 23, 301–310. [Google Scholar]
- Wolf, M.A.; Sciuto, K.; Andreoli, C.; Moro, I. Ulva (Chlorophyta, Ulvales) Biodiversity in the North Adriatic Sea (Mediterranean, Italy): Cryptic Species and New Introductions. J. Phycol. 2012, 48, 1510–1521. [Google Scholar] [CrossRef] [PubMed]
- Miladi, R.; Manghisi, A.; Armeli Minicante, S.; Genovese, G.; Abdelkafi, S.; Morabito, M. A DNA Barcoding Survey of Ulva (Chlorophyta) in Tunisia and Italy Reveals the Presence of the Overlooked Alien U. ohnoi. Cryptogam. Algol. 2018, 39, 85–107. [Google Scholar] [CrossRef]
- Loughnane, C.J.; McIvor, L.M.; Rindi, F.; Stengel, D.B.; Guiry, M.D. Morphology, RbcL Phylogeny and Distribution of Distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and Southern Britain. Phycologia 2008, 47, 416–429. [Google Scholar] [CrossRef]
- Hughey, J.R.; Maggs, C.A.; Mineur, F.; Jarvis, C.; Miller, K.A.; Shabaka, S.H.; Gabrielson, P.W. Genetic Analysis of the Linnaean Ulva lactuca (Ulvales, Chlorophyta) Holotype and Related Type Specimens Reveals Name Misapplications, Unexpected Origins, and New Synonymies. J. Phycol. 2019, 55, 503–508. [Google Scholar] [CrossRef]
- Hughey, J.R.; Gabrielson, P.W.; Maggs, C.A.; Mineur, F. Genomic Analysis of the Lectotype Specimens of European Ulva rigida and Ulva lacinulata (Ulvaceae, Chlorophyta) Reveals the Ongoing Misapplication of Names. Eur. J. Phycol. 2022, 57, 143–153. [Google Scholar] [CrossRef]
- Steinhagen, S.; Hoffmann, S.; Pavia, H.; Toth, G.B. Molecular Identification of the Ubiquitous Green Algae Ulva Reveals High Biodiversity, Crypticity, and Invasive Species in the Atlantic-Baltic Sea Region. Algal Res. 2023, 73, 103132. [Google Scholar] [CrossRef]
- Fort, A.; McHale, M.; Cascella, K.; Potin, P.; Perrineau, M.; Kerrison, P.D.; da Costa, E.; Calado, R.; Domingues, M.d.R.; Costa Azevedo, I.; et al. Exhaustive Reanalysis of Barcode Sequences from Public Repositories Highlights Ongoing Misidentifications and Impacts Taxa Diversity and Distribution. Mol. Ecol. Resour. 2022, 22, 86–101. [Google Scholar] [CrossRef]
- Vieira, C.; Kim, M.S.; N’Yeurt, A.D.R.; Payri, C.; D’Hondt, S.; De Clerck, O.; Zubia, M. Marine Flora of French Polynesia: An Updated List Using DNA Barcoding and Traditional Approaches. Biology 2023, 12, 1124. [Google Scholar] [CrossRef]
- Torrano-Silva, B.N.; Vieira, B.R.; Riosmena-Rodríguez, R.; Oliveira, M.C. Guidelines for DNA Barcoding of Coralline Algae, Focusing on Lithophylloideae (Corallinales) from Brazil. Bot. Mar. 2018, 61, 127–140. [Google Scholar] [CrossRef]
- Gabriel, D.; Draisma, S.G.A.; Schils, T.; Schmidt, W.E.; Sauvage, T.; Harris, D.J.; Norris, J.N.; Fredericq, S. Quite an Oddity: New Worldwide Records of Renouxia (Rhodogorgonales, Rhodophyta), Including R. marerubra sp. nov. Eur. J. Phycol. 2020, 55, 197–206. [Google Scholar] [CrossRef]
- Brodie, J.; Mols Mortensen, A.; Ramirez, M.E.; Russell, S.; Rinkel, B. Making the links: Towards a global taxonomy for the red algal genus Porphyra (Bangiales, Rhodophyta). In Nineteenth International Seaweed Symposium: Proceedings of the 19th International Seaweed Symposium; Borowitzka, M.A., Critchley, A.T., Kraan, S., Peters, A., Sjøtun, K., Notoya, M., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 489–499. [Google Scholar]
