Biota from the coastal wetlands of Praia da Vitória (Terceira, Azores, Portugal): Part 1 - Arthropods

Abstract Background During a LIFE research project aiming at the implementation of the conservation of the habitats and restoration of coastal wetland areas of Praia da Vitória (Terceira, Azores, Portugal), there was the opportunity undertake a systematic record of several groups of arthropods in three wetland areas: Paul da Praia da Vitória (PPV), Paul do Belo Jardim (PBJ) and Paul da Pedreira do Cabo da Praia (PPCP). The objective of the study was to perform a rapid biodiversity assessment, comparing the three sites in two different years, before and after the implementation of several conservation measures. This project also contributed to improve the knowledge of Azorean arthropod diversity at both local and regional scales, including new taxa for Terceira island and new records for Azores. Taking into consideration those aims, a set of standardised sampling methods were performed, inspired by the COBRA protocol originally developed for spiders. New information A total of 15,810 specimens belonging to 216 arthropod species and subspecies were collected. Beetles (Insecta, Coleoptera) and spiders (Araneae) dominated, with 81 and 51 taxa, respectively. Two beetle families dominated, Staphylinidae and Curculionidae with, respectively, 22 and 17 species and subspecies. Exotic species were also dominant (132 species and subspecies), the Azorean endemics being restricted to only eight taxa. The remaining 76 species and subspecies are native non-endemic. Two rare endemic species were found with relatively sustainable populations, the Azores Cone-head Conocephalus chavesi (Orthoptera, Tettigoniidae) and the true weevil Drouetius oceanicus oceanicus (Coleoptera, Curculionidae). A total of six species are novel for the Azores, five exotic (Bledius unicornis, Carpelimus zealandicus, Oenopia doublieri, Sitona hispidulus, Trichiusa immigrata) and one possibly native (Pyrrhocoris apterus). An additional 15 taxa are novel for Terceira island, ten exotic (Cheiracanthium mildei, Cylindroiulus latestriatus, Eumodicogryllus bordigalensis, Nemobius sylvestris, Pissodes castaneus, Psyllipsocus ramburi, Trachyzelotes lyonneti, Trigonnidium cicindeloides, Tychius cuprifer, Zelotes tenuis) and five native (Aegialia arenaria, Oxypoda lurida, Platycleis sabulosa, Plinthisus brevipennis, Tachyura diabrachys).


Introduction
The terrestrial coastal lines of the Azores include important wetland areas, namely salty lakes. These habitats were subject to intense human disturbance and, after almost 600 years of human occupancy, only very few coastal wetland habitats still persist in these Atlantic islands. Despite these impacts, three small areas are still available in Terceira Island: i) a native but highly modified coastal saltmarsh habitat, Paul Praia da Vitória (PPV); ii) a new coastal saltmarsh that was created by rehabilitation of the quarry at Cabo da Praia, Paul da Pedreira do Cabo da Praia (PPCP) (Morton et al. 1997); iii) a wetland included in a dune area, the Paul do Belo Jardim (PBJ). The knowledge of the arthropod fauna of these habitats was until recently very incipient, but more recently, the LIFE project "Ecological Restoration and Conservation of Praia da Vitória Coastal Wet Green Infrastructure" (2013-2018) implemented a two-year inventory and monitoring of the biota in these wetland areas. As a consequence, a first survey was conducted in 2016 in order to compare the diversity of arthropods in ground and aerial habitats (herbaceous, shrubs and trees) in the referred wetland areas (Borges et al. 2017). A second survey was performed in 2017, repeating the same sampling protocols with some additional sampling.

General description
Purpose: In this contribution, we present detailed data on the distribution and abundance of species belonging to several groups of arthropods in three Terceira Island (Azores) wetlands during two years (2016)(2017). In addition, we list the new taxonomic records for the Azores or Terceira Island. In doing this, we are contributing to address two key biodiversity shortfalls (see : i) the need for improving current information on the local and regional distribution of Azorean arthropods (the Wallacean shortfall); and ii) the need for collecting abundance data for future monitoring purposes (the Prestonian shortfall).

