New records and detailed distribution and abundance of selected arthropod species collected between 1999 and 2011 in Azorean native forests

Paulo AV Borges; Clara Gaspar; Luís Carlos Fonseca Crespo; François Rigal; Pedro Cardoso; Fernando Pereira; Carla Rego; Isabel R Amorim; Catarina Melo; Carlos Aguiar; Genage André; Enésima P Mendonça; Sérvio Ribeiro; Joaquín Hortal; Ana MC Santos; Luís Barcelos; Henrik Enghoff; Volker Mahnert; Margarida T Pita; Jordi Ribes; Arturo Baz; António B Sousa; Virgílio Vieira; Jörg Wunderlich; Aristeidis Parmakelis; Robert J Whittaker; José Alberto Quartau; Artur RM Serrano; Kostas A Triantis

doi:10.3897/BDJ.4.e10948

. 2016 Dec 22;(4):e10948. doi: 10.3897/BDJ.4.e10948

New records and detailed distribution and abundance of selected arthropod species collected between 1999 and 2011 in Azorean native forests

Paulo AV Borges ^1,^✉, Clara Gaspar ¹, Luís Carlos Fonseca Crespo ^1,², François Rigal ^3,¹, Pedro Cardoso ^4,¹, Fernando Pereira ¹, Carla Rego ¹, Isabel R Amorim ¹, Catarina Melo ¹, Carlos Aguiar ⁵, Genage André ⁵, Enésima P Mendonça ¹, Sérvio Ribeiro ^6,¹, Joaquín Hortal ^7,¹, Ana MC Santos ^7,¹, Luís Barcelos ¹, Henrik Enghoff ⁸, Volker Mahnert ⁹, Margarida T Pita ¹⁰, Jordi Ribes ¹¹, Arturo Baz ¹², António B Sousa ¹³, Virgílio Vieira ^1,¹⁴, Jörg Wunderlich ^15,15, Aristeidis Parmakelis ^16,¹, Robert J Whittaker ¹⁷, José Alberto Quartau ⁵, Artur RM Serrano ⁵, Kostas A Triantis ^16,¹

¹cE3c – Centre for Ecology, Evolution and Environmental Changes / Azorean Biodiversity Group and Universidade dos Açores - Departamento de Ciências e Engenharia do Ambiente, Rua Capitão João d’Ávila, São Pedro, 9700-042 Angra do Heroísmo, Terceira, Azores, Portugal

²Departament de Biologia Animal and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Avinguda Diagonal 643, 08071, Barcelona, Spain

³Environment and Microbiology Team, IPREM UMRCNRS-UPPA 5254, IBEAS BP1155, Université de Pau et des Pays de l’Adour, 64013 Pau Cedex, France

⁴Finnish Museum of Natural History, University of Helsinki, Pohjoinen Rautatiekatu 13, P.O.Box 17, 00014, Helsinki, Finland

⁵cE3c, Centre for Ecology, Evolution and Environmental Changes & Faculty of Sciences, University of Lisbon, 1749-016, Lisbon, Portugal

⁶Laboratório de Ecologia Evolutiva de Herbívoros de Dossel, DEBIO, Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, 35400-000, Ouro Preto, MG, Brazil

⁷Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales (CSIC), C⁄Joseé Gutiérrez Abascal 2, 28006, Madrid, Spain

⁸Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen OE, Denmark

⁹Museum d´Histoire Naturelle, Case Postale 6434, 1211, Geneva, Swaziland

¹⁰Centro de Estudos da Macaronésia (CEM), Universidade da Madeira, Campus Universitário da Penteada - Bloco C - Piso 1, 9000-399 Funchal, Madeira, Portugal

¹¹Valencia 123-125, ent., 3a, E-08011, Barcelona, Spain

¹²Dep. de Ciencias de la Vida. Universidad de Alcalá, 28871 Alcalá de Henares, Madrid, Spain

¹³SPEN – Sociedade Portuguesa de Entomologia, Apartado 8221, P-1803-001, Lisboa, Portugal

¹⁴Departamento de Biologia, Universidade dos Açores, Apartado 1422, 9501-301, Ponta Delgada, S. Miguel, Azores, Portugal

¹⁵Hindenburgstr. 94, D-75334, Straubenhardt, Germany

¹⁶Department of Ecology and Taxonomy, Faculty of Biology, National and Kapodistrian University of Athens, Athens, GR-15784, Greece

¹⁷Biodiversity Research Group, Oxford University, Centre for the Environment, South Parks Road, Oxford, OX1 3QY, United Kingdom

^✉

Corresponding authors: Paulo Borges

Academic editor: Pavel Stoev

^✉

Corresponding author.

