Biota of coastal wetlands of Praia da Vitória (Terceira Island, Azores): Part 2 - Bryophytes

Abstract Background During the LIFE-CWR project "Ecological Restoration and Conservation of Praia da Vitória Coastal Wet Green Infrastructures", there was the opportunity to undertake a systematic record of bryophytes at Paul da Praia da Vitória (PPV), Paul do Belo Jardim (PBJ) and Paul da Pedreira do Cabo da Praia (PPCP), three coastal wetland areas of Praia da Vitória (Terceira, Azores, Portugal). The objective of the study was to perform a biodiversity assessment, comparing the three sites at two different moments, before and after the implementation of several conservation measures. This project also contributed to improve the knowledge of Azorean bryophyte diversity at both local and regional scales, including the recording of two new taxa for the Azores and three new taxa for Terceira Island. New information This paper reports the results of the first extensive survey of bryophyes of the three coastal wetland areas of Praia da Vitória (Terceira Island, Azores, Portugal). The identification of a total of 504 samples, 240 collected in 2013 and 2016 (before the LIFE-CWR intervention) and 265 in 2017 and 2018 (after the intervention), resulted in a list of 58 species of bryophytes (one hornwort, eight liverworts and 48 mosses). These include two new records for the Azores (Bryum klinggraeffii, Ptychostomum bornholmense), three new records for Terceira Island (Bryum tenuisetum, Dicranella howei, Trichostomum crispulum) and at least 15 new records for the municipality of Praia da Vitória (e.g., Cephaloziella hampeana). Some species that had not been recorded on the island since 1937 (e.g., Fissidens crispus) were collected during this study, as well as a Macaronesian endemic liverwort (Radula wichurae), an Iberian-Macaronesian liverwort (Frullania azorica) and a moss species with European distribution (Ptychomitrium nigrescens). From the recorded species, only one moss (Leptophascum leptophyllum), of subtropical origin, is considered invasive in Europe.


Introduction
Bryophytes are small plants without vascular tissues, directly depending on immediate environmental conditions. Most species are poikilohydric, i.e., lacking the ability (structural or functional) to maintain and/or regulate water content to achieve homeostasis of cells and tissue. Because they are so dependant on their immediate environment, they respond quickly to environmental change, which makes them good bioindicators of changes in land use, precipitation regime, temperature, salinity and pollution.
The Azores archipelago is well-known for its rich bryoflora (480 species and subspecies) (Gabriel et al. 2010), which may be related to the high humidity and mild temperatures, influenced by the Atlantic Ocean, and scarce pollution sources.
Although the coastal areas of the islands are among their most deteriorated habitats, mainly due to urbanization pressure, some interesting, though fragmented, ecosystems remain at lower elevations in the Azores. The three coastal wetlands of Praia da Vitória municipality are a case in point, well worth restoration and habitat protection. The areas, studied during the LIFE-CWR Project -Paul da Praia da Vitória (PPV), Paul do Belo Jardim (PBJ) and Paul da Pedreira do Cabo da Praia (PPCP) -are best known for their birds (Barcelos et al. 2015;Dias 2018;Goulart et al. 2019); however, they harbour other important and interesting biological groups, such as molluscs and arthropods (Martins and Borges 2019), plants and lichens (Elias et al. 2019).
The coastal areas of the Azorean Islands are not thoroughly studied, since bryologists tend to focus on the rich natural forests of the archipelago (e.g., Aranda et al. 2011) and the bryophytic flora of these coastal wetlands had never been systematically sampled. This is the second contribution in a series of papers  intending to characterize the biota of the three areas.

General description
Purpose: The main aim of this work was to inventory the bryophyte species present in Paul da Praia da Vitória (PPV), Paul do Belo Jardim (PBJ) and Paul da Pedreira do Cabo da Praia (PPCP), three neighbouring areas focused on by the restoration project LIFE-CWR, in order to improve knowledge on the regional distribution of bryophytes (mosses, liverworts, hornworts) and set a baseline for future research in the area.

Project description
Title: Inventory of bryophytes in three coastal wetlands of Terceira Island (Azores)  Table 1. Species identifications were performed by César Pimentel under the supervision of Rosalina Gabriel (2016and 2017), and David Claro (2013  Study area description: Terceira Island (area: 400.6 km²; elevation: 1,021.14 m) is one of the nine islands of the Azores archipelago, located in the North Atlantic, roughly at 38°43′ 49″N, 27°19′10″W (Forjaz 2004). The climate in the Azores is temperate oceanic, with regular and abundant rainfall, high levels of relative humidity and persistent western winds, mainly during the winter and autumn seasons (Azevedo et al. 2004).
Terceira Island is known for the presence of some very important native forest areas at high elevation (e.g., Gabriel and Bates 2005      Potentially, the plant cover of Praia da Vitória would include Erica-Morella coastal woodlands (cf. Elias et al. 2016). However, apart from some native shrubs of Morella faya, still found in PPV and PPCP, the main native species found in the area include species typical of humid zones, namely Juncus (J. acutus, J. maritimus, J. effusus) and Ruppia maritima (Elias et al. 2019). Presently, most of the area is covered with exotic and invasive species, with the giant cane (Arundo donax), being especially abundant in PBJ, and the sticky snakeroot (Ageratina adenophora) in PPCP. Both these species are included in the first quartile of invasive species in the three archipelagos of Macaronesia (Silva et al. 2008). The bryophytic component of the flora had previously not been systematically studied in the area.

