SLAM Project - Long Term Ecological Study of the Impacts of Climate Change in the Natural Forest of Azores: II - A survey of exotic arthropods in disturbed forest habitats

Abstract Background The data we present consist of an inventory of exotic arthropods, potentially invasive, collected in exotic and mixed forests and disturbed native forest patches of the Azores Archipelago. The study was carried out between 2019 and 2020 in four islands: Corvo, Flores, Terceira and Santa Maria, where a total of 45 passive flight interception SLAM traps were deployed, during three to six consecutive months. This manuscript is the second contribution of the “SLAM Project - Long Term Ecological Study of the Impacts of Climate Change in the Natural Forest of Azores”. New information We provide an inventory of terrestrial arthropods belonging to Arachnida, Diplopoda, Chilopoda and Insecta classes from four Azorean islands. We identified a total of 21,175 specimens, belonging to 20 orders, 93 families and 249 species of arthropods. A total of 125 species are considered introduced, 89 native non-endemic and 35 endemic. We registered 34 new records (nine for Corvo, three for Flores, six for Terceira and 16 for Santa Maria), of which five are new for Azores, being all exotic possibly recently introduced: Dieckmanniellusnitidulus (Gyllenhal, 1838), Gronopsfasciatus Küster, 1851, Hadroplontustrimaculatus (Fabricius, 1775), Hypurusbertrandi (Perris, 1852) (all Coleoptera, Curculionidae) and Cardiocondylamauritanica Forel, 1890 (Hymenoptera, Formicidae). This publication highlights the importance of planted forests and disturbed native forest patches as reservoirs of potentially invasive arthropods and refuges for some rare relict endemic arthropod species.