PMCID: PMC5267528 PMID: 28174509

Abstract Abstract

Background

In this contribution we present detailed distribution and abundance data for arthropod species identified during the BALA – Biodiversity of Arthropods from the Laurisilva of the Azores (1999-2004) and BALA2 projects (2010-2011) from 18 native forest fragments in seven of the nine Azorean islands (all excluding Graciosa and Corvo islands, which have no native forest left).

New information

Of the total 286 species identified, 81% were captured between 1999 and 2000, a period during which only 39% of all the samples were collected. On average, arthropod richness for each island increased by 10% during the time frame of these projects. The classes Arachnida, Chilopoda and Diplopoda represent the most remarkable cases of new island records, with more than 30% of the records being novelties. This study stresses the need to expand the approaches applied in these projects to other habitats in the Azores, and more importantly to other less surveyed taxonomic groups (e.g. Diptera and Hymenoptera). These steps are fundamental for getting a more accurate assessment of biodiversity in the archipelago.

Keywords: Azores; terrestrial arthropods; BALA project; laurissilva forest; Linnean, Wallacean and Prestonian shortfalls.

Introduction

In 1999 a group of researchers from the University of the Azores and the University of Lisbon started a long-term (1999-2004) standardized sampling program to inventory the arthropod biodiversity in native forest remnants of the Azores - the BALA I project – Biodiversity of Arthropods from the Laurisilva of the Azores (Borges et al. 2000, Borges et al. 2005a, Borges et al. 2011, Ribeiro et al. 2005, Gaspar et al. 2008). More recently, this project was extended by researchers from the Universities of the Azores, Athens and Oxford, by surveying part of the same native forest plots almost 10 years later - BALA II project (2010-2011).

Eight years of standardized survey of the native forest in seven of the nine Azorean islands resulted in a major improvement on the knowledge of the Azorean arthropod fauna, in particular concerning Araneae, Opiliones, Pseudoscorpionida, Diplopoda, Chilopoda and Insecta (excluding Collembola, Diptera and Hymenoptera). As a consequence, several new endemic taxa were described for the archipelago (e.g. Blas and Borges 1999, Ribes and Borges 2001, Platia and Borges 2002, Quartau and Borges 2003, Borges et al. 2004, Borges and Wunderlich 2008, Crespo et al. 2013, Crespo et al. 2014) or are in the process of being described (Borges et al. 2016 in press). In fact, after examining the shape and characteristics of discovery curves, Lobo and Borges (2010) clearly show that it is very likely that many new species of arthropods remain to be discovered in the Azores particularly for less studied groups in this archipelago such as Diptera and Hymenoptera. Besides purely faunistic results, the BALA data was also used to evaluate abundance, spatial variance and occupancy of arthropods (Gaston et al. 2006, Rigal et al. 2013), the effects of disturbance and biotic integrity of the native forests on arthropod assemblages (Cardoso et al. 2007, Cardoso et al. 2013, Gaspar et al. 2011, Florencio et al. 2013, Florencio et al. 2015), the extinction debt of Azorean forest specialist species (Triantis et al. 2010) and the performance of species richness estimators (Hortal et al. 2006). Moreover, such data allowed the ranking of conservation priorities for the fauna and flora of the Azores (e.g. Borges et al. 2005a, Martín et al. 2010) and allowed the estimation of extinction debt in Azores (Terzopoulou et al. 2015, Triantis et al. 2010).

During this period, two complete checklists of Azorean arthropod fauna were produced (Borges et al. 2005b, Borges et al. 2010), which included the distribution of each species per island. In this paper we compile and synthesize the faunistic results of both BALA projects, highlighting novel distribution records and presenting not only detailed distribution but also abundance data for each species, adding taxonomical and biogeographical information whenever possible. Finally, we provide a general and updated overview on the diversity of the Azorean arthropods.