- Boo, G.H.; Van Nguyen, T.; Kim, J.Y.; Gall, L.L.; Rico, J.M.; Bottalico, A.; Boo, S.M. A revised classification of the Gelidiellaceae (Rhodophyta) with descriptions of three new genera: Huismaniella, Millerella and Perronella. Taxon 2016, 65, 965–979. [Google Scholar] [CrossRef]
- Alvarez, A.; Anaya, J.; Arellano, B.; Bartlebaugh, A.; Capurro, M.C.; Carrillo, A.; Chacon, I.R.; Cordova, L.; Corral, B.; DaSilva, M.; et al. Analysis of the Complete Organellar Genomes of the Rockweed Fucus spiralis (Fucaceae, Phaeophyceae) Supports Its Infraspecific Recognition as Fucus vesiculosus var. spiralis. Mitochondrial DNA Part B 2018, 3, 482–483. [Google Scholar] [CrossRef] [PubMed]
- Xu, K.; Zhou, B.; Sun, Y.; Zang, Y. The Complete Plastid Genome of the Brown Alga Scytosiphon lomentaria (Scytosiphonaceae, Phaeophyceae). Mitochondrial DNA Part B 2019, 4, 2161–2162. [Google Scholar] [CrossRef]
- De Jesus, P.B.; de Lyra, G.M.; Zhang, H.; Fujii, M.T.; Nauer, F.; de Nunes, J.M.C.; Davis, C.C.; Oliveira, M.C. Phylogenomics and Taxon-Rich Phylogenies of New and Historical Specimens Shed Light on the Systematics of Hypnea (Cystocloniaceae, Rhodophyta). Mol. Phylogenet. Evol. 2023, 183, 107752. [Google Scholar] [CrossRef]
- González-Nieto, D.; Oliveira, M.C.; Núñez Resendiz, M.L.; Dreckmann, K.M.; Mateo-Cid, L.E.; Sentíes, A. Molecular Assessment of the Genus Sargassum (Fucales, Phaeophyceae) from the Mexican Coasts of the Gulf of Mexico and Caribbean, with the Description of S. xochitlae sp. nov. Phytotaxa 2020, 461, 254–274. [Google Scholar] [CrossRef]
- Calderon, M.S.; Bustamante, D.E.; Gabrielson, P.W.; Martone, P.T.; Hind, K.R.; Schipper, S.R.; Mansilla, A. Type Specimen Sequencing, Multilocus Analyses, and Species Delimitation Methods Recognize the Cosmopolitan Corallina berteroi and Establish the Northern Japanese C. yendoi sp. nov. (Corallinaceae, Rhodophyta). J. Phycol. 2021, 57, 1659–1672. [Google Scholar] [CrossRef]
Locality | Collectors | Date | Coordinates |
---|---|---|---|
São Miguel Island | |||
Caloura, Cerco | D. Gabriel, A. F. Santos | 21, 24-July-2020 | 37.708154 N 25.509782 W |
Atalhada, Cruzeiro | D. Gabriel | 9-June-2020 | 37.744306 N 25.594341 W |
Livramento, Praia do Pópulo | D. Gabriel | 8-June-2020 | 37.750304 N 25.618740 W |
São Vicente de Ferreira, harbour | D. Gabriel | 27-September-2022 | 37.834432 N 25.668619 W |
Mosteiros, tide pools | D. Gabriel | 28-September-2022 | 37.899311 N 25.821360 W |
Santa Maria Island | |||
Maia | D. Gabriel, A. I. Ferreira | 27-August-2022 | 36.939619 N 25.014179 W |
Praia Formosa | D. Gabriel, A. I. Ferreira | 25-August-2022 | 36.949958 N 25.094974 W |
Anjos, Poça do Carro | D. Gabriel, A. I. Ferreira, S. Cabral | 25-August-2022 | 37.005955 N 25.161788 W |
Taxa | Genetic Markers | First Report to the Azores | Status in the Azores | Comments |
---|---|---|---|---|
Phylum Ochcrophyta Class Phaeophyceae Order Dictyotales Family Dictyotaceae | ||||
Dictyota cyanoloma Tronholm, De Clerck, A.Gómez-Garreta & Rull Lluch | psbA [24,25] | 2006 [24] | Native [7] | |
Dictyota dichotoma (Hudson) J.V.Lamouroux | psbA; cox1 [24,25] | 1928 [26] | Native [7] | |
Dictyota implexa (Desfontaines) J.V.Lamouroux | psbA; cox1 [24,25] | 1870 [27] | Native [7] | |
