Marine algal flora of Santa Maria Island, Azores

Abstract Background The algal flora of the Island of Santa Maria (eastern group of the Azores archipelago) has attracted interest of researchers on past occasions (Drouët 1866, Agardh 1870, Trelease 1897, Schmidt 1931, Ardré et al. 1974, Fralick and Hehre 1990, Neto et al. 1991, Morton and Britton 2000, Amen et al. 2005, Wallenstein and Neto 2006, Tittley et al. 2009, Wallenstein et al. 2009a, Wallenstein et al. 2010, Botelho et al. 2010, Torres et al. 2010, León-Cisneros et al. 2011, Martins et al. 2014, Micael et al. 2014, Rebelo et al. 2014, Ávila et al. 2015, Ávila et al. 2016, Machín-Sánchez et al. 2016, Uchman et al. 2016, Johnson et al. 2017, Parente et al. 2018). Nevertheless, the Island macroalgal flora is not well-known as published information reflects limited collections obtained in short-term visits by scientists. To overcome this, a thorough investigation, encompassing collections and presence data recording, was undertaken at both the littoral and sublittoral levels down to a depth of approximately 40 m, covering an area of approximately 64 km2. The resultant taxonomic records are listed in the present paper which also provides information on species ecology and occurrence around the Island, improving, thereby, the knowledge of the Azorean macroalgal flora at both local and regional scales. New information A total of 2329 specimens (including some taxa identified only to genus level) belonging to 261 taxa of macroalgae are registered, comprising 152 Rhodophyta, 43 Chlorophyta and 66 Ochrophyta (Phaeophyceae). Of these, 174 were identified to species level (102 Rhodophyta, 29 Chlorophyta and 43 Ochrophyta), encompassing 52 new records for the Island (30 Rhodophyta, 9 Chlorophyta and 13 Ochrophyta), 2 Macaronesian endemics (Laurencia viridis Gil-Rodríguez & Haroun; and Millerella tinerfensis (Seoane-Camba) S.M.Boo & J.M.Rico), 10 introduced (the Rhodophyta Acrothamnion preissii (Sonder) E.M.Wollaston, Antithamnion hubbsii E.Y.Dawson, Asparagopsis armata Harvey, Bonnemaisonia hamifera Hariot, Melanothamnus harveyi (Bailey) Díaz-Tapia & Maggs, Scinaia acuta M.J.Wynne and Symphyocladia marchantioides (Harvey) Falkenberg; the Chlorophyta Codium fragile subsp. fragile (Suringar) Hariot; and the Ochrophyta Hydroclathrus tilesii (Endlicher) Santiañez & M.J.Wynne, and Papenfussiella kuromo (Yendo) Inagaki) and 18 species of uncertain status (11 Rhodophyta, 3 Chlorophyta and 4 Ochrophyta).


Introduction
The marine algal flora of the isolated mid-Atlantic Azores archipelago is considered cosmopolitan, with species shared with Macaronesia, North Africa, the Mediterranean Sea, Atlantic Europe and America (Tittley 2003, Tittley and Neto 2006, Wallenstein et al. 2009b and relatively rich when compared to that of other remote oceanic Islands , Wallenstein et al. 2009b. Amongst the Atlantic archipelagos, Azores, with 405 species, comes second in species richness after the Canary Islands, with 689 species and is followed by Madeira (396), Cabo Verde (333) and Selvagens (295 2 species) (Freitas et al. 2019). The latter authors, based on extensive analysis encompassing data on coastal fishes, brachyurans, polychaetes, gastropods echinoderms and macroalgae, suggested that the Azores should be a biogeographical entity on its own and proposed a re-definition of the Lusitanian biogeographical province, in which they consider four ecoregions: the South European Atlantic Shelf, the Saharan Upwelling, the Azores ecoregion and a new ecoregion they named Webbnesia, which comprises the archipelagos of Madeira, Selvagens and the Canary Islands.
It should be noted that the paper by Freitas et al. (2019) reflects data from only a few of the nine Islands, since not all data were available to them. São Miguel, with 260 algal species cited at the moment (Table 1), is the Island with the greatest amount of research dedicated to the subject. To overcome this situation and with the aim of providing a better knowledge of the archipelago's seaweed flora, research has been conducted over the past three decades on all the Islands. Data on the Islands of Corvo and Flores, Graciosa, Pico and Terceira are already available on the recently-published papers by Neto et al. (2020a), Neto et al. (2020b), Neto et al. (2020c), Neto et al. (2020e). The present paper presents both physical and occurrence data and information gathered from macroalgae surveys undertaken on Santa Maria Island mainly by the Island Aquatic Research Group of the Azorean Biodiversity Centre of the University of the Azores (Link: https://ce3c.ciencias.ulisboa.pt/sub-team/island-aquatic-ecology), the BIOISLE, Biodiversity and Islands Research Group of CIBIO-Açores at the University of the Azores (Link: https://cibio.up.pt/research-groups-1/details/bioisle) and the OKEANOS Centre of the University of the Azores (Link: http://www.okeanos.uac.pt). In these surveys, particular attention was given to the small filamentous and thin sheet-like forms that are often shortlived and fast-growing and usually very difficult to identify in the wild, without the aid of a microscope and specialised literature in the laboratory.