Introduction
Arthropod communities, particularly insects, are being affected by unprecedented and rapid population declines (Hallmann et al. 2017, Sánchez-Bayo and Wyckhuys 2019, Harvey et al. 2020Cowie et al. 2022. The most important causes for this biodiversity loss are habitat loss, degradation and fragmentation, climate change and the introduction and spread of invasive species (Russell et al. 2017, Borges et al. 2019a. In this context, the biodiversity of oceanic islands has been especially and dramatically affected by these drivers as consequence of human colonisation, global trade and tourism (Triantis et al. 2010, Borges et al. 2019b, Cowie et al. 2022, Stüben 2022).
In the case of Azores islands, since Portuguese settlement in the 15 century, the original landscape was strongly altered by replacing pristine and native forest areas with exotic tree plantations, crops, pastures and urban areas (Triantis et al. 2010, Borges et al. 2019b, Norder et al. 2020. Currently, the remaining native forest covers only about 5% of the total surface of the Archipelago, being restricted to the higher elevation and inaccessible areas of the islands (Gaspar et al. 2008, Triantis et al. 2010, Stüben and Borges 2019, Norder et al. 2020. Native forest destruction (Triantis et al. 2010) and the consequent lack of connectivity between forest patches (Aparício et al. 2018), climate change (Ferreira et al. 2016) and invasive species are the main factors that contribute to arthropod decline in Azores (Stüben 2003, Stüben 2004, Borges et al. 2019b. Previous studies demonstrated that endemic species of Azorean arthropods are restricted mainly to native vegetation dominated th habitats, while introduced species usually occupy human-altered habitats , Florencio et al. 2015, Florencio et al. 2016. Additionally, the proportion of introduced arthropod species in Azores is higher than native (around 60%) and, due to the higher adaptability to environmental conditions of many introduced species, they represent one of the main threats to indigenous biota in the native forest areas (Borges et al. 2019b). Moreover, Tsafack et al. (2021) showed the importance of isolated and small native forest patches, as well exotic and mixed forests close to native areas, which can function as refuges for native and rare endemic species, playing a relevant role for conservation of native biota outside Azorean protected areas.
This publication is the second data paper of the project "SLAM Project -Long Term Ecological Study of the Impacts of Climate Change in the Natural Forest of Azores" (see first in Costa and Borges 2021) that aims to monitor the distribution and abundance of arthropods in native forests from Azores using SLAM traps (Sea, Land and Air Malaise traps). Additional publications, using data coming from this project, tested specific ecological questions, namely patterns of seasonal variation on species abundance , patterns of temporal beta diversity in native and exotic species , the potential decline of endemic insects , patterns of arthropod diversity in Azorean urban gardens (Arteaga et al. 2020), patterns of species richness and beta diversity in a small elevational gradient (de Vries et al. 2021) and the investigation of the role of small lowland patches of exotic forests as refuges for rare endemic Azorean arthropods (Tsafack et al. 2021).
In this second data paper, we aim to: i) survey arthropods in exotic and mixed forests and small disturbed remnants of native forests; ii) investigate the occurrence and current distribution of exotic (potentially invasive) arthropods in those habitats; and also iii) investigate the occurrence of rare endemic arthropods in those habitats.
Design description: Passive flight interception SLAM traps (Sea, Land and Air Malaise traps) (Fig. 2) were used to sample 45 sites in the four study Islands (Corvo (n = 1), Flores (n = 5), Santa Maria (n =16) and Terceira (n = 23)) with one trap being set up at each plot. Although this protocol was originally developed to sample flying arthropods, by working as an extension of the tree, non-flying species can also crawl into the trap , enhancing the range of groups that can be sampled by this technique. Recent studies have used this sampling technique to study diversity and abundance variations in the communities of arthropod on Azorean native areas , de Vries et al. 2021, Tsafack et al. 2021. The samples were collected every three or six months depending on sites. The collected specimens were sorted to morphospecies and posteriorly identified at species level by an expert taxonomist in laboratory.   The database management and Open Access was funded by the project "MACRISK-Traitbased prediction of extinction risk and invasiveness for Northern Macaronesian arthropods" Fundação para a Ciência e Tecnologia FCT -PTDC/BIA-CBI/0625/2021 (2022-2024). Sampling description: A total of 45 passive flight interception SLAM traps (Sea, Land and Air Malaise traps) were used to sample the plots in the four study Islands, with one trap being set up at each plot. Trap size is of approximately 110 x 110 x 110 cm. The trap functions on the basis of intercepting arthropods that crawl up the mesh and then fall inside the sampling recipient, which is filled with propylene glycol (pure 1,2-propanodiol) . A total of 19 SLAM traps were deployed in exotic forest areas, eight on native forest patches and 18 on mixed forests. The trap samples were collected every three months in Flores and Corvo and six months in Terceira and Santa Maria. In Corvo Island, one trap was available in a mixed forest ( Fig. 3; Table 1). In Flores Island, five traps were available in both exotic forests and native forests ( Fig. 4; Table 1). In Santa Maria Island, a total of 16 traps were available with only three located in disturbed native forest patches ( Fig. 5; Table 1). Finally, in Terceira Island, 23 traps were available with only four in disturbed native forest patches ( Fig. 6; Table 1).

Sampling methods
Quality control: All sampled individuals were first sorted by trained paratoxonomists (see list above). All specimens were allocated to a taxonomic species by Paulo A. V. Borges. Despite the uncertainty of juvenile identification, juveniles are also included in the data presented in this paper, since the low diversity allowed a relatively precise identification of this life-stage in Azores.
Step description: At the laboratory, specimen sorting and arthropod identification followed standard procedures during the last 20 years or arthropod surveys in Azores. First, a combination of morphological and anatomical characters and reproductive structures was used for morphospecies creation. After, morphospecies were sent to experts for proper identification. With this procedure, a reference collection was made for all collected specimens by assigning them a morphospecies code number and respective taxonomic name and depositing them at the Dalberto Teixeira Pombo Insect Collection, University of Map with the location of the sampling sites in Corvo Island, Azores. Codes of sites as in Table  1 (Land-use data extracted from Cruz et al. 2007) (Credit: Enésima Pereira, Azorean Biodiversity Group).
Azores. Colonisation status of the species was obtained from the last updated checklist of Azorean arthropods . Map with the location of the sampling sites in Flores Island, Azores. Codes of sites as in Table  1 (Land-use data extracted from Cruz et al. 2007) (Credit: Enésima Pereira, Azorean Biodiversity Group).

