Biodiversity Data Journal : Data Paper (Biosciences)
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Data Paper (Biosciences)
Standardised inventories of spiders (Arachnida, Araneae) on touristic trails of the native forests of the Azores (Portugal)
expand article infoRui Carvalho‡,§, Pedro Cardoso§,, Artur Gil|, Maria Teresa Ferreira, Cândida Ramos, Lucas Lamelas-Lopez, Fernando Pereira, Jagoba Malumbres-Olarte‡,§, Alejandra Ros-Prieto, Mário Boieiro, Paulo A. V. Borges‡,
‡ cE3c – Centre for Ecology, Evolution and Environmental Changes / Azorean Biodiversity Group and Universidade dos Açores, Rua Capitão João d’Ávila, São Pedro, 9700-042, Angra do Heroísmo, Portugal
§ Laboratory for Integrative Biodiversity Research (LIBRe), Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland
| cE3c – Centre for Ecology, Evolution and Environmental Changes / Azorean Biodiversity Group and Universidade dos Açores, Ponta Delgada, Portugal
¶ IUCN SSC Mid-Atlantic Islands Specialist Group, Angra do Heroísmo, Portugal
Open Access

Abstract

Background

The sharp increase in tourist visitation of the Azores Archipelago from 2015 onwards raised concerns about the impacts of recreational tourism on native habitats. In response, a project was financed by the Azorean Government to investigate the drivers of biodiversity erosion associated with recreational tourism. Here, we present the data on spider biodiversity found on trails located within the native Azorean forests as they are home to several endemic species of great conservation value. We applied an optimised and standardised sampling protocol (COBRA) in twenty-three plots located in five trails on Terceira and São Miguel Islands and assessed diversity and abundance of spider species at different distances from the trail head and the trail itself.

New information

Of the 45 species (12435 specimens) collected, 13 were endemic to the Azores (9690 specimens), 10 native non-endemic (2047 specimens) and 22 introduced (698 specimens). This database will be the baseline of a long-term monitoring project for the assessment of touristic impacts on native forest trails. This methodology can also be used on other habitats and biogeograhical regions.

Keywords

Arthropoda, hiking, recreation ecology, Macaronesia, endemic species, checklist

Introduction

In the Azores, as in many other temperate, semi-tropical and tropical islands, historical patterns of habitat loss have typically resulted in lowland clearance, meaning that the last remnants of the pre-human pristine forest that covered the major parts of oceanic islands are in the mountain areas (Gaspar et al. 2011). The communities of these mountain forests are of critical importance for the protection of current island biodiversity since they are home to many Azorean endemic species (Borges et al. 2017, Borges et al. 2018, Malumbres-Olarte et al. 2019) and provide a variety of ecosystem services (e.g. water storage, erosion control, pollination, pest-control, food supply, recreation and tourism), contributing to the local economy and welfare (Fernandez-Palacios et al. 2017).

The recent increase in recreational tourist activities in native habitats of the Azores (SREA 2018) raises concerns about the use of trails being a threat to the already imperilled native forest biodiversity. Hiking trails in particular have been found to be promoting the spread of invasive plants (Barros and Pickering 2014), which may cause adverse cascading effects on arthropods.

The spider communities of the Azores are exceptionally well known due to ongoing inventorying and monitoring projects carried out since 1999 (Borges et al. 2016, Emerson et al. 2017, Malumbres-Olarte et al. 2019). The protocol used in NETBIOME ISLANDBIODIV and in this project is part of a long term monitoring proposal for oceanic islands (Borges et al. 2018).

General description

Purpose: 

We aimed to characterise the richness and abundance of spiders in areas surrounding trails in native Azorean forest and to assess if the distance to the head of hiking trails or to the trail itself explains shifts in spider community composition, compared with areas undisturbed by tourists.

Project description

Title: 

Spiders (Arachnida, Araneae) from Azorean native forest trails

Personnel: 

Rui Carvalho led the sampling in the field with the participation of Alejandra Ros-Prieto, Cândida Ramos, Fernando Pereira, Jagoba Malumbres-Olarte, Maria T. Ferreira, Mário Boieiro, Lucas Lamelas-López and Paulo A. V. Borges.

Study area description: 

We focused on the Azorean forests of Terceira and São Miguel Islands, as they have pedestrian trails going through native forests with a relevant level of visitation (Fig. 1). Terceira Island (area: 400.6 km²; elevation: 1021.14 m) and São Miguel Island (area: 744.6 km²; elevation: 1103 m) are two of the nine islands from the Azores Archipelago. The climate in the Azores is temperate oceanic, with regular and abundant rainfall, with high levels of relative humidity and persistent winds, mainly during winter and autumn seasons. Terceira Island is known for the presence of some very important pristine areas at high elevation (Gaspar et al. 2011).