Dictyota pleiacantha Tronholm * | psbA [25] | 2005 [25] | Native (This study) | Phylogenetic reconstruction of Dictyota pleiacantha based on multiple genes (psaA, psbA, rbcL, cox1; [28]) indicates that the species comprises two clades, one occurring in the Canary Islands (type locality), Madeira and the Azores, therefore a Macaronesian endemic, and another occurring on the Western Atlantic coasts. |
Lobophora delicata Camacho & Fredericq | cox3 [28] | 2018 [28] | Native (This study) | According to Vieira et al. [25,29], the Azores are within the species’ native distributional range. |
Padina gymnospora (Kützing) Sonder * | UPA (This study) | First report (This study) | Cryptogenic (This study) | The species currently has a worldwide distribution and is not reported as introduced or invasive elsewhere. |
Rugulopteryx okamurae (E.Y.Dawson) I.K.Hwang, W.J.Lee & H.S.Kim | psbA, rbcL [4] | 2019 [4] | Introduced [4] | This species exhibits a highly invasive behavior in the Azores [5,30]. |
Order Ectocarpales Family Scytosiphonaceae | ||||
Colpomenia sinuosa (Mertens ex Roth) Derbès & Solier | cox1, rbcL, UPA (Unpublished; this study) | 1894 [29] | Native [7] | |
Hydroclathrus tilesii (Endlicher) Santiañez & M.J.Wynne | psaA, cox3 ([31]; as Hydroclathrus stephanosorus) | 2016 [31] | Introduced [2] | |
Petalonia binghamiae (J.Agardh) K.L.Vinogradova | cox1 (Unpublished) | 1989 ([32]; as Endarachne binghamiae) | Introduced [2] | |
Scytosiphon lomentaria (Lyngbye) Link, nom. cons. | cox1, UPA (Unpublished; this study) | 1911 ([33]; as Scytosiphon lomentarius) | Native [7] | Although the binomial Scytosiphon simplicissimus has priority over Scytosiphon lomentaria, the latter was maintained due to its widespread and consistent use for the species [34]. |
Zonaria tournefortii (J.V.Lamouroux) Montagne | cox1 (Unpublished; [25]) | 1928 [26] | Native [7] | |
Order Fucales Family Fucaceae | ||||
Fucus spiralis Linnaeus | cox1, UPA (Unpublished; this study) | 1911 ([33]; as Fucus platycarpus var. spiralis) | Cryptogenic [7] | |
Family Sargassaceae | ||||
Cystoseira pustulata (Ercegovic) Neiva & Serrão * | cox1, cox3, nad1, psaA (Unpublished; [35,36]) | 1986 ([37]; as Cystoseira compressa and C. humilis) | Native (This study) | According to Neiva et al. [36], Cystoseira compressa and C. humilis are apparently absent in the Azores and should be referred to as C. pustulatus. According to Neiva et al. [36], the Azores are within the native distributional range of Cystoseira pustulata. Sequences not found in the search described in Section 2.3 for missing the locality in GenBank were added to the list by the authors who knew the article where the sequences were published [35]. |
Ericaria selaginoides (Linnaeus) Molinari & Guiry | cox1 [36] | 1986 ([37]; as Cystoseira tamariscifolia) | Native ([38]; as Cystoseira tamariscifolia) | |
Gongolaria abies-marina (S.G.Gmelin) Kuntze | cox1, cox3, nad1, psaA (Unpublished; [36]) | 1938 ([39]; as Cystoseira abies-marina) | Native [7] | |
Sargassum cymosum C.Agardh | cox1 (Unpublished) | 1986 [37] | Native [7] | |
Order Ralfsiales Family Pseudoralfsiaceae | ||||
Pseudoralfsia azorica Parente, Fletcher & G.W.Saunders * | cox1, rbcL [40] | 2009 [40] | Endemic [40] | |