Materials and methods

Area of study: The Azores

The remote Azores archipelago extends for 615 km in the North Atlantic Ocean (37-40 °N, 25-31 °W), 1584 km to the east (southern Europe) and 2150 km to the west (northern America) of the nearest mainland. It comprises nine main islands and some small islets, all of volcanic origin, and is located at the triple junction of the Eurasian, African and American tectonic plates. The nine islands are divided into three groups: the western group (Corvo and Flores isls.), the central group (Faial, Pico, Graciosa, São Jorge and Terceira isls.), and the eastern group (São Miguel and Santa Maria isls) (Fig. 1). The climate is temperate and oceanic, strongly influenced by the ocean and island topography, which together produce high relative atmospheric humidity, above 95% on average on native forests.

Figure 1. — Location of the Azores and of native forest fragments in the archipelago. Codes for forest fragments as in Table 1.

Sampling protocol

Eighteen native forest fragments distributed across seven of the nine islands were sampled (Table 1; see also Gaspar et al. 2008). Graciosa and Corvo islands were excluded as they no longer present native forest. Human settlement in the Azores lead to considerable native forest destruction which has left the entire archipelago with little over 2% of the original forest cover. During the summer (June to September) 150 m long and 5 m wide transects were set up in 100 sites from 1999 to 2004 (BALA I: 18 native forest fragments) and some were sampled twice in that period totalling 123 samples; about 29 of those sites were resampled from 2010 to 2011 using the same protocol (BALA II project; 15 native forest fragments). Along each transect, arthropods from the soil (mainly epigean) and herbaceous vegetation were surveyed with pitfall traps, while arthropods from woody plants were sampled using a beating tray. Pitfall traps consisted of plastic cups with 4.2 cm diameter and 7.8 cm height. Thirty pitfall traps were set up per transect. Half of the traps were filled with a non-attractive ethylene glycol preservative solution (antifreeze solution), and the remaining with a general attractive solution, a modified version of Turquin (Turquin 1973) prepared mainly with dark beer and preservative agents. A few drops of dishwashing liquid were added to both solutions to reduce surface tension. Traps were sunk in the soil (cup rim at surface level) every 5 m along the transects, those filled with Turquin alternating with traps containing antifreeze solution. Traps were protected from rain using a plastic plate, placed about 5 cm above surface level and fixed to the ground by two pieces of wire. Accidental collection of small vertebrates and damage by rodents was prevented using a piece of plastic mesh placed on top of the trap and fixed to the ground by pieces of wire. The traps remained active in the field for two weeks.

Table 1.

Main characteristics of the Azorean islands (bold) and native forest fragments sampled from 1999 to 2011, including area (hectares), highest point (altitude in metres), distance to the nearest island/fragment (isolation in kilometres) and the oldest geological age of emerged substrate (million years BP) (adapted from Gaspar et al. 2008).

Island	Fragment	Code	Area (ha)	Altitude (m)	Isolation (km)	Age (my)
Flores		FLO	14102	911	236.43	2.16
	Morro Alto e Pico da Sé	MO	1331	911	6.02	2.16
	Caldeiras Funda e Rasa	FR	240	773	6.02	2.16
Faial		FAI	17306	1043	34.26	0.73
	Caldeira do Faial	CA	190	934	4.67	0.73
	Cabeço do Fogo	CG	36	597	4.67	0.60
Pico		PIC	44498	2350	32.42	0.30
	Mistério da Prainha	MP	689	881	2.92	0.26
	Caveiro	CA	184	1077	4.61	0.27
	Lagoa do Caiado	LC	79	945	2.92	0.28
São Jorge		SJG	24365	1053	32.42	0.55
	Topo	TO	220	946	15.13	0.55
	Pico Pinheiro	PP	73	717	15.13	0.55
Terceira		TER	40030	1021	71.67	3.52
	S. Bárbara e M. Negros	SB	1347	1021	7.20	1.24
	Biscoito da Ferraria	BF	557	809	3.03	0.10
	Guilherme Moniz	GM	223	487	2.70	0.41
	Terra Brava	TB	180	726	2.70	0.10
	Pico do Galhardo	PG	38	655	2.79	0.10
São Miguel		SMG	74456	1105	97.53	4.01
	Pico da Vara	PV	306	1105	3.42	3.20
	Graminhais	GR	15	930	4.02	3.20
	Atalhada	AT	10	500	3.42	4.01

