Marine algal flora of Formigas Islets, Azores

Abstract Background The oldest reference to marine life in Formigas Islets (oriental group of the Azores archipelago) goes back to the 16th century. Nevertheless, their macroalgal flora is poorly known, the published information mainly resulting from occasional collections of sporadic visitors. To overcome this and contribute to the knowledge of Azorean macroalgal flora at both local and regional scales, a thorough investigation was conducted in 1990 and 1991 under two expeditions promoted by the Marine Biology Research Group of the Department of Biology, University of the Azores. Collections and presence data recordings were undertaken at the littoral and sublittoral levels down to approximately 40 m, in an area of approximately 0.04 km2. This paper lists the taxonomic records and provides information regarding each species’ ecology and occurrence on the Islets’ littoral. New information A total of 320 specimens are registered (including taxa identified only at generic level) belonging to 90 taxa of macroalgae, from which 70 were diagnosed at species level. The confirmed species comprise 39 Rhodophyta, 12 Chlorophyta and 19 Ochrophyta (Phaeophyceae), distributed in 22 orders (13 Rhodophyta, 3 Chlorophyta and 6 Ochrophyta) and 37 families (24 Rhodophyta, 6 Chlorophyta and 7 Ochrophyta). Sixty-one species represent new records for the Islets, from which Botryocladia macaronesica Afonso-Carrillo, Sobrino, Tittley & Neto and Laurencia viridis Gil-Rodriguez & Haroun are Macaronesian endemisms. Most species are native to the Azores, but six have an uncertain origin and four are introduced (the Rhodophyta Asparagopsis armata Harvey; Laurencia dendroidea J.Agardh; Neoizziella divaricata (C.K.Tseng) S.-M.Lin, S.-Y.Yang & Huisman and the Ochrophyta Hydroclathrus tilesii (Endlicher) Santiañez & M.J.Wynne).


Introduction
The Formigas Islets are located about 31 km NE of Santa Maria Island and 55 km SE of São Miguel Island (oriental group of Azorean archipelago, approximately 37°16′35″N, 24°46′54″W). They are arranged in a N-S direction, over a total length of about 165 m and a width of 80 m. Together with the submersed bank of Dollabarat, they form the Nature Reserve of Formigas Bank (DLR n° 11/88/ A).
The oldest reference to life in Formigas Islets consists of descriptions of its marine fauna in the 16th century manuscript "Saudades da terra", written by the naturalist clergyman Gaspar Frutuoso. Subsequently, these Islets were occasionally studied in sporadic visits by researchers, the first reference to the marine macroalgae being that of Piccone (1889). After that, several expeditions were made in order to study of the fauna and flora of the Islets, which resulted in a few publications (see revision in Azevedo et al. 1991). An important finding was the first Azorean record of the brown alga Laminaria ochroleuca Bachelot de la Pylaie (made by Ardré et al. 1973). Despite these efforts, the algal flora of these Islets remained poorly known until the nineties, when a thorough investigation conducted by the Marine Biology Research Group of the Department of Biology, University of the Azores, took place. This research group went to the Islets in 1990 and 1991 and undertook collections and presence data recordings at the littoral and sublittoral levels down to about 40 m, over an area of approximately 0.04 km .

General description
Purpose: This paper, aimed at contributing to a better understanding of the seaweed flora of the Azores archipelago, lists the macroalgae recorded on surveys undertaken on the Formigas Islets (Azores, eastern group) and presents general information for each taxon's occurrence on the Islets' littoral, thus addressing several biodiversity shortfalls (see 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). It is intended as a resource for academics, students, government, private organisations and the general public and also as a practical basis for biological studies, such as systematics, diversity and conservation, biological monitoring, climate change and ecology. Ana I. Neto and Heather Baldwin were responsible for the species identification.