Figure 5.
Map with the location of the sampling sites in Santa Maria Island, Azores. Codes of sites as in  Map with the location of the sampling sites in Terceira Island, Azores. Codes of sites as in  ). The following data table includes 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 that has 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 45 records (eventID). This IPT (Integrated Publishing Toolkit) archives the data and thus serves as the data repository. The data and resource metadata are available for download in the Portuguese GBIF Portal IPT .

Column label Column description
id Unique identification code for sampling event data.
eventID Identifier of the events, unique for the dataset. 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.
eventDate Date or date range the record was collected. year Year of the event. minimumElevationInMetres The lower limit of the range of elevation (altitude, usually above sea level), in metres.

verbatimEventDate
The verbatim original representation of the date and time information for an Event.
In this case, we use the season and year. habitat The habitat of the sample. 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 in metres.
coordinatePrecision A decimal representation of the precision of the coordinates given in the decimalLatitude and decimalLongitude.
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.

Description:
The dataset was published in Global Biodiversity Information Facility platform, GBIF ). The following data table includes all the records for which a taxonomic identification of the species was possible. The dataset submitted to GBIF is structured as an occurrence table that has 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 2095 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 in the Portuguese GBIF Portal IPT .

Column description
id Unique identification code for sampling event 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. institutionCode The code of the institution publishing the data. collectionID The identity of the collection publishing the data. collectionCode The code of the collection where the specimens are conserved. basisOfRecord The nature of the data record. scientificNameAuthorship Name of the author of the lowest taxon rank included in the record.
At island scale, the native ant Lasius grandis was also one of the most abundant arthropods in Corvo (n = 31) and Santa Maria (n = 348). Curiously, in both Islands, one of the two most abundant species represent a new island record, being the exotic spider Porrhoclubiona genevensis (L. Koch, 1866) (n = 15), new for Corvo and the exotic (possibly invasive) beetle Lagria hirta (Linnaeus, 1758) (n =382), new for Santa Maria.

New Azores species records
In this study, we registered a total of 34 new records for one or more islands of Azores  . 7); 1.4 -2.1 mm (Stüben 2022).
Gronops cf. fasciatus Küster, 1851 The genus Gronops (Curculionidae: Cyclominae: Rhytirrhinini) includes about 20 Palaearctic species, mainly from the arid regions of North Africa and is only represented with certainty on the Canary Islands by the species Gronops fasciatus. The determination of the specimen of Gronops cf. fasciatus, a male, recorded at the airfield of Santa Maria (Azores) in December 2019, must be checked again by a specialist of this group. The biology of these terricolous, flightless species is largely unknown, although they are often found near Caryophyllaceae and Amaranthaceae. Carry-over with soil is conceivable. Characteristic features of G. fasciatus compared to G. lunatus (Fabricius, 1775): elytra shorter, hardly narrowing towards the apex (subparallel); pronotum wider, strongly widened in the front third (see Fig. 8); length: 2.2-3.2 mm (Stüben 2022).    (Stüben et al. 2014, Stüben 2022.

Cardiocondyla mauritanica Forel, 1890
This ant species is native to northern Africa, Middle East, Afghanistan and Pakistan, but has been introduced in many other regions, including the United States of America, Mexico, Zimbabwe, several European countries and many islands worldwide (Wetterer 2012, Janicki et al. 2016, Seifert et al. 2017. In Macaronesia, C. mauritanica was perviously known to occur in Madeira and the Canary Islands (Espadaler 2008, Báez andOromí 2010). These ants are small, inconspicuous and can be separated from other Cardiocondyla species using a combination of morphometric characters ( Seifert 2003, Seifert et al. 2017) (see Fig. 11). They form polygynous colonies and mating occurs inside the nests (Seifert et al. 2017). These characteristics and their ability to co-exist with other aggressive invasive ant species, like the Argentine ant Linepithema humile, are important to explain their ecological success and ongoing spread (Wetterer 2012). However, contrary to other exotic ant species, C. mauritanica does not seem to have significant ecological impacts on native biodiversity (Wetterer 2012).