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Canopy sampling was conducted during the trapping period, when the vegetation was dry. A 5 m wide square was established every 15 m (total of 10 squares per transect). Two woody plant specimens of the most abundant species (up to three species when available) were sampled in each square. For each selected plant, a branch was chosen at random and a beating tray placed beneath. The tray consisted of a 1 m wide and 60 cm deep cloth inverted pyramid, with a plastic bag at the vertex. Five beatings were made using a stick for each plant individual sampled.

The arthropod taxa considered in this study were selected based on the availability of expert taxonomists and ability to readily separate them by morphological criteria. All Araneae, Opiliones, Pseudoscorpionida, Diplopoda, Chilopoda and Insecta (excluding Collembola, Diptera and Hymenoptera) were assigned to morphospecies through comparison with a reference collection. Various taxonomists (PAVB, ARMS, LC, PC, HE, FI, VM, MTP, JR, AB, ABS, RzS, VV, JW, JAQ, and see also Acknowledgments) checked the assignment to morphospecies, performed species identifications and supplied additional ecological information. The taxonomic nomenclature follows the most recent list of Azorean arthropods (Borges et al. 2010).

All specimens are deposited in the Entomological Collection Dalberto Teixeira Pombo at the University of the Azores (Portugal), under the curation of Paulo A. V. Borges (pborges@uac.pt).

In this contribution we list the 286 species for which we obtained an identification. The new records for each island are marked with *. For this list two families of Coleoptera were not considered since they will be presented elsewhere, Staphylinidae (Borges et al. in prep.) and Zopheridae (Borges et al. 2016). For detailed maps on the distribution of these species in Azores consult the Azores Bioportal.

All specimens were assigned a SITE CODE composed of several letters and numbers that read as follows (see Suppl. material 1 for complete data). Detailed metadata is given in Suppl. material 2):

i) the first three letters refer to island name (FLO – Flores; FAI – Faial; PIC – Pico; SJG – São Jorge; GRA – Graciosa; TER – Terceira; SMG – São Miguel; SMR – Santa Maria);

ii) the following two letters refer to fragment name (Flores: FR - Caldeiras Funda e Rasa, MA - Morro Alto e Pico da Sé; Faial: CF – Caldeira do Faial, CG – Cabeço do Fogo; Pico: CA – Caveiro, LC – Lagoa do Caiado, MP – Mistério da Prainha; São Jorge: PP – Pico Pinheiro, TO – Topo; Terceira: BF – Biscoito da Ferraria, GM – Caldeira do Guilherme Moniz, PG – Pico do Galhardo, SB –Serra de Santa Bárbara, TB – Terra Brava; São Miguel: AT – Atalhada, GR – Graminhais, PV – Pico da Vara; Santa Maria: PA – Pico Alto);

iii) the following three characters refer to the sampling transect; and

iv) the next letter refers to the sampling technique: P - pitfall, B - canopy beating; for pitfall samples (P) TU – Turquin and ET – ethylene glycol; for canopy samples (B) the next two letters refer to the plant sampled: CA = Calluna vulgaris, CL = Clethra arborea, ER = Erica azorica, FR = Frangula azorica, IL = Ilex perado azorica, JU = Juniperus brevifolia, LA = Laurus azorica, MC = Morella faya, MS = Myrsine africana, PI = Picconia azorica, PT = Pittosporum undulatum, VA = Vaccinium cylindraceum.

For the geographical location of transects within reserves (UTM coordinates) see Suppl. material 3.

Accumulation curves were obtained using the software “Species Diversity and Richness” V.4.

