Marine algal (seaweed) flora of Terceira Island, Azores

Abstract Background As for many other Azorean Islands, the macroalgal flora of Terceira (belonging to the central group of the archipelago) is poorly known, the published information reflecting occasional collections of sporadic visitors to the island. In order to overcome this and contribute to improve the knowledge of Azorean macroalgal flora at both local and regional scales, a thorough investigation was conducted. Both collections and presence data recordings were undertaken at the littoral and sublittoral levels down to approximately 40 m around the island, covering a total area of approximately 49 km2. This paper lists the taxonomic records and provides information on each species’ ecology and occurrence on the Island’s littoral. New information A total of 418 specimens (including taxa identified only to genus level) belonging to 147 taxa of macroalgae, comprising 95 Rhodophyta, 33 Chlorophyta and 19 Ochrophyta (Phaeophyceae) are registered. Of these, 113 were identified to species level (73 Rhodophyta, 24 Chlorophyta and 16 Ochrophyta), encompassing 35 new records for the Island (27 Rhodophyta, 6 Chlorophyta and 2 Ochrophyta). Most species are native, including the Macaronesian endemisms Codium elisabethiae O.C.Schmidt, Millerella tinerfensis (Seoane-Camba) S.M.Boo & J.M.Rico and Phyllophora gelidioides P.Crouan & H.Crouan ex Karsakoff. Eight species are introduced and 15 have uncertain origin.


Introduction
The macroalgal flora of the isolated mid-Atlantic Azores archipelago, as a whole, may be considered relatively rich when compared to that of other remote oceanic islands, such as the Shetlands and Faroes in the colder North Atlantic and Ascension and Tristan da Cunha in the Southern Atlantic , Wallenstein et al. 2009). With approximately 400 species (Freitas et al. 2019), the Azorean algal flora has been considered cosmopolitan, as it shares species with Macaronesia, North Africa, the Mediterranean Sea, Atlantic Europe and America (Tittley 2003, Tittley and Neto 2006, Wallenstein et al. 2009).
The published information, however, reflects data from only a few of the nine islands. Terceira, the second largest island of the central group and the third largest of the archipelago, is amongst the lesser-studied ones. To overcome this and contribute to a better understanding of the seaweed flora of the Azores archipelago, a thorough investigation was conducted in the period between 2000 and 2014, mainly by the Island Aquatic Research Group of the Azorean Biodiversity Centre of the University of the Azores (https://ce3c.ciencias.ulisboa.pt/sub-team/island-aquatic-ecology). In these surveys, special attention was dedicated to the sheet-like and filamentous forms that are difficult to identify in the wild, the seasonal and fast growing annuals and particularly to the small forms that are often short-lived and fast growing species, very difficult to identify without the aid of a microscope. This paper compiles physical, occurrence and survey data and is intended as a practical resource for biological studies (such as systematics, diversity and conservation, biological monitoring, climate change and ecology) and for academics, students, government, private organisations and the general public.

General description
Purpose: By listing the taxonomic records for Terceira and presenting general information for each taxon's occurrence on the Island's littoral, this paper addresses several biodiversity shortfalls (see Cardoso et al. 2011, Hortal et al. 2015, namely the need to catalogue the Azorean macroalgae (Linnean shortfall) and improve the current information on their local and regional geographic distribution (Wallacean shortfall), as well as on species' abundances and dynamics in space (Prestonian shortfall). Voucher specimen management was mainly undertaken by Afonso Prestes, Ana I. Neto, Eunice Nogueira, Natália Cabral and Roberto Resendes.

Study area description:
Located along a WNW-trending strip and spreading over 500 km in the North Atlantic, roughly at 38°43'49"N, 27°19'10"W ( Fig. 1), the Azores archipelago is composed of nine islands and several islets. The islands are surrounded by deep waters due to the absence of a continental shelf and, therefore, have a restricted coastal extension, which is subjected to swell and surge most of the year. The tidal range is small (< 2 m, see Hidrográfico 1981) and the shore geomorphology alternates between high cliffs and rocky cobble/boulder beaches (Borges 2004). The climate is temperate oceanic, with regular and abundant rainfall and high levels of relative humidity and persistent winds, mainly during winter and autumn (Morton et al. 1998). Fig. 1), located in the central group roughly at 38°48'50"N, 27°23'25"W, 150 km northeast of São Miguel, is the third largest island of the Azores archipelago. It has an elliptical form, 29 km long and 18 km wide, a maximum altitude of 1021 m at the summit of Serra de Santa Bárbara and a total area of about 397 km . The coastline has a total length of 112 km and is characterised by cliffs that vary from small to moderate heights, interrupted by small bays. Sandy beaches are limited to Praia da Vitória, located on the more protected eastern part of the Island. The northern coast is more exposed and constantly submitted to the wave action (Gomes and Pinto 2004).