Figure 1.  

Location of trails in Terceira: Lagoinha (pink), Santa Bárbara (yellow), Mistérios Negros (blue), Guilherme Moniz (red); in S. Miguel: Malhadas (purple).

Funding: 

This research was supported by the Rui Carvalho Ph.D. DRCT scholarship from the Azores Government (M3.1.a/F/135/2015). Data was obtained mostly during the Ph.D. DRCT scholarship, but some samples ("Control 250", see below) are from a previous project (ERA-Net NetBiome research framework, financed through Portuguese FCT-NETBIOME ISLANDBIODIV grant 0003/2011).

Sampling methods

Description: 

We selected six 50 x 50 m sampling sites in native forest patches along the studied trails, at increasing distances from the trail head: 0 m, 50 m and 250 m. Another sampling site, termed Max, was set independently from distance - it was located where the forest adjacent to the trail was most pristine. Finally, two control sites were selected at 50 m and 250 m from the closest trail point (Table 1). This setup is repeated at each trail. In Terceira, the Control 250 data were retrieved from NETBIOME-ISLANDBIODIV samples from 2012 (see Malumbres-Olarte et al. 2019).

Table 1.

Island, fragment, trail name and coordinates of sampling sites

Island Fragment Trail Sampling sites Latitude Longitude
Terceira Santa Bárbara Lagoinha 0 38.7496 -27.3340
Terceira Santa Bárbara Lagoinha 50 38.74946 -27.3333
Terceira Santa Bárbara Lagoinha 250 38.7497 -27.3320
Terceira Santa Bárbara Lagoinha Control 50 38.7496 -27.3304
Terceira Santa Bárbara Lagoinha Control 250 38.7521 -27.3313
Terceira Santa Bárbara Mistérios Negros 0 38.7383 -27.2786
Terceira Santa Bárbara Mistérios Negros 50 38.7383 -27.2789
Terceira Santa Bárbara Mistérios Negros 250 38.7390 -27.2801
Terceira Santa Bárbara Mistérios Negros Max 38.7394 -27.2824
Terceira Santa Bárbara Mistérios Negros Control 50 38.7390 -27.2819
Terceira Santa Bárbara Mistérios Negros Control 250 38.7372 -27.2899
Terceira Santa Bárbara Santa Bárbara 0 38.7322 -27.3111
Terceira Santa Bárbara Santa Bárbara 50 38.7325 -27.3106
Terceira Santa Bárbara Santa Bárbara 250 38.7336

-27.3088

Terceira Santa Bárbara Santa Bárbara Max 38.7347 -27.3073
Terceira Santa Bárbara Santa Bárbara Control 50 38.7348 -27.3090
Terceira Santa Bárbara Santa Bárbara Control 250 38.7356 -27.3074
Terceira Guilherme Moniz Guilherme Moniz 0 38.7087 -27.1904
São Miguel Pico da Vara Malhadas 0 37.8170 -25.1848
São Miguel Pico da Vara Malhadas 50 37.8164 -25.1855
São Miguel Pico da Vara Malhadas 250 37.8157 -25.1864
São Miguel Pico da Vara Malhadas Max 37.8163 -25.1900
Sampling description: 

The inventory COBRA (Conservation Oriented Biodiversity Rapid Assessment) protocol (Cardoso 2009) was used at the most pristine area in the studied fragment, firstly to assess whether completeness is sufficient to use the less time-intensive protocols; secondly, in order to be used as alpha and beta diversity baselines (Borges et al. 2018). It is composed of four hours of aerial search, four hours of tree beating, four hours of vegetation sweeping and pitfall sampling using 48 traps. The traps containing propylene glycol were active for 15 days and, during sample collection, they were arranged in groups of four to make 12 sample units. For the remaining sampling areas of each trail, the much less intensive monitoring COBRA protocol was used. It is composed of four hours of aerial search and two hours of beating trees using a drop cloth (see Borges et al. 2018 for details). The COBRA protocol has been proposed as part of standard inventorying and monitoring programmes targeting spiders and beetles and has been used on island and continental ecosystems, from subarctic regions to the tropics (Cardoso 2009, Borges et al. 2018, Malumbres-Olarte et al. 2019, Malumbres-Olarte et al. 2020).