Conservation remarks
This publication highlights the importance of exotic and mixed forest areas, as well as small native disturbed forest patches as potential reservoirs of both exotic potentially invasive species, as well as rare endemic species (see also Tsafack et al. 2021 Within endemics, we wish to comment on the recently-described subspecies Pseudophloeophagus tenax borgesi Stüben, 2022 (Curculionidae: Cossoninae) (Fig. 12). This subspecies, common in many islands of the Azores, was described only in 2022 (Stüben 2022). The nominotypic taxon occurs on Madeira. Accordingly, material of P. tenax from trap findings and in collections from the Azores must be assigned to this new subspecies. Type locality of P. tenax borgesi is on São Jorge (Vigia da Baleia), but perhaps the subspecies occurs on all islands of the Azores. Apart from clear molecular differences in the mitochondrial COI gene (Stüben et al. 2012), this subspecies of the Azores differs from the nominotypic taxon on Madeira in the following characteristics: elytral striae more strongly and deeply punctured and the interstriae much narrower than in the sister taxon from Madeira; aedeagus narrower (see Fig. 12, Borges 2019, Stüben 2022).
Several other rare endemic species were found in this study (see list below), which highlights the importance of expanding surveys in Azores to small isolated forest patches in order to find relict populations of rare endemic species: -Canariphantes acoreensis (Wunderlich, 1992) (Araneae, Linyphiidae). This rare spider is usually found in pristine native forests and is considered Vulnerable (VU) by IUCN (Borges and Cardoso 2021b). In the current study, we sampled a single specimen in a disturbed mixed forest of Eucalyptus spp. and Pittospsorum undulatum at Terceira Island located near a native forest at Pico Rachado.
-Canariphantes relictus Crespo & Bosmans, 2014 (Araneae, Linyphiidae). Another very rare species, classified as Critically Endangered (CR) (Borges and Cardoso 2021a). The species was found originally in high elevation at Santa Maria Island (Crespo et al. 2014), but in our study, two females were found at Piedade (PRIBS_T03_12_2019) at low elevation in a mixed forest of Picconia azorica, Pittosporum undulatum and Pinus sp. The species possibly has a larger distribution than originally recorded. -Olisthopus inclavatus Israelson, 1983 (Coleoptera, Carabidae). This is a very rare groundbeetle classified as Critically Endangered (CR) by IUCN  and currently occurring only in exotic forests (dominated by Cryptomeria japonica, Acacia spp.). In this study, the unique specimen was sampled in Monteiro (SMR_PRIBS_T12).
-Athous azoricus Platia & Gudenzi, 2002 (Coleoptera, Elateridae) (Fig. 13). This is a relatively rare species known from Flores, Graciosa, Terceira and S. Miguel Islands. Considered Endangered by the IUCN (Borges and Lamelas-López 2017a), this species tends to occur at low elevations in disturbed exotic forests. In the current study, we found the species in three places all at mid-elevations (300-500 m) and in three types of forest, one plantation of Cryptomeria japonica (Mistérios Negros; TER-MNEG-T-62 corresponding also to code TER_PRIBS_T05), a mixed forest dominated by Eucalyptus spp. (Escampadouro; TER_PRIBS_T23) and a mixed forest dominated by Pittosporum undulatum (Mata do Estado; TER_PRIBS_T04). At least in Terceira Island, the species seems to be more widespread than previously assumed.
-Brachypera multifida (Israelson, 1984) (= Donus multifudus (Israelson, 1984)) (Coleoptera, Curculionidae) (Fig. 14). This is a particularly rare curculionid beetle classified as Critically Endangered (CR) (Borges and Lamelas-López 2017b). Previously, it was sampled at high elevation at Pico Alto in Santa Maria Island. In the current survey, we sampled this species in three sites, Estação Loran (SMR_PRIBS_T08), Piquinhos (SMR_PRIBS_T10) and Figueiral (SMR_PRIBS_T14) expanding the range of the species to lower elevations and to different types of forest. -Tarphius rufonodulosus Israelson, 1984 (Coleoptera, Zopheridae) (Fig. 15). This is a rare ironclade beetle also Critically Endangered (CR) (Borges and Lamelas-López 2018) that is associated with the canopies of native trees (e.g. Picconia azorica) and under-bark of dead trees, both in native and exotic forests (dominated by Acacia sp. and Cryptomeria japonica). In the current study, one specimen was collected in mixed forests of Erica azorica, Cryptomeria japonica and Pittosporum undulatum at three locations at high elevation (Piquinhos and Fontinhas forest areas).