Design description:
In each wetland, a network of three (PBJ) or four (PPV, PPCP) transects (160 m × 2 m or 300 m × 2 m), was set and sampled every 20 m (ocasionally every 10 m), in quadrats/sampling points of 4 m ; each quadrat was searched for bryophytes. Whenever possible, a maximum of six samples or microplots (10 cm × 5 cm) were collected: three replicates from soil and three replicates from rock. Bryophyte samples were brought to the laboratory for identification and herborization at the Herbarium of the University of Azores (AZU) -section Bryophytes.
In 2018, after the project's completion, the areas continued to be visited and in one of those visits a new species for the Paul da Pedreira do Cabo da Praia location was collected.

Sampling methods
Study extent: This study coverered a small coastal area, extending from PPV (to the North) to PPCP (to the South), with an extent of 3.58 km.

Sampling description:
In each site, bryophytes were sampled using standardised methods, during one or two visits in 2013, 2016 and 2017, respectively (Table 1). Within each transect, a quadrat with an area of 4 m was delimited at intervals of 10 or 20 meters. Each sampling point (quadrat) was carefully examined to collect three samples (replicates or microplots) for each of the available substrates (soil, rock); microplots were randomly selected from areas colonized by bryophytes. The area collected in each replica (microplot) was 50 cm (10 cm × 5 cm). The maximum number of samples obtained per sampling point was six (three replicates of bryophytes growing on soil and three of bryophytes growing on rock), but many sampling points did not contain bryophytes, especially those located in areas periodically flooded with brackish waters. For each microplot, some ecological variables were also measured (e.g., insulation, water availability) using ordinal scales adapted from Gabriel and Bates (2005), and some soil or rock was recovered for pH measurement.
Quality control: The correct identification of the sampled taxa is crucial in an inventory. Keys and floras were used to identify the species, and their coverage (in %) was also estimated for each microplot in the laboratory. The main floras used for the identification of liverworts were by Paton (1999) and Casas et al. (2009), whereas for mosses Smith (2004), Casas et al. (2006) and different volumes of "Flora Briofítica Ibérica" (Guerra 2018) were used. Taxonomic keys provided by Schumacker and Váňa (2005) and field guides (Atherton et al. 2010, Llimona et al. 2004 were also checked. Some important internet databases were consulted, namely the Azorean Biodiversity Portal and TROPICOS for taxonomic data and BBS Field Guide online pages, Bildatlas der Moose Deutschlands and Swissbryophytes for morphological and ecological data. Nomenclature mostly follows Gabriel et al. (2010)

Additional information
The identification of the samples (242 before the LIFE-CWR intervention [2013,2016], 261 after it [2017]) resulted in a set of 57 species of bryophytes, including one hornwort, eight liverwort species (Table 2) and 48 moss species (Table 3), representing about 80% of the bryophyte species present in the three sampled areas, according to the first-order Jackknife estimator (Table 4)   Comparison between years (before and after CWR intervention): The main interventions performed by the LIFE-CWR project in the three coastal areas included the removal of garbage and litter from PPCP, the opening of a small lagoon in PBJ and the connection of PPV to the sea.
The number of species varied slightly before and after the interventions, but the level of completeness is acceptable, higher than 75%, for both sampling periods (Table 4). The highest value of bryophyte species richness was observed in Paul da Pedreira do Cabo da Praia, probably due to the availability of a higher proportion of rocky substrata, while the lowest richness value was observed in Paul da Praia da Vitória.
A Ward's dissimilarity analysis performed with the diversity of species found at the three studied wetlands shows a remarkable homogeinity of results between the studied years ( Fig. 7). Thus, the LIFE-CWR restoration interventions, especially focused on the improvement the bird habitat and water flow, did not hinder the conservation of bryophytes. Noteworthy species: Among the observed species, two represent new records for the Azores, Bryum klinggraeffii (Ellis et al. 2016) and Ptychostomum bornholmense (Ellis et al. 2018). There are also three new records for Terceira Island (Bryum tenuisetum, Dicranella howei and Trichostomum crispulum) and at least 15 new recordsfor the municipality of Praia da Vitória, including the moss Leucodon sciuroides, a species previously known only from Monte Brasil (Angra do Heroísmo, Terceira Island) (Fontinha and Sérgio 1995) and which has been declining in the United Kingdom (Blockeel et al. 2014), and the liverwort Cephaloziella hampeana, also known from a single location on Terceira Island (Algar do Carvão) (Crundwell et al. 2013).

Main biogeographic distribution of the species:
Some species that had not been recorded on Terceira Island since 1937 (e.g., Fissidens crispus)  were found on the wetlands, which may be explained by a lack of fieldwork at low elevations on the island .
A Macaronesian endemic liverwort (Radula wichurae) and an Iberian-Macaronesian liverwort (Frullania azorica; Fig. 8) were found growing on rocks in the different wetlands. Actually, Praia da Vitória county, parish of Cabo da Praia, represents the classical locality of Frullania azorica, the place from where the species was originally collected and described (Sim-Sim et al. 1995). This species is frequently found in the area, sometimes forming extensive colonies on exposed rocks near the ocean. However, in this study, it was not identified in Paul da Praia da Vitória, possibly because there are not many rocks available for colonization.
The acrocarpic moss species Ptychomitrium nigrescens, endemic to Europe and Macaronesia (Macaronesia, Portugal and France), was also reported from Paul da Pedreira do Cabo da Praia (PPCP), where boulders and large rocks are available for colonization.
Further details related to the LIFE-CWR project can be found in the book by Brian Morton, Elisabete Nogueira and António Frias Martins (Morton et al. 2019) and in the report by RG . The liverwort Frullania azorica was described from material collected in the Praia da Vitória area (Photo by Rosalina Gabriel).