Quality control: 

All the spider specimens were first sorted into morphospecies by R Carvalho and later identified by a trained taxonomist (one of the authors: PAV Borges).

Geographic coverage

Description: 

Terceira and São Miguel Islands, Azores, Portugal

Bounding Coordinates: South West [37.579, -27.466], North East [39.045, -25.049]

Taxonomic coverage

Taxa included:
Rank Scientific Name Common Name
order Araneae Spiders

Traits coverage

Macías-Hernández et al. (2020) published the database of functional traits for all species in the study.

Temporal coverage

Notes: 

July to August 2012 for the Control 250 samples; July to October 2017 for all other samples.

Collection data

Collection name: 
Dalberto Teixeira Pombo insect collection at the University of Azores.
Collection identifier: 
DTP
Specimen preservation method: 
All specimens were preserved in 96% ethanol.
Curatorial unit: 
Dalberto Teixeira Pombo insect collection at the University of the Azores (Curator: Paulo A. V. Borges)

Usage licence

Usage licence: 
Open Data Commons Attribution License
IP rights notes: 

CC-BY 4.0

Data resources

Data package title: 
Diversity of Spiders from Azorean Trails
Alternative identifiers: 
Number of data sets: 
1
Data set name: 
Diversity of Spiders from Azorean Trails
Data format: 
Darwin Core Archive
Data format version: 
version 1
Description: 

The following data table includes all the records for which a taxonomic identification of the species was possible. The dataset submitted to GBIF (Global Biodiversity Information Facility) 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 file contains 194 records (eventID) and the occurrences file 1290 records (occurrenceID). This IPT (integrated publishing toolkit) archives the data and thus serves as the data repository. The data and resource metadata are available for download from Carvalho et al. (2021).

Column label Column description
Table of Sampling Events Table with sampling events data (beginning of table)
id Unique identification code for sampling event data
eventID Identifier of the events, unique for the dataset
stateProvince Name of the region of the sampling site
islandGroup Name of archipelago
island Name of the island
country Country of the sampling site
countryCode ISO code of the country of the sampling site
municipality Municipality of the sampling site
decimalLongitude Approximate centre point decimal longitude of the field site in GPS coordinates
decimalLatitude Approximate centre point decimal latitude of the field site in GPS coordinates
geodeticDatum The ellipsoid, geodetic datum or spatial reference system (SRS) upon which the geographic coordinates given in decimalLatitude and decimalLongitude are based
coordinateUncertaintyInMetres Uncertainty of the coordinates of the centre of the sampling plot
coordinatePrecision Precision of the coordinates
georeferenceSources A list (concatenated and separated) of maps, gazetteers or other resources used to georeference the Location, described specifically enough to allow anyone in the future to use the same resources.
locationID Identifier of the location
locationRemarks Details on the locality site
locality Name of the locality
minimumElevationInMetres The lower limit of the range of elevation (altitude, usually above sea level), in metres.
maximumElevationInMetres The upper limit of the range of elevation (altitude, usually above sea level), in metres.
habitat The surveyed habitat
year Year of the event
month Month of the event
day Day of the event
eventRemarks Comments or notes about the Event
samplingProtocol The sampling protocol used to capture the species
sampleSizeValue The numeric amount of time spent in each sampling
sampleSizeUnit The unit of the sample size value
samplingEffort The amount of time of each sampling
fieldNumber An identifier given to the event in the field. Often serves as a link between field notes and the Event.
eventDate Date or date range the record was collected
Table of Species Occurrence Table with species abundance data (beginning of new table)
id Unique identification code for species abundance data
type Type of the record, as defined by the Public Core standard
licence Reference to the licence under which the record is published
institutionID The identity of the institution publishing the data
collectionID The identity of the collection publishing the data
institutionCode The code of the institution publishing the data
collectionCode The code of the collection where the specimens are conserved
datasetName Name of the dataset
basisOfRecord The nature of the data record
dynamicProperties The name of the scientific project funding the sampling
occurrenceID Identifier of the record, coded as a global unique identifier
recordedBy Name of the person who performed the sampling of the specimens
individualCount Total number of individuals captured
sex The sex and quantity of the individuals captured
lifeStage The life stage of the organisms captured
establishmentMeans The process of establishment of the species in the location, using a controlled vocabulary: 'naturalised', 'introduced', 'endemic', "unknown"
eventID Identifier of the events, unique for the dataset
scientificName Complete scientific name including author and year
kingdom Kingdom name
phylum Phylum name
class Class name
order Order name
family Family name
genus Genus name
specificEpithet Specific epithet
taxonRank Lowest taxonomic rank of the record
scientificNameAuthorship Name of the author of the lowest taxon rank included in the record

Additional information

Results

We collected a total of 12435 specimens belonging to 45 species of spiders. A total of 13 species are endemic to the Azores Archipelago (9690 specimens), 10 are native non-endemic (2047 specimens) and 22 are introduced (698 specimens) (Table 2, Table 3).