Terceira (in black in
The intertidal and shallow subtidal rocky-shore communities of Terceira are dominated by macroalgae, similarly to those of the remaining Azorean Islands . The frondose species Fucus spiralis Linnaeus (Fig. 2), Ulva rigida C.Agardh and Gelidium microdon Kützing are often present at mid-shore levels, growing interspaced with the small chthamalid barnacles. Slightly below this level, the lack of herbivores, resulting from the over-exploitation of limpets (Martins et al. 2011, Martins et al. 2008, Faria et al. 2014, favours an almost homogeneous coverage of the shore by algal turfs (Fig. 3). These are growth forms of either diminutive algae or diminutive forms of larger species that create a dense, compact mat 20-30 mm thick, either monospecific (mainly composed of Caulacanthus ustulatus (Mertens ex Turner) Kützing or Gymnogongrus spp.) or multispecific and composed of articulate calcareous algae (e.g. Ellisolandia elongata (J.Ellis & Solander) K.R.Hind & G.W.Saunders and Jania spp.) and/or soft algae (e.g. Centroceras clavulatum (C.Agardh) Montagne, Chondracanthus spp. and Laurencia spp.). Lower on the shore, the erect, corticated macrophytes Ellisolandia elongata, Cystoseira spp. and Osmundea pinnatifida (Hudson) Stackhouse are commonly found, frequently epiphyting multi-specific algal turfs (Fig. 4). The shallow subtidal is mainly characterised by associations of two or three frondose macrophytes, predominantly the brown seaweeds Dictyota spp. and Zonaria tournefortii (J.V. Lamouroux) Montagne (Fig. 5).

Design description:
The algae, referred to in this paper, were sampled during field studies at littoral and sublittoral levels down to approximately 40 m on Terceira Island, covering an area of 49 km . Presence recordings and physical collections were made by walking over the shores or by scuba diving. The specimens collected were taken to the laboratory for standard procedures and the resulting vouchers were deposited at the AZB Herbarium Ruy Telles Palhinha, 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: Sampling description: Intertidal collections were made at low tide by walking over the shores. Subtidal collections were made by scuba diving around the area. Sampling encompassed both physical collections and species presence recordings. For the former, in each sampling location, collections were made manually by scraping one or two specimens of species found into labelled bags. Species recording data were gathered by registering all species present in the visited locations (Fig. 7).

Quality control:
The collected taxa were investigated by trained taxonomists with the help of keys and floras. This involved morphological and anatomical examination by eye or under the dissecting and compound microscopes of an entire specimen or slide preparation. In difficult cases, specimens were sent to experts for identification.  Macroalgae recordings at the rocky subtidal (by the Island Aquatic Ecology Subgroup of cE3c-ABG) .
Step description: In the laboratory, the specimens were sorted and studied following standard procedures used in macroalgae identification.
Species identification was based on morphological and anatomical characters and reproductive structures. For small and simple thalli, this required observation of the entire thallus by eye and/or using dissecting and compound microscopes (Fig. 8). For larger and more complex algae, the investigation of the thallus anatomy required histological work to obtain longitudinal and transverse sections needed for the observation of cells, reproductive structures and other diagnosing characters. Since the Azorean algal flora is composed of taxa from various geographical regions, floras and keys mainly from the Atlantic and Western Mediterranean were used in species identification (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, 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 or sent to specialists.
A reference collection was made for all specimens collected by giving them a herbarium code number and depositing them at the AZB Herbarium Ruy Telles Palhinha, University of Azores. Depending on the species and on planned further research, different types of collections were made, namely (i) liquid 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 collections for molecular studies.
Nomenclatural and taxonomic status used here follow Algaebase (Guiry and Guiry 2020). The database was organised on FileMaker Pro.

Taxonomic coverage
Description: All macroalgae were identified to genus or species level. In total, 147 taxa were identified belonging to 21 orders and 45 families, distributed by the phyla Rhodophyta (9 orders and 25 families), Chlorophyta (5 orders and 8 families) and Ochrophyta (7 orders and 12 families). Description: This data paper presents physical and occurrence data from macroalgal surveys undertaken on Terceira Island between 2000 and 2014. The dataset submitted to GBIF is structured as a sample event dataset, with two tables: event (as core) and occurrences (Neto et al. 2020). 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 18 records (eventID). The extension data table has 418 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.

Additional information
This paper accommodates the 418 specimens of macroalgae recorded from Terceira Island in 147 taxa (Tables 2, 3) comprising 113 confirmed species and 34 taxa identified only to genus level, belonging to 21 orders and 45 families, distributed by the phyla Rhodophyta (9 orders and 25 families), Chlorophyta (5 orders and 8 families) and Ochrophyta (7 orders and 12 families  A mismatch regarding the GBIF backbone taxonomy of some of the macroalgae species names was identified as detailed in Suppl. material 1. Table 3.
Main taxonomic figures with information on the species origin and status.