The paper aims to provide a valuable marine biological tool for research on systematics, diversity and conservation, biological monitoring, climate change, ecology and more applied studies, such as biotechnological applications, for academics, students, government, private organisations and the general public. Table 1.
Number of macroalgal species on the Azorean Islands: Santa Maria, São Miguel, São Jorge and Faial (authors' unpublished data); Terceira (Neto et al. 2020a); Graciosa (Neto et al. 2020c); Pico (Neto et al. 2020b); Flores and Corvo (Neto et al. 2020e). tectonic plates (the North American Plate, the Eurasian Plate and the African Plate, Hildenbrand et al. 2014), the Azores archipelago (38°43′49″N, 27°19′10″W, Fig. 1) comprises nine Islands and several islets spread over 500 km in a WNW direction. The Island of Santa Maria (in black in Fig. 1), approximately 97 km², is the easternmost one of the archipelago (37°1'1''N, 25°11'6''W, Fig. 2), located approximately 430 km east of the Mid-Atlantic Ridge within the boundary that divides the Eurasian and African Plates (Hildenbrand et al. 2014). The western part of the Island is flat and has extensive wave-cut platforms reaching altitudes of 250 m above sea level. The eastern part is very irregular and has its highest point around 450 m (Neto et al. 2008c). There are no indications of recent volcanism and the last eruptions occurred during the Upper Pliocene. It is the only Island of the archipelago where marine fossiliferous deposits are known, which have been studied since the 19th century (see, for example, Amen et al. 2005, Neto et al. 2008c, Rebelo et al. 2014, Ávila et al. 2015).
The climate is characterised by regular rainfall, medium levels of relative humidity and persistent winds, mainly during the winter and autumn seasons (Morton et al. 1998). As in the remaining Azorean Islands, the tidal range is small (< 2 m), the coastal extension is restricted, with deep waters occurring within a few kilometres offshore and coasts are subjected to swell and surge most of the year (see Hidrográfico 1981).
The Island coastline is approximately 63 km long and the coastal morphology results from the effect of the wave action, responsible for the predominance of erosive formations and from the Island antiquity and, also, the fact that it has been frequently submerged. As a consequence, several agglomerations of marine sedimentary rocks occur (e.g. marine conglomerates, fossiliferous calcarenites and arenites) distributed through cliffs and headlands, providing a special geological value to this Island that is not present elsewhere in the archipelago (Neto et al. 2008c). The north and east coasts are characterised by discontinuous and mixed geological forms, with abrupt headlands between which lengths of large boulder and cobbles occur. At São Lourenço high cliffs give rise to narrow high-tide platforms and low headlands generally less than 10 m high, that allow the establishment of cobble beaches and marine deposition that creates the local sandy beach. The northwest coastline of the Island is characterised by the occurrence of marine deposition and agglomerations of small cobbles, while the northeast coast is sculpted by plunging cliffs. Boulders and cobbles are commonly present. The west and south coasts of the Island have predominantly steep slopes, characterised by the occurrence of plunging cliffs that vary in height, abrupt headland segments and occasional high-tide platforms covered by boulders and cobbles. Praia Formosa has a different configuration with a smooth typology that facilitates seasonal marine deposition processes that alternate between a sandy beach in summer and a cobble beach during the rest of the year (Neto et al. 2008c).