Order Sphacelariales Family Stypocaulaceae | ||||
Halopteris filicina (Grateloup) Kützing | cox1 (Unpublished) | 1938 ([39]; as Sphacelaria filicina) | Native [7] | |
Halopteris scoparia (Linnaeus) Sauvageau | LSU (Unpublished) | 1911 [33] | Native [7] | |
Phylum Rhodophyta Class Florideophyceae Order Bonnemaisoniales Family Bonnemaisoniaceae | ||||
Asparagopsis armata Harvey | cox1 (Unpublished) | 1988 [41] | Introduced [2] | Previous reports Asparagopsis armata (see list from [42]) are based on A. delilei, which is currently a synonym of A. taxiformis. |
Asparagopsis taxiformis (Delile) Trevisan | cox1, cox2, LSU, rbcL-rbcS spacer (Unpublished; [43]) | 1928 ([44]; as Asparagopsis delilei) | Introduced [2] | |
Order Ceramiales Family Rhodomelaceae | ||||
Herposiphonia tenella (C.Agardh) Ambronn | rbcL [3] | 2018 [3] | Native [3] | |
Laurencia pyramidalis Bory ex Kützing | cox1, rbcL, UPA ([45]; This study) | 2011 [45] | Native [7] | |
Laurencia viridis Gil-Rodríguez & Haroun | cox1, rbcL [45] | 1981 [46] | Native [38] | |
Laurenciella marilzae (Gil-Rodríguez, Sentíes, Díaz-Larrea, Cassano & M.T.Fujii) Gil-Rodríguez, Sentíes, Díaz-Larrea, Cassano & M.T.Fujii | cox1, rbcL [45] | 2011 [45] | Native [7] | |
Lophocladia trichoclados (C.Agardh) F.Schmitz | rbcL [3] | 2018 [3] | Native [3] | |
Lophosiphonia simplicissima Díaz-Tapia | rbcL [3] | 2018 [3] | Native [3] | |
Melanothamnus macaronesicus Rodríguez-Buján & Díaz-Tapia | rbcL [47] | 2018 [47] | Native (This study) | According to Rodriguez-Bujan et al. [47], Melanothamnus macaronesicus was only found in the Canary Islands and the Azores; therefore, it is a Macaronesian endemic. |
Melanothamnus pseudoforcipatus Díaz-Tapia | rbcL [3] | 2018 [3] | Cryptogenic [3] | |
Osmundea oederi (Gunnerus) G.Furnari | cox1, rbcL [48] | 2010 [45,48] | Native [7] | |
Osmundea pinnatifida (Hudson) Stackhouse | cox1, rbcL [45] | 1938 ([39]; as Chondria pinnatifida) | Native [7] | |
Polysiphonia villum J.Agardh | rbcL [3] | 2018 [3] | Native [3] | |
Vertebrata barbarae Muñoz-Luque & Díaz-Tapia | rbcL [49] | 2018 [49] | Endemic [49] | Sequences not found in the search described in Section 2.3 for missing the locality in GenBank were added to the list by the authors who knew the article where the sequences were published [49]. |
Vertebrata cymatophila (Børgesen) Muñoz-Luque | rbcL [49] | 2018 [49] | Native (This study) | According to Díaz-Tapia et al. [49], Vertebrata cymatophila was only found in the Canary Islands and the Azores; therefore, it is a Macaronesian endemic. Sequences not found in the search described in Section 2.3 for missing the locality in GenBank were added to the list by the authors who knew the article where the sequences were published [49]. |
Order Corallinales Family Corallinaceae | ||||
Corallina berteroi Montagne ex Kützing | cox1, rbcL (Unpublished; [50]; as Coralllina caespitosa) | 2013 [51] | Native [7] | Sequences not found in the search described in Section 2.3 for missing the locality in GenBank were added to the list by the authors who knew the article where the sequences were published [50]. |