Checklists

Checklist of the Studied Azorean Arthropods

Animalia

Arthropoda

Arachnida

Pseudoscorpiones

Chthoniidae

Chthonius ischnocheles

(Hermann, 1804)

http://azoresbioportal.uac.pt/azores-species/chthonius-ischnocheles-10257/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO*; FAI; PIC; GRA; SJG*; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Western Palearctic)

Chthonius tetrachelatus

(Preyssler, 1790)

http://azoresbioportal.uac.pt/azores-species/chthonius-tetrachelatus-10380/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO*; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Western Palearctic)

Neobisiidae

Neobisium maroccanum

Beier, 1930

http://azoresbioportal.uac.pt/azores-species/neobisium-maroccanum-10482/

Ecological interactions

Native status

Introduced

Distribution

FLO; FAI; PIC; GRA; SJG*; TER*

Notes

Biogeographical Realm: Palearctic

Opiliones

Phalangiidae

Homalenotus coriaceus

(Simon, 1879)

http://azoresbioportal.uac.pt/azores-species/homalenotus-coriaceus-8096/

Ecological interactions

Native status

Native

Distribution

FLO*; FAI*; PIC*; TER*; SMG; SMR*

Notes

Biogeographical Realm: Palearctic

Leiobunum blackwalli

Meade, 1861

http://azoresbioportal.uac.pt/azores-species/leiobunum-blackwalli-7831/

Ecological interactions

Native status

Native

Distribution

FLO*; FAI*; PIC*; GRA; SJG*; TER*; SMG*

Notes

Biogeographical Realm: Western Palearctic

Araneae

Araneidae

Gibbaranea occidentalis

Wunderlich, 1989

http://azoresbioportal.uac.pt/azores-species/gibbaranea-occidentalis-6895/

Ecological interactions

Native status

Azores endemic

Distribution

FLO; FAI; PIC*; GRA; SJG*; TER*; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Mangora acalypha

(Walckenaer, 1802)

http://azoresbioportal.uac.pt/azores-species/mangora-acalypha-7972/

Ecological interactions

Native status

Introduced

Distribution

FLO; FAI; PIC; GRA; SJG*; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Western Palearctic)

Biogeographical Realm: Western Palearctic

Also present: MAD; CAN (Biogeographical Realm: Western Palearctic (Macaronesia))

Dysderidae

Dysdera crocata

C. L. Koch, 1838

http://azoresbioportal.uac.pt/azores-species/dysdera-crocata-7212/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO; FAI; PIC; GRA; SJG*; TER; SMG; SMR

Notes

Also present: MAD (Biogeographical Realm: Cosmopolitan)

Tetragnathidae

Metellina merianae

(Scopoli, 1763)

http://azoresbioportal.uac.pt/azores-species/metellina-merianae-7965/

Ecological interactions

Native status

Introduced

Distribution

FLO*; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD (Biogeographical Realm: Palearctic)

Sancus acoreensis

(Wunderlich, 1992)

http://azoresbioportal.uac.pt/azores-species/sancus-acoreensis-7971/

Ecological interactions

Native status

Azores endemic

Distribution

FLO; FAI; PIC; SJG*; TER; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Also present: MAD; CAN; CVP (Biogeographical Realm: Western Palearctic (Macaronesia))

Thomisidae

Xysticus cor

Canestrini, 1873

http://azoresbioportal.uac.pt/azores-species/xysticus-cor-7922/

Ecological interactions

Native status

Native

Distribution

COR; FLO; FAI*; PIC; GRA; SJG*; TER; SMG; SMR*

Notes

Biogeographical Realm: Palearctic

Xysticus nubilus

Simon, 1875

http://azoresbioportal.uac.pt/azores-species/xysticus-nubilus-7737/

Ecological interactions

Native status

Introduced

Distribution

FLO*; FAI; PIC; GRA; SJG*; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Palearctic)

Zodariidae

Zodarion atlanticum

Pekár & Cardoso, 2006

http://azoresbioportal.uac.pt/azores-species/zodarion-atlanticum-7786/

Ecological interactions

Native status

Introduced

Distribution

FAI; PIC; GRA; TER*; SMG

Notes

Biogeographical Realm: Palearctic

Diplopoda

Polydesmida

Paradoxosomatidae

Oxidus gracilis

(C. L. Koch, 1847)

http://azoresbioportal.uac.pt/azores-species/oxidus-gracilis-8134/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO*; FAI*; PIC; GRA; TER*; SMG; SMR*