Along the coastline of the Island, the bottom is dominated by irregular rocky beds, with compact bedrock dominating over boulder and cobble ones. Only two sand basins occur, Praia Formosa (south coast) and São Lourenço on the east coast (Neto et al. 2008c). On both beaches, bedrock patches emerge from the sediment bed. This mixed substrate is common to several other places around Santa Maria, at variable depths down to 30 m (e.g. Baía do Salto de Cães and Ilhéu das Lagoinhas on the north coast, Baía do Aveiro and Baía da Maia on the east coast). Shore slope and topography show substantial variation along the shoreline. Western and northern shores are usually flatter, with depths of 30 m occurring about 500 m offshore. Eastern shores are steeper: depths of 30 m can be reached less than 200 m away from the coast. Southern shores are intermediate in this respect. The area that comprises the Praia Formosa presents a slope that is similar to that of the north side of the Island, while the one between Ponta da Malbusca and Ponta do Castelo is steeper (Neto et al. 2008c). Submerged or semi-submerged caves, arches and tunnels of small amplitude and reduced length are common. As depth increases, the slope decreases, although the bottom is still rocky and uneven (Neto et al. 2008a). The sediment floor covering the deepest areas is stable, generally composed of medium and/or coarse sand (Neto et al. 2008a). Along the coastline, natural sheltered habitats (arches and semisubmerged caves, tide pools) create favourable conditions for the growth and the occurrence of a considerable diversity and abundance of macroalgae, macroinvertebrates  (Neto et al. 2008a, Neto et al. 2008b) and pelagic and benthic coastal fish (Azevedo et al. 2008).
As on the other Islands of the archipelago, intertidal communities of Santa Maria Island are, in part, dominated by algal vegetation, which exhibits a distribution pattern in mosaic and/or bands, with a predominance of algal turfs, covering the rocks as a carpet (Neto et al. 2008c). This turf-growing form is a taxonomically complex mixture of small algae, recruits and juveniles of larger algae, in which the thalli intertwine and re-attach to one another and are adapted for vegetative spread using such multiple attachments to the substratum and adjacent thalli for anchorage (Wallenstein et al. 2009a). The compact mat retains water and provides a suitable habitat for admixed algae and other organisms. A very distinct horizontal pattern of species occurrence characterises the Azorean intertidal shores. In Santa Maria Island three major zones are commonly found (Neto et al. 2008c): the uppermost is dominated by littorinids (Fig. 3); the mid-level zone is characterised by chthamalid barnacles, sometimes limpets ( Fig. 4) and dominated by algal turf (Fig. 5); and the lowest zone, representing the transition to the sublittoral fringe, is characterised by various species of frondose algae growing in bands (e.g. the Macaronesian endemic Laurencia viridis, Fig. 6), as epiphytes or forming patches amongst and over turf species (e.g. Ellisolandia elongata (J.Ellis & Solander) K.R.Hind & G.W.Saunders, Fig. 7). The midshore level zone on bedrock or boulder shores sometimes exhibits patches of the brown alga Fucus spiralis Linnaeus and the red agarophyte Gelidium microdon Kützing (Fig. 8) and/or the occasional occurrence of the red algae Porphyra/Pyropia and/or Nemalion elminthoides (Velley) Batters, this latter commonly growing in patches with the brown crust Nemoderma tingitanum Schousboe ex Bornet (Fig. 9). In spring and summer, considerable amounts of the introduced red alga Asparagopsis armata can be seen at the lower intertidal level.   Mid-shore intertidal level, dominated by algal turf. Patches of the red algae Nemalion elminthoides can be seen in the image first plan (by the Island Aquatic Ecology Subgroup of cE3c-ABG).  The erect calcareous frond of Ellisolandia elongata growing epiphytically on the algal turf at the low intertidal level (by the Island Aquatic Ecology Subgroup of cE3c-ABG). Important features and habitats at the shore level are rock pools, occurring in different shapes and sizes and often recreating a shallow subtidal habitat which contains a rich  Patches of the red algae Nemalion elminthoides and the brown crust Nemoderma tingitanum at the mid-shore level of bedrock shores (by the Island Aquatic Ecology Subgroup of cE3c-ABG). diversity of marine life (Neto et al. 2008b). There is a gradient in the proportion of different algal groups in pools at different shore levels. Green algae dominate the upper shore while red and brown algae dominate rock pools lower on the shore. Similarly, faunal diversity in rock pools is greater at lower intertidal levels. Species diversity and richness are lower in upper shore rock-pools where climatic conditions are more stressful (Neto et al. 2008b).

Design description:
The sampling referred to in this paper was performed across littoral and sublittoral levels down to approximately 40 m on the Island of Santa Maria. Each sampling location was visited several times and, on each occasion, a careful and extensive survey was undertaken to provide a good coverage of the area. Both physical collections and presence recording were made by walking over the intertidal shores during low tides or by SCUBA diving. The specimens collected were taken to the laboratory for identification and preservation and the resulting vouchers were deposited at the AZB Herbarium Ruy Telles Palhinha and the LSM -Molecular Systematics Laboratory at the Faculty of Sciences and Technology of the University of the Azores.