Table 2.

Diversity and abundance for the collected species, according to biogeographic origin and sampling area.

Endemic Native Introduced
Trail / Sampling Area Species richness Abundance Species richness Abundance Species richness Abundance
Lagoinha 0 5 479 10 62 5 7
Lagoinha 50 7 364 14 91 7 15
Lagoinha 250 5 534 12 64 7 11
Lagoinha Control 50 9 419 15 174 3 5
Lagoinha Control 250 5 417 14 187 10 27
Mistérios Negros 0 6 466 17 94 14 33
Mistérios Negros 50 8 421 15 55 7 14
Mistérios Negros 250 8 418 18 119 18 184
Mistérios Negros Max 9 628 20 64 15 57
Mistérios Negros Control 50 6 993 13 187 10 27
Mistérios Negros Control 250 9 394 17 128 7 12
Santa Bárbara 0 8 325 13 17 2 12
Santa Bárbara 50 7 230 13 38 5 22
Santa Bárbara 250 6 417 11 43 3 7
Santa Bárbara Max 8 410 15 40 4 6
Santa Bárbara Control 50 7 463 16 26 6 10
Santa Bárbara Control 250 10 405 17 75 8 17
Guilherme Moniz 0 8 903 26 220 20 57
Malhadas 0 6 148 18 41 13 20
Malhadas 50 7 245 22 63 19 79
Malhadas 250 5 232 14 43 10 30
Malhadas Max 7 378 22 217 35

46

Table 3.

Spider species abundance in each study area and their biogeographic origin. Abbreviations: Biogeographic origin (Biog. origin); Endemic (END); Introduced (INT); Native (NAT).

Family Scientific name Biog. origin Lagoinha Mistérios Negros Santa Bárbara Guilherme Moniz Malhadas
Araneidae Gibbaranea occidentalis Wunderlich, 1989 END 813 1754 365 563 140
Araneidae Mangora acalypha (Walckenaer, 1802) INT 0 138 0 1 18
Araneidae Neoscona crucifera (Lucas, 1838) INT 0 0 0 0 3
Clubionidae Porrhoclubiona decora (Blackwall, 1859) NAT 2 1 0 4 9
Dictynidae Lathys dentichelis (Simon, 1883) NAT 337 507 151 168 198
Dictynidae Nigma puella (Simon, 1870) INT 0 0 0 0 1
Dysderidae Dysdera crocata C. L. Koch, 1838 INT 0 3 0 1 0