Notes

Also present: MAD; CAN (Biogeographical Realm: Afro-tropical; Australian; Eastern Palearctic; Nearctic; Neotropical; Oriental)

Polydesmidae

Brachydesmus superus

Latzel, 1884

http://azoresbioportal.uac.pt/azores-species/brachydesmus-superus-8136/

Ecological interactions

Native status

Introduced

Distribution

FLO*; FAI; PIC; SJG; TER*; SMG; SMR

Notes

Also present: MAD; CAN; CVP (Biogeographical Realm: Australian; Eastern Palearctic; Nearctic; North Africa)

Polydesmus coriaceus

Porat, 1871

http://azoresbioportal.uac.pt/azores-species/polydesmus-coriaceus-8146/

Ecological interactions

Native status

Introduced

Native status

Introduced

Distribution

FLO*; FAI; TER*; SMG; SMR*

Notes

Also present: MAD; CAN (Biogeographical Realm: Nearctic)

Also present: MAD; CAN (Biogeographical Realm: Afro-tropical; Australian)

Chordeumatida

Haplobainosomatidae

Haplobainosoma lusitanum

Verhoeff, 1900

http://azoresbioportal.uac.pt/azores-species/haplobainosoma-lusitanum-8162/

Ecological interactions

Native status

Introduced

Distribution

FAI*; PIC; TER*; SMG*; SMR*

Notes

Biogeographical Realm: Palearctic

Also present: MAD (Biogeographical Realm: Western Palearctic)

Linotaeniidae

Strigamia crassipes

(C. L. Koch, 1835)

http://azoresbioportal.uac.pt/azores-species/strigamia-crassipes-8177/

Ecological interactions

Native status

Native

Distribution

FLO*; TER*; SMG*

Notes

Biogeographical Realm: Western Palearctic

Insecta

Microcoryphia

Machilidae

Dilta saxicola

(Womersley, 1930)

http://azoresbioportal.uac.pt/azores-species/dilta-saxicola-8352/

Ecological interactions

Distribution

PIC; TER; SMG

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Gryllidae

Gryllus bimaculatus

De Geer, 1773

http://azoresbioportal.uac.pt/azores-species/gryllus-bimaculatus-8305/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN; CVP (Biogeographical Realm: Afro-tropical; Eastern Palearctic; Near East; North Africa; Oriental)

Dermaptera

Anisolabididae

Euborellia annulipes

(Lucas, 1847)

http://azoresbioportal.uac.pt/azores-species/euborellia-annulipes-8315/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN; CVP (Biogeographical Realm: Cosmopolitan)

Forficulidae

Forficula auricularia

Linnaeus, 1758

http://azoresbioportal.uac.pt/azores-species/forficula-auricularia-8316/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Holarctic)

Psocoptera

Caeciliusidae

Valenzuela burmeisteri

(Brauer, 1876)

http://azoresbioportal.uac.pt/azores-species/valenzuela-burmeisteri-7098/

Ecological interactions

Native status

Native

Distribution

FLO*; FAI*; SJG*; TER*; SMG*; SMR*

Notes

Also present: MAD; CAN (Biogeographical Realm: Holarctic)

Valenzuela flavidus

(Stephens, 1836)

http://azoresbioportal.uac.pt/azores-species/valenzuela-flavidus-8351/

Ecological interactions

Native status

Native

Distribution

COR; FLO; FAI*; PIC*; GRA; SJG*; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Holarctic)

Also present: MAD; CAN; CVP (Biogeographical Realm: Palearctic)

Elipsocidae

Elipsocus azoricus

Meinander, 1975

http://azoresbioportal.uac.pt/azores-species/elipsocus-azoricus-7156/

Ecological interactions

Native status

Azores endemic

Distribution

COR; FLO*; FAI*; PIC*; GRA; SJG*; TER*; SMG; SMR

Notes

Native status

Native

Distribution

FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: CAN (Biogeographical Realm: Oriental)

Biogeographical Realm: Eastern Palearctic; Near East; Nearctic; Neotropical; North Africa; Oriental