Jania pedunculata var. adhaerens (J.V.Lamouroux) A.S.Harvey, Woelkerling & Reviers | cox1, UPA (This study) | 1986 ([37]; as Jania adhaerens) | Native [7] | Studies based on lectotype material have supported the recognition of Jania pedunculata var. adhaerens as a variety rather than a distinct species [52]. However, the synonym Jania adhaerens is still widely used. |
Jania verrucosa J.V.Lamouroux, nom. rejic. | cox1, rbcL, UPA (This study) | 1993 [53] | Native [7] | Although studies based on lectotype material have indicated that Jania verrucosa is a name of uncertain nomenclatural application [54], it is still widely used. |
Family Lithophyllaceae | ||||
Amphiroa beauvoisii J.V.Lamouroux | cox1, UPA (This study) | 1886 ([55]; as Amphiroa exilis) | Native [7] | Gain [33] is the first to report Amphiroa beauvoisii to the Azores based on Piccone [55]. Nevertheless, Piccone reported A. exilis (currently a valid species) with various synonyms, including A. pustulata. (currently a synonym of A. beauvoisii). Although it is unknown how or when the species identity was clarified, the date of the original record was maintained. |
Order Gelidiales Family Gelidiaceae | ||||
Gelidium microdon Kützing | rbcL, UPA (This study) | 1938 ([39]; as Sphaerococcus corneus var. spinulosus) | Native [7] | |
Order Gelidiales Family Pterocladiaceae | ||||
Pterocladiella capillacea (S.G.Gmelin) Santelices & Hommersand | cox1 (Unpublished) | 1886 ([55]; as Pterocladia capillacea | Native [7] | |
Order Gigartinales Family Cystocloniaceae | ||||
Hypnea musciformis (Wulfen) J.V.Lamouroux | cox1, rbcL, UPA (This study) | 1911 [33] | Cryptogenic [7] | |
Order Nemastomatales Family Nemastomataceae | ||||
Predaea feldmannii subsp. azorica Gabriel | rbcL [56] | 1990 ([57]; as Predaea feldmannii) | Endemic [56] | |
Family Schizymeniaceae | ||||
Platoma cyclocolpum (Montagne) F.Schmitz | rbcL [58,59] | 1986 [37] | Native [7] | |
Schizymenia apoda (J.Agardh) J.Agardh | LSU, rbcL [59,60,61] | 1894 ([29]; as Schizymenia obovata and S. undulata) | Native [7] | |
Order Peyssonneliales Family Peyssonneliaceae | ||||
Olokunia boudouresquei (Yoneshigue) Pestana, Lyra, Cassano & J.M.C.Nunes * | rbcL (Unpublished; as Cruoriopsis crucialis) | First report (This study) | Cryptogenic (This study) | Olokunia boudouresquei is mostly an Atlantic species, with few reports to Australia and New Zealand. Due to the taxonomic confusion within Peyssonneliaceae [62,63], further studies are necessary to assess the species status in the Azores. |
Peyssonnelia coriacea Feldmann | LSU, rbcL ([60,64]; as Peyssonnelia squamaria) | 1990 [65] | Native ([7]; as Peyssonnelia squamaria) | Reappraisal of sequences of Peyssonnelia species indicates that the species reported from the Azores as P. squamata (KR732900) may be P. coriacea [62,63]. The sequencing of type material is necessary to confirm the new identity. |
Order Rhodymeniales Family Lomentariaceae | ||||
Lomentaria articulata (Hudson) Lyngbye | cox1, UPA (This study) | 1911 [33] | Native [7] | |
Phylum Chlorophyta Class Ulvophyceae Order Bryopsidales Family Caulerpaceae | ||||
Caulerpa prolifera (Forsskål) J.V.Lamouroux | tufA [66] | 2013 [67] | Introduced [2] | |
Caulerpa webbiana f. disticha Vickers | tufA (Unpublished) | 2002 ([68]; as Caulerpa webbiana) | Introduced ([68]; as Caulerpa webbiana) | This species has an invasive behavior in the Azores [68,69]. |