Cheiracanthiidae

Cheiracanthium erraticum (Walckenaer, 1802) INT 51 7 20 0 27
Linyphiidae Acorigone acoreensis (Wunderlich, 1992) END 5 4 11 1 0
Linyphiidae Agyneta decora (O.P.-Cambridge, 1871) INT 0 0 3 0 2
Linyphiidae Canariphantes acoreensis (Wunderlich, 1992) END 12 17 91 0 0
Linyphiidae Erigone atra Blackwall, 1833 INT 1 0 0 0 1
Linyphiidae Erigone autumnalis Emerton, 1882 INT 0 1 0 1 1
Linyphiidae Erigone dentipalpis (Wider, 1834) INT 0 0 0 0 1
Linyphiidae Meioneta fuscipalpa (C.L. Koch, 1836) INT 0 0 0 1 0
Linyphiidae Mermessus bryantae (Ivie & Barrows, 1935) INT 0 1 0 0 0
Linyphiidae Mermessus fradeorum (Berland, 1932) INT 0 0 0 2 0
Linyphiidae Microlinyphia johnsoni (Blackwall, 1859) NAT 16 19 12 16 0
Linyphiidae Minicia floresensis Wunderlich, 1992 END 1 0 3 0 7
Linyphiidae Neriene clathrata (Sundevall, 1830) INT 0 0 0 0 2
Linyphiidae Oedothorax fuscus (Blackwall, 1834) INT 0 0 0 1 1
Linyphiidae Palliduphantes schmitzi (Kulczynski, 1899) NAT 2 0 3 0 0
Linyphiidae Porrhomma borgesi Wunderlich, 2008 END 0 1 1 0 0
Linyphiidae Prinerigone vagans (Audouin, 1826) INT 0 0 0 1 4
Linyphiidae Savigniorrhipis acoreensis Wunderlich, 1992 END 430 537 384 60 184
Linyphiidae Tenuiphantes miguelensis (Wunderlich, 1992) NAT 97 22 20 0 46
Linyphiidae Tenuiphantes tenuis (Blackwall, 1852) INT 3 2 2 1 14
Linyphiidae Walckenaeria grandis (Wunderlich, 1992) END 1 0 11 0 0
Lycosidae Pardosa acorensis Simon, 1883 END 3 4 45 0 72
Mimetidae Ero furcata (Villers, 1789) INT 4 23 0 2 10
Pisauridae Pisaura acoreensis Wunderlich, 1992 END 3 13 57 8 21
Salticidae Macaroeris cata (Blackwall, 1867) NAT 97 55 16 28 63
Salticidae Macaroeris diligens (Blackwall, 1867) NAT 0 0 1 0 0
Salticidae Neon acoreensis Wunderlich, 2008 END 0 2 0 1 0
Tetragnathidae Metellina merianae (Scopoli, 1763) INT 5 146 15 35 78
Tetragnathidae Sancus acoreensis (Wunderlich, 1992) END 831 621 974 165 505
Theridiidae Cryptachaea blattea (Urquhart, 1886) INT 0 0 1 1 1
Theridiidae Lasaeola oceanica Simon, 1883 END 53 105 4 2 6
Theridiidae Rhomphaea nasica (Simon, 1873) INT 0 0 0 1 0
Theridiidae Rugathodes acoreensis Wunderlich, 1992 END 61 263 304 103 68
Theridiidae Steatoda nobilis (Thorell, 1875) INT 1 6 1 9 11
Theridiidae Theridion musivivum Schmidt, 1956 NAT 0 0 0 0 2
Thomisidae Xysticus cor Canestrini, 1873 NAT 27 42 36 4 46
Thomisidae Xysticus nubilus Simon, 1875 INT 0 0 32 0 0

The five most abundant species were Gibbaranea occidentalis Wunderlich, 1989 (3635 specimens) (endemic), Sancus acoreensis (Wunderlich, 1992) (3096 specimens) (endemic), Savigniorrhipis acoreensis Wunderlich, 1992 (1595 specimens) (endemic), Lathys dentichelis (Simon, 1883) (1361 specimens) (native non-endemic) and Rugathodes acoreensis Wunderlich, 1992 (799 specimens) (endemic). These five species accounted for 84% of all individuals of the total. The most abundant introduced species was Metellina merianae Scopoli, 1763 with 279 specimens.

This database will be used in future studies where the variation of the spider communites amongst the various sites will be tested against variables that are known to be relevant for understanding the impact of touristic activities, such as the distance to the trail head and the distance from the sampling area to the nearest trail point. We will use GLMMs, where the trail identity will be used as random effect and the edge effect will be added as an independent variable in order to avoid spurious results. This will respond to the questions of whether there is a detectable effect of recreational activities on the spiders community structure and what is contributing to this ecological shift.

Contrary to Canary Islands and Madeira, the Azorean Archipelago has not yet experienced continuous high levels of visitation. This sampling was made at the early times of a noticeably higher touristic pressure in the Azores and will allow for future monitoring events to have a comparable baseline and better isolate the touristic factors from others, thus improving the management outlook on tourism's ecological effects on spider communities.

Acknowledgements

This research was supported by a Ph.D. scholarship from the Azores Governmentto to Rui Carvalho (DRCT M3.1.a/F/135/2015). Data was obtained mostly during the Rui Carvalho DRCT scholarship, but some samples are from a previous project (ERA-Net NetBiome research framework, financed through Portuguese FCT-NETBIOME ISLANDBIODIV grant 0003/2011). Open access was funded by FEDER in 85% and by Azorean Public funds by 15% through Operational Programme Azores 2020, under the project AZORESBIOPORTAL –PORBIOTA (ACORES-01-0145-FEDER-000072)

Author contributions

RC, PC and PAVB conceived the study design and the sampling programme. RC, PAVB, CR, MTF, LLL, MB, JMO, ARP and FP performed spider sampling. PAVB and RC performed spider identification. RC analysed the data and led the writing. All authors contributed to the final version of the manuscript.

References

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