Patterns of invasion
The main aim of this study was to investigate the importance of disturbed native forest patches and exotic vegetation areas as potential reservoirs of exotic potentially invasive arthropods. As expected, we found a large number of exotic species, some of them new for Azores, as listed above. In addition to the 125 species identified as introduced (Table 2), many more are waiting a proper identification (Suppl. material 1). In previous studies, we identified thirteen widespread exotic arthropods as new records for Azores (Borges et al. 2013) and some previously unknown exotic species in Azorean urban gardens (Arteaga et al. 2020). This clearly indicates that there is an ongoing continuous flux of new introductions in Azores.
Some of the introduced species found in the current study are a matter of concern for nature conservation in the Azores Archipelago and their populations should be monitored. For instance, Lagria hirta (Linnaeus, 1758) (Coleoptera, Tenebrionidae) that was recently recorded as new for Azores and found originally at Terceira Island , is expanding dramatically in Santa Maria. In Santa Maria, we found it everywhere at all elevations and habitats. This seems to be a recent introduction in Azores and the impact of this species is still unknown. The Australian exotic planthopper Siphanta acuta (Walker, 1851) (Hemiptera, Flatidae) was recorded originally for Azores in 2013 (Borges et al. 2013) and is expanding rapidly in several Azorean islands with potential impacts on agriculture. In our study, we found it quite abundant in many sites at Terceira and Santa Maria Islands. The expansion of the Eucalyptus snout beetle Gonipterus platensis (Marelli, 1926) (Coleoptera, Curculionidae) that was found in several sites at Terceira Island is also of concern. This species was originally recorded for Azores by Borges et al. (2013) and is currently known also from São Miguel Island.
In potential expansion in Terceira (and also known from Pico) is the two-spotted leafhopper Sophonia orientalis (Matsumura, 1912) (Hemiptera; Cicadellidae) (Tarantino et al. 2022). This species is native to south-east Asia and is a highly polyphagous pest, considered an invasive species that affects crops as well as endemic plants (Tarantino et al. 2022).
Several exotic ant species have been recorded in the Azores (Espadaler 2010) and, here, we report new findings at both island and archipelago levels that highlight their rapid spread. Jointly with the first record of Cardiocondyla mauritanica for Azores, we found that two exotic Tetramorium species (T. bicarinatum and T. caldarium) are now present in Santa Maria. Both C. mauritanica and T. caldarium do not seem to have significant impacts on native biodiversity (Wetterer 2012, Wetterer andHita Garcia 2015), but T. bicarinatum and, particularly, the Argentine ant L. humile, are serious threats to island native invertebrates and natural ecological processes and have also been reported as agricultural pests (Wetterer 2009, Wetterer et al. 2009). The severe consequences of Argentine ant invasion on local biodiversity have been reported from many areas around the world, including oceanic islands, but their effects remain poorly understood in Macaronesian archipelagos (Holway et al. 2002, Wetterer and Espadaler 2010, Boieiro et al. 2018a, Boieiro et al. 2018b).
Finally, it is important to highlight that, amongst the most abundant introduced species in our study, several are listed in the TOP100 worst invasive species of Azores and Macaronesia , namely the woodlouse spider Dysdera crocata C.L. Koch, 1838, the Argentine ant Linepithema humile (Mayr, 1868) and the millipede Ommatoiulus moreleti (Lucas, 1860).
Our study stresses the need for arthropod biodiversity monitoring in different habitats of oceanic islands as an important strategy for early detection of invasive species that may have severe impacts on the environment, economy and human well-being (see also . It also allows us to assess changes on species abundance and distribution, thus providing valuable information to support decision-making by conservation managers.