Project description
Voucher specimen management was mainly undertaken by Afonso Prestes, Ana I. Neto, Eunice Nogueira, Natália Cabral and Roberto Resendes.
Study area description: Located in the eastern group of the Azores archipelago, the Formigas Islets (37°16′35″N, 24°46′54″W, Fig. 1) are approximately 32 km NE of Santa Maria Island and 55 km SE of São Miguel Island, thus being the most isolated Islets of the Azores. Consequently, they are relatively protected from human action and function as a breeding and nursing ground for many marine species occurring in the Azorean waters (Costa et al. 1994). The Islets, together with the submersed bank of Dollabarat, form the Formigas Bank, located between the parallels 37°14'N and 37°17'N and the meridians 24°43'W and 24°47'W, occupying an area about 11 km long and 5 km wide (Azevedo et al. 1991) and designated as a Nature Reserve in 1988 (DLR n° 11/88/ A).
The Formigas Islets are located in the NW part of the bank. With a N-S arrangement, they have a total length of about 165 m and width of 80 m, with an area of compact rocks in the southern part and one of large blocks in the North (Fig. 2). The highest block (Formigão) is 11 m high. In the South region, there is a lighthouse, from which there are two small anchorages (Azevedo et al. 1991).
As in the remaining archipelago, the climate is temperate oceanic with persistent winds, regular and abundant rainfall and high levels of relative humidity, mainly during winter and autumn (Morton et al. 1998). The tidal range is small (< 2 m, see Hidrográfico 1981) and  the Islets are surrounded by deep waters. Intertidal space is limited and permanently subjected to the action of the waves, which does not allow the establishment of terrestrial fauna and flora (Costa et al. 1994), but the marine biota is rich. Most seaweeds and invertebrates that characterise the exposed Azorean coasts can be found there; the great clarity of the waters allows the algal communities to extend to great depths. This profusion of algae provides shelter and food for many animals and supports a complex food web (Costa et al. 1994).
The intertidal zone is narrow and mostly dominated by animals (e.g. gastropods, chthamalid barnacles and decapods) and algal turfs (mostly composed by various species of Ceramium spp. and Gymnogongrus spp.) (Fig. 3), that are typically found in most of the Islands. The many channels that cross the rocky platforms are dominated by luxuriant forms of the brown algae Cystoseira spp., Treptacantha abies-marina (Fig. 4) and Sargassum spp. At the low intertidal, the algal turfs give rise to erect forms of algae, for example, Elisolandia elongata (Fig. 5). Subtidally, the rocky walls and rocky platforms are covered with erect, corticated macrophytes, for example, Dictyota spp. and Plocamium cartilagineum ( Fig. 6). At and below 40 m depth, the leathery brown algae Laminaria ochroleuca can form some monospecific patches (Neto, pers. observ.).

Design description:
The macroalgae, referred to in this paper, were collected during field studies at littoral and sublittoral levels down to approximately 40 m on the Formigas Islets, over an area of 0.04 km (Table 1, Fig. 2). Intertidal collections were undertaken at low tide by walking over the shore. Subtidal collections were undertaken by scuba diving. Each sampling location was visited several times. On each occasion, a careful survey was made to allow a good coverage of the area. Whenever an unknown species was found, it was collected, given an individual registration number and vouchers deposited at the AZB Herbarium Ruy Telles Palhinha, at the Faculty of Sciences and Technology of the University of the Azores.  Figure 6.

Sampling methods
Study extent: Collections were made at littoral and sublittoral levels down to about 40 m around Formigas Islets over a total area of approximately 0.04 km (Fig. 2).
Sampling description: Intertidal collections were made at low tide by walking over the shore. Subtidal collections were made by scuba diving. In each sampling location, one or two specimens of all different species found were scraped into labelled bags (Fig. 7).
Complementary data, such as shore level (high, mid, low), orientation and type of substrate (bedrock, boulders, mixed), habitat (tide pool, open rock, gully, crevice) were also recorded.
Quality control: Each sampled taxon was 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.
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 the observation of the entire thallus with the naked eye and/or using dissecting and compound microscopes. For larger and more complex algae, the investigation of thalli anatomy required histological work to obtain longitudinal and transverse sections needed for the observation of cells, reproductive structures and other diagnostic characters.
Due to the mixed nature of the Azorean macroalgal flora, relevant floras from the Atlantic and western Mediterranean were used for the 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 herbarium of the Natural History Museum (London) for comparison with collections there. Collecting macroalgae at the rocky intertidal (by the Island Aquatic Ecology Subgroup of cE3c-ABG).
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 further research planned, 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) and (ii) dried collections, either by pressing the algae (most species) following the method described by Gayral and Cosson (1986).
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, 90 taxa were identified comprising 71 confirmed species, belonging to 22 orders and 37 families, distributed by the phyla Rhodophyta (13 orders and 24 families), Chlorophyta (3 orders and 6 families) and Ochrophyta (6 orders and 7 families) (see Tables 2, 3).   Table 3.

Phylum Species (Accepted Name) Number of records
Main taxonomic figures with information on the species origin and status.

Notes:
The sampling was performed in the summers of 1990 and 1991.

Collection identifier:
de350d60-48c0-409c-a71f-0ae4df753fde; 2d4aad32-17f3-426e-92f1-3d8654fc781e. Description: This data paper presents data from macroalgae surveys developed in Formigas Islets in 1990(Neto et al. 2020. 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 eight records (eventID). The extension data table has 320 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. A mismatch regarding the GBIF backbone taxonomy of some of the macroalgae species names was identified as detailed in Suppl. material 1.