Cercopidae

Philaenus spumarius

(Linnaeus, 1758)

http://azoresbioportal.uac.pt/azores-species/philaenus-spumarius-8400/

Ecological interactions

Native status

Introduced

Distribution

TER; SMG

Notes

Also present: CAN (Biogeographical Realm: Cosmopolitan)

Also present: CAN (Biogeographical Realm: Holarctic)

Biogeographical Realm: Palearctic

Microphysidae

Loricula coleoptrata

(Fallén, 1807)

http://azoresbioportal.uac.pt/azores-species/loricula-coleoptrata-8458/

Ecological interactions

Native status

Native

Distribution

FAI; SMG*; SMR

Notes

Biogeographical Realm: Western Palearctic

Loricula elegantula

(Bärensprung, 1858)

http://azoresbioportal.uac.pt/azores-species/loricula-elegantula-8445/

Ecological interactions

Native status

Native

Distribution

FLO; PIC*; GRA; SMG*; SMR

Notes

Biogeographical Realm: Western Palearctic

Also present: CAN (Biogeographical Realm: Australian)

Cacopsylla pulchella

(Löw, 1877)

http://azoresbioportal.uac.pt/azores-species/cacopsylla-pulchella-8527/

Ecological interactions

Native status

Introduced

Distribution

PIC*

Notes

Thysanoptera

Aeolothripidae

Aeolothrips collaris

Priesner, 1919

http://azoresbioportal.uac.pt/azores-species/aeolothrips-collaris-8269/

Ecological interactions

Native status

Native

Distribution

FAI; PIC; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Palearctic)

Aeolothrips gloriosus

Bagnall, 1914

http://azoresbioportal.uac.pt/azores-species/aeolothrips-gloriosus-8271/

Ecological interactions

Native status

Native

Distribution

FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Biogeographical Realm: Palearctic

Also present: MAD; CAN (Biogeographical Realm: Cosmopolitan)

Also present: MAD (Biogeographical Realm: Holarctic)

Neuroptera

Hemerobiidae

Hemerobius azoricus

Tjeder, 1948

http://azoresbioportal.uac.pt/azores-species/hemerobius-azoricus-6862/

Ecological interactions

Native status

Azores endemic

Distribution

FLO*; FAI*; PIC; GRA; SJG; TER*; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Biogeographical Realm: Western Palearctic (Macaronesia)

Cerambycidae

Crotchiella brachyptera

Israelson, 1985

http://azoresbioportal.uac.pt/azores-species/crotchiella-brachyptera-7879/

Ecological interactions

Native status

Azores endemic

Distribution

PIC; TER; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Also present: MAD (Biogeographical Realm: Palearctic)

Ciidae

Atlantocis gillerforsi

Israelson, 1986

http://azoresbioportal.uac.pt/azores-species/atlantocis-gillerforsi-7674/

Ecological interactions

Native status

Azores endemic

Distribution

FLO; PIC; TER*; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Also present: MAD; CAN; CVP (Biogeographical Realm: Cosmopolitan)

Corylophidae

Sericoderus lateralis

(Gyllenhal, 1827)

http://azoresbioportal.uac.pt/azores-species/sericoderus-lateralis-7672/

Ecological interactions

Native status

Introduced

Distribution

COR; FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN; CVP (Biogeographical Realm: Palearctic)

Also present: MAD (Biogeographical Realm: Holarctic)

Dryophthoridae

Sitophilus oryzae

(Linnaeus, 1763)

http://azoresbioportal.uac.pt/azores-species/sitophilus-oryzae-7910/

Ecological interactions

Native status

Introduced

Distribution

FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Also present: MAD; CAN; CVP (Biogeographical Realm: Cosmopolitan)

Dryopidae

Dryops algiricus

(Lucas, 1846)

http://azoresbioportal.uac.pt/azores-species/dryops-algiricus-7545/

Ecological interactions

Native status

Native

Distribution

FLO; TER; SMG; SMR

Notes

Biogeographical Realm: Palearctic

Dryops luridus

(Erichson, 1847)

http://azoresbioportal.uac.pt/azores-species/dryops-luridus-7546/

Ecological interactions

Native status

Native

Distribution

COR; FLO; FAI*; GRA; TER*; SMG; SMR

Notes

Also present: MAD; CAN (Biogeographical Realm: Palearctic)