Project description
Title: The inventory of selected groups of terrestrial arthropods in three coastal wetlands from Terceira Island (Azores) Personnel: The inventory was conducted during two years (2016)(2017) under the responsibility of Paulo A. V. Borges with constant participation of César Pimentel. For the night sampling, additional help in the field was provided by Rosalina Gabriel and Mariana Brito. A large group of taxonomists contributed for the species identification: Luís Crespo (Araneae); Artur Serrano (Insecta, Coleoptera); Volker Assing and Michael Schülke (Coleoptera, Staphylinidae); António O. Soares (Coleoptera, Coccinellidae); Simone Fattorini (Coleoptera, Tenebrionidae); Peter Stüben (Coleoptera, Curculionidae). Finally, in the lab, we had the support of Alejandra Ros-Prieto in vouchers management for the University of Azores Insect Collection "Dalberto Teixeira Pombo" and Enésima Mendonça for the database management.
Study area description: Terceira Island (area: 400.6 km²; elevation: 1,021.14 m) is one of the nine islands from the Azores archipelago, located in the North Atlantic, roughly at 38°4 3′49″N 27°19′10″W. The climate in the Azores is temperate oceanic, with regular and abundant rainfall, with high levels of relative humidity and persistent winds, mainly during the winter and autumn seasons.
Terceira Island is known for the presence of some very important pristine areas at high elevation (Gaspar et al. 2011). However, few natural areas still remain at lower elevations, notably in Praia da Vitória county. Three wetland areas, Paul da Praia da Vitória (PPV), Paul do Belo Jardim (PBJ) and Paul da Pedreira do Cabo da Praia (PPCP) (Figs 1, 2) were studied in this project. Coastal vegetation dominates, namely Juncus acutus and still includes some arboreal cover by the native shrub Morella faya. The Erica-Morella coastal woodlands as described in Elias et al. (2016) are not present and the exotic invasive species Arundo donax is very common.
The PPV (Fig. 1) was a large coastal salty marshland with associated dunes, which was largely transformed and reduced for urban development and underwent several dynamic changes in the last 500 years of human occupation. After some major work performed between 2006 and 2010, PPV is currently characterised by a large waterbody with islands  of Juncus acutus isolated by channels (Fig. 2). PBJ was originally one of the largest dune areas from the Azores (Fig. 3), but after the construction of the Praia da Vitória harbour, it was reduced to a very small wetland area, with a dune covered partially by J. acutus (Fig. 4). Of particular relevance is the presence of a small stream adding some diversity of vegetation and arthropods (Borges et al. 2017). The case of PPCP is completely different, since this is a recently created wetland (Fig. 5), resulting from the removal of large amounts of stones for the construction of the Praia da Vitória harbour, around 1980 (Fig. 6). As a consequence a new ecosystem was created, the quarry of Cabo da Praia (Morton et al. 1997).  Biota from the coastal wetlands of Praia da Vitória (Terceira, Azores, ...

Design description:
In each of the three wetland areas, transects were setup to allow the sampling of epigean arthropods in the main habitats.
In PPV, three main transects were setup: i) PPV-T200 (Paul da Praia Vitória -Margins) that covers the main margins of the water bodies; ii) PPV-T201 (Paul da Praia Vitória -Island) that covers some of the isolated islands; iii) PPV-T205 (Paul da Praia Vitória -Cerrado São Lazaro) to sample an historical locality with a high diversity of ground-beetle species (Borges 1995;Borges et al. 2017).  In PBJ, two transects were setup: i) PBJ-T203 (Paul do Belo Jardim -Margins), which was located within the Juncus acutus plants; ii) PBJ-T204 (Paul do Belo Jardim -Stream), which was setup in a small stream.
In PPCP, only one transect was setup, PPCP-T202 (Paul da Pedreira do Cabo da Praia -Margins), which covers the main margins of the water.
The beating and sweeping samples were conducted both during the day and night and were undertaken by walking randomly within the sites.