Family Codiaceae | ||||
Codium adhaerens C.Agardh | rpl16, rbcL [70] | 1912 [33] | Native [7] | |
Order Ulvales Family Ulvaceae | ||||
Ulva australis Areschoug * | tufA (This study) | First report (This study) | Introduced (This study) | Molecular analyses point to a greater genetic diversity of Ulva australis in the Northwest Pacific, with populations in Australia, New Zealand, California, Chile, and Europe deriving from multiple introductions [71,72,73]. In European waters, Ulva australis was discovered at several scattered locations in the 1990s and early 2000s, including the Delta region of the Netherlands, the Dutch Wadden Sea [74], off Brittany [75], the Iberian Peninsula, from the Bay of Biscay to Portugal [76,77] and the Mediterranean Sea (e.g., [78,79,80]). Possible introduction vectors include ballast water, hull fouling, and oyster transplants. |
Ulva compressa Linnaeus | tufA (This study) | 1938 [39] | Native [7] | |
Ulva lactuca | rbcL ([81]; as Ulva fasciata) | 1938 [39] | Cryptogenic [7] | Loughane et al. [81] provided an rbcL sequence (EU484418) of a voucher identified as Ulva fasciata. Later studies including type material [82] corrected the voucher identity to Ulva lactuca. |
Ulva lacinulata (Kützing) Wittrock * | tufA (This study) | First report (This study) | Cryptogenic (This study) | According to Hughey et al. [83], there is a common taxonomic confusion with this species, which has been mistakenly reported as U. laetevirens (JQ048945), U. scandinavica (MW570777), U. armoricana (AB097632), and U. rigida (EU484395). Genetic investigations of Ulva spp. in the Baltic Sea and the Atlantic proximities showed that U. rigida was absent from the studied areas while U. lacinulata was relatively frequent [84]. The worldwide distribution of Ulva species needs to be reappraised based on sequences from type material due to the general misuse of species names [85]. Additionally, further studies are necessary to assess the real identity of U. rigida, which is currently reported to be native to the Azores [7]. |
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© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Gabriel, D.; Schmidt, W.E.; Micael, J.; Moura, M.; Fredericq, S. DNA Barcode-Assisted Inventory of the Marine Macroalgae from the Azores, Including New Records. Phycology 2024, 4, 65-86. https://doi.org/10.3390/phycology4010004
Gabriel D, Schmidt WE, Micael J, Moura M, Fredericq S. DNA Barcode-Assisted Inventory of the Marine Macroalgae from the Azores, Including New Records. Phycology. 2024; 4(1):65-86. https://doi.org/10.3390/phycology4010004
Chicago/Turabian StyleGabriel, Daniela, William E. Schmidt, Joana Micael, Mónica Moura, and Suzanne Fredericq. 2024. "DNA Barcode-Assisted Inventory of the Marine Macroalgae from the Azores, Including New Records" Phycology 4, no. 1: 65-86. https://doi.org/10.3390/phycology4010004
APA StyleGabriel, D., Schmidt, W. E., Micael, J., Moura, M., & Fredericq, S. (2024). DNA Barcode-Assisted Inventory of the Marine Macroalgae from the Azores, Including New Records. Phycology, 4(1), 65-86. https://doi.org/10.3390/phycology4010004