Funding: This study was mainly financed by the following projects/scientific expeditions: •

RCGO -"Coastal Waste of the Eastern Group (São Miguel and Santa Maria
Islands; Formigas Islets): inventory, catalog, raise awareness", funded by QUERCUS (2006); • CAMAG/ORI -"Characterization of coastal water bodies on the islands of Santa Maria and São Miguel", funded by the Regional Government of the Azores, Regional Secretariat for the Environment and the Sea, Regional Directorate for Planning and Water Resources ( ERDF funds through the Operational Programme for Competitiveness Factors -COMPETE; • Portuguese Regional Funds, through DRCT -Regional Directorate for Science and Technology, within several projects, 2019 and 2020 and SRMCT /DRAM -Regional Secretariat for the Sea, Science and Technology, Sampling description: Sampling involved specimen collecting and species presence recording. At each location, samples were obtained by scraping and/or manually collecting one or two specimens of all different species found into labelled bags (Fig. 14). Species recording data were gathered by registering all species present in the sampled locations (Fig. 15). Intertidal collections were made during low tide by walking over the shores. Subtidal collections were made by SCUBA diving around the area.
Quality control: Each sampled taxon was identified by trained taxonomists and involved morphological and anatomical observations of whole specimens by eye and/or of histological preparations under microscopes to determine the main diagnostic features of each species as described in literature.
Step description: At the laboratory, standard procedures were followed in specimens sorting and macroalgae identification. A combination of morphological and anatomical characters and reproductive structures was used for species identification. For small and simple thalli, this required the observation of the entire thallus with the naked eye and/or using dissecting and compound microscopes. For larger and more complex algae, investigation of the thallus anatomy required histological preparations (longitudinal and transverse sections) or squashed preparations of mucilaginous thalli, sometimes after staining, to observe vegetative and reproductive structures and other diagnostic features.
The Azorean algal flora has components from several geographical regions which implies difficulties in species identification. Floras and keys for the North Atlantic, Tropical Atlantic and Western Mediterranean were used (e.g. Schmidt 1931, Taylor 1967, Taylor 1978, Levring 1974, Dixon and Irvine 1977, Lawson and John 1982, Irvine 1983, Gayral and Cosson 1986, Fletcher 1987, Afonso-Carrillo and Sansón 1989, Burrows 1991. Collecting macroalgae at the subtidal of Santa Maria Island (by the Island Aquatic Ecology Subgroup of cE3c-ABG).

Figure 15.
Quantitative recording of the presence and coverage of macroalgal species from subtidal rocky habitat (by the Island Aquatic Ecology Subgroup of cE3c-ABG). Boudouresque et al. 1992, Cabioc'h et al. 1992, Maggs and Hommersand 1993, Irvine and Chamberlain 1994, Brodie et al. 2007, Lloréns et al. 2012, Rodríguez-Prieto et al. 2013. For more critical and taxonomically difficult taxa, specimens were taken to the Natural History Museum (London) for comparison with collections there.
A reference collection was made for all collected specimens by assigning them a herbarium code number and depositing them at the AZB Herbarium Ruy Telles Palhinha and the LSM -Molecular Systematics Laboratory, University of Azores. Depending on the species and on planned further research, different types of collections were made, namely (i) wet collections using 5% buffered formaldehyde seawater and then replacing it by the fixing agent Kew (Bridsen and Forman 1999); (ii) dried collections, either by pressing the algae (most species) as described by Gayral and Cosson (1986) or by letting them air dry (calcareous species); and (iii) silica gel collections for molecular study.
Nomenclatural and taxonomic status used here follow Algaebase (Guiry and Guiry 2020). The database was organised on FileMaker Pro.

Temporal coverage
b74c3414-e277-4789-8806-27a9abf0f7ee; 22941d45-0678-49fb-bdfe-8b0052ceb298; 93e46396-33b2-4dff-b3d1-acff7e76753c. Description: This data paper presents physical and occurrence data from macroalgal surveys undertaken on Santa Maria Island between 1989 and 2019 (Neto et al. 2020d). The dataset submitted to GBIF is structured as a sample event dataset, with two tables: event (as core) and occurrences. The data in this sampling event resource have been published as a Darwin Core Archive (DwCA), which is a standardised format for sharing biodiversity data as a set of one or more data tables. The core data table contains 139 records (eventID). The extension data table has 2329 occurrences. An extension record supplies extra information about a core record. The number of records in each extension data table is illustrated in the IPT link. This IPT archives the data and thus serves as the data repository. The data and resource metadata are available for downloading in the downloads section.    Table 4.
Summary of the macroalgal flora of the Island of Santa Maria with information on the species origin and status