Sampling methods
Study extent: This study covers a small coastal area with 3.58 km extension between PPV and PPCP.
Sampling description: In each site, arthropods were sampled during the summers of 2016 and 2017 using a combination of standardised methods inspired by the COBRA protocol (Cardoso 2009 were placed immediately outside the perimeter of each lake, spaced 10 metres apart. Traps were filled with 3-4 cm of 100% propylene glycol and left in the field for seven days. Traps were protected from predation, inundation with rainwater and unwanted vertebrate capture by using plates sitting on stilts 2 cm above the ground surface. In PBJ, two transects were performed with 30 traps in the main transect and 15 traps in a secondary transect covering a small stream. In PPV and PPCP, single transects of 30 traps each were setup in the margins of water bodies. In PPV, half of the traps were in the margins of the largest "island". In 2017, additional traps were setup in Cerrado São Lazaro (PPV-T205 Paul da Praia Vitória).
For each site, a total of four samples of AAS, 20 samples of FB, two samples of FS and 30 main samples of PIT were obtained, totalling 56 samples per site and an overall 168 samples in 2017. Further, in 2017, additional pitfall traps in the PBJ small stream added 15 more samples totalling 183 samples. The main 56 samples per site included the sampling of two main sub-habitats, the aerial vegetation with 26 samples (20 beatings during the day, two sweeps during the day and four night aerial searches) and the ground habitat with 30 pitfall samples.
In 2017, the additional samples made during the night added four samples for each site, totalling 60 samples per site. Accumulation curves were performed and completeness was high for all sites (see Borges et al. 2017).

Quality control:
The correct identification of the sampled taxa is crucial. We followed a three-step process to identify arthropod species: (1) for arthropod orders for which there was taxonomic expertise, one of us (CP) performed morphospecies sorting using a parataxonomy approach (see Oliver and Beattie 1993) with a reference collection; (2) a trained taxonomist (PAVB) corrected all the splitting and lumping errors and identified most of the species; and 3) the morphospecies for which a correct identification was not possible were sent to experts for identification. Taxonomic nomenclature followed the arthropod checklist in Borges et al. (2010)  Description: In this data table, we include all the records for which a taxonomic identification of the species was possible. 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 has been published as a Darwin Core Archive (DwC-A), which is a standardised format for sharing biodiversity data as a set of one or more data tables. The core data table contains 343 records. One extension data table also exists. 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. The versions table lists other versions of the resource that have been made publicly available and allows tracking changes made to the resource over time.
In Suppl. material 1, we provide a simpler dataset with few columns in a single table. Insecta endemic species in PBJ, the Azores Cone-head Conocephalus chavesi (Orthoptera, Tettigoniidae) (Fig. 7), that was recently listed as Endangered by IUCN (Hochkirch and Borges 2016) and the true weevil Drouetius oceanicus oceanicus (Coleoptera, Curculionidae) (Fig. 8), that was recently listed as Endangered by IUCN (see Borges and Lamelas-López 2018). The Azores Cone-head Conocephalus chavesi was also found in the two other sites but with lower abundance.

Known ranges and ecology of newly reported species
Twenty-one species, which represent 10% of the total species collected, are new records for either the Azores and Terceira island (six species) or only Terceira Island (15 species). The new species for the Azores include five exotic and one possibly native species. The 15 new records for Terceira island include ten exotic and five native species (see also Table  1).

Diplopoda -Julida
-  Borges et al. (2013) and now also found in Terceira. This is a southern Europe (Mediterranean area) native species, but occurs also on the Canary Islands, Africa, Madagascar, China, Japan and Korea. This species if frequently found associated with ponds. Captured with pitfall traps.
-Pyrrhocoris apterus (Linnaeus,1758) (new for the Azores). This is a very common and widespread Palaearctic species. This is possibly a native species from Azores. Captured with pitfall traps, but also associated with Arundo donax.

Insecta -Psocoptera
-Psyllipsocus ramburi Sélys-Longchamps, 1872 (new for Terceira island). Previously recorded on two islands (S. Miguel and S. Maria). This is an exotic species in Azores and native from West Palaearctic. Captured with pitfall traps, this species is usually associated with damp sites (Robinson 2005).

Insecta -Coleoptera
-Aegialia arenaria (Fabricius, 1787) (new for Terceira island). Previously recorded on a single island (S. Miguel). This is a native dune scarab beetle species in Azores and native from West Palaearctic. Captured with pitfall traps, this species is commonly associated with coastal dune areas.
-Bledius unicornis (Germar, 1825) (new for the Azores). This is a common rove-beetle species distributed from the Atlantic Islands across Europe and the Mediterranean eastwards to Middle Asia (Schülke and Smetana 2015). Captured with pitfall traps, this species is adapted to damp areas, particularly salt-marsh areas (Zanella and Scarton 2017).
-Carpelimus zealandicus (Sharp, 1900) (new for the Azores). Originally most likely from the Australian Region, this species is adventive in Europe, with confirmed records from Central Europe, the British Isles and Scandinavia (Schülke and Smetana 2015). Captured with pitfall traps.
-Oenopia doublieri (Mulsant, 1846) (new for the Azores). This exotic species is native from the Mediterranean region. The species was recently recorded also in Morocco and associated with citrus orchards (Smaili et al. 2009). This is, possibly, a recent introduction in the Azores. The species was found associated with the invasive Arundo donax.
-Oxypoda lurida Wollaston, 1857 (new for Terceira island). Previously recorded on a single island (S. Maria). Oxypoda lurida is a widespread and mostly parthenogenetic species distributed from the Atlantic Islands across Europe and the Mediterranean eastwards to Turkey and Cyprus) (Schülke and Smetana 2015). Captured with pitfall traps.
-Pissodes castaneus (De Geer, 1775) (new for Terceira island). Previously recorded on four islands (Faial, Pico, S. Miguel and S. Maria). The small banded pine weevil is a cosmopolitan species commonly associated with pines, the larval stage having some impact on adult trees. This species is considered invasive (Pestaña and Santolamazza-Carbone 2010) and is widespread on all Macaronesian islands (Stüben 2018) where pines from Europe (e.g. Pinus sylvestris) were introduced. Captured with pitfall traps.
-Sitona hispidulus (Fabricius, 1777) (new for the the Azores). Known as Clover Root Curculio, this species is native to and widespread throughout Eurasia, but also introduced in North America (Quinn and Hower 1986). Captured with pitfall traps. This species has a short-winged and a long-winged form and prefers stands of Trifolium (especially T. repens) on damp and relatively dry localities and with a minor preference also for Medicago and Vicia. It seems to have just arrived into the Azores, otherwise this Sitona species could/ should have been found even before.
-Tachyura diabrachys (Kolenati, 1845) (new for Terceira island). Previously recorded on a single island (S. Maria). This is a west European species. Captured with pitfall traps, this is a species usually associated with damp areas.
-Trichiusa immigrata Lohse, 1984 (new for the Azores; Note: there is a mention of this species in the latest edition of the Palaearctic Catalogue, but we have no idea who published the primary record). Originally from North America, this adventive rove-beetle species was first recorded from Central Europe by Lohse (1984) and is now widespread and common in the West Palaearctic region from the Atlantic Islands eastwards to Russia and Ukraine. It is usually found in decomposing plant material and in the leaf litter (Moore 2004). The material from the Azores was found in grassland.
-Tychius cuprifer (Panzer, 1799) (new for Terceira island). Previously recorded on a single island (S. Miguel). It is also reported from Madeira in 2015 for the first time, collected in multifunnel traps (Stüben 2018). It is most probably introduced with Fabaceae (forage). T. cuprifer is a xerothermophilous species from South Europe and North Africa (uninterruptedly until Turkmenistan) and develops mainly on Trifolium arvense (it is also called T. pratense and T. stellatum (CURCULIO_Team 2010).