Biogeographical Realm: Western Palearctic (Macaronesia)

Biogeographical Realm: Western Palearctic (Macaronesia)

Hydrophilidae

Cercyon haemorrhoidalis

(Fabricius, 1775)

http://azoresbioportal.uac.pt/azores-species/cercyon-haemorrhoidalis-7400/

Ecological interactions

Native status

Introduced

Distribution

FLO; FAI; PIC; GRA; SJG; TER; SMG; SMR

Notes

Biogeographical Realm: Holarctic

Trichoptera

Limnephilidae

Limnephilus atlanticus

Nybom, 1948

http://azoresbioportal.uac.pt/azores-species/limnephilus-atlanticus-8582/

Ecological interactions

Native status

Azores endemic

Native status

Azores endemic

Distribution

FLO; FAI; PIC; SJG; TER; SMG; SMR

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Gelechiidae

Brachmia infuscatella

Rebel, 1940

http://azoresbioportal.uac.pt/azores-species/brachmia-infuscatella-8738/

Ecological interactions

Native status

Azores endemic

Distribution

FAI; PIC; SJG; TER; SMR*

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Biogeographical Realm: Western Palearctic (Macaronesia)

Also present: MAD; CAN (Biogeographical Realm: Cosmopolitan)

Also present: MAD (Biogeographical Realm: Holarctic)

Nymphalidae

Hipparchia azorina occidentalis

(Sousa, 1985)

http://azoresbioportal.uac.pt/azores-species/hipparchia-azorina-occidentalis-13545/

Ecological interactions

Native status

Azores endemic

Distribution

COR; FLO

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Hipparchia miguelensis

(Le Cerf, 1935)

http://azoresbioportal.uac.pt/azores-species/hipparchia-miguelensis-8798/

Ecological interactions

Native status

Azores endemic

Distribution

SMG

Notes

Biogeographical Realm: Western Palearctic (Macaronesia)

Tineidae

Oinophila v-flava

(Haworth, 1828)

http://azoresbioportal.uac.pt/azores-species/oinophila-v-flava-8833/

Ecological interactions

Native status

Introduced

Distribution

FLO; FAI; PIC*; TER; SMG

Notes

Analysis

Azorean Arthropod biodiversity - towards a more complete knowledge

The ultimate goal of biodiversity assessments is documenting all species inhabiting a region. However, this has often proven impossible to achieve given the unfeasibility of collecting every single species that exists in a study area. This study focuses on the terrestrial arthropod diversity of the Azores and encompasses most orders of the phylum Arthropoda. A pool of a total of 1215 species and subspecies was surveyed, representing 53% of the whole arthropod fauna known from the Azores (Borges et al. 2010). By deliberately not surveying Crustacea, Acari, Collembola, Diptera and Hymenoptera, we excluded 47% of the archipelago's species pool. Yet, this study added 10 endemic and at least 16 other species, mostly exotics, to the known Azorean arthropod fauna. More will be added soon after the on-going revision of Staphylinidae (in prep.) and Zopheridae (Borges et al. 2016, in press). Overall, at least 26 species that occur in native forests were added to the Azorean arthropod fauna list. The new 346 taxonomic records provided by this study (see Suppl. material 4 for the complete list of new records per island) represent on average an increase in species number of about 10% for each studied island (Table 2). However, the increment for São Jorge island was about 22%, while for São Miguel this represented only 3% (Table 2). 164 species were found in new islands, with an average of two islands per species. For 82 of those species only one new island was added to their known distribution contrasting with 27 species for which four or more islands were added (Fig. 2). Notably, nine out of the 27 species with more than three island added to their previous distribution belong to Arachnida. In fact, arachnids but also millipedes and centipedes experienced a large proportion of new records (more than 30%) (see Table 3).

Table 2.

Species richness for the Azores archipelago and each island. Total currently known species, the number of species surveyed during this study and those that represent new records are presented.

	Known species in the Azores	Pool of surveyed taxa	New records	New records (%)
AZORES	2316	1215	26	2.13
FLO	797	461	55	11.93
FAI	945	537	51	9.49
PIC	808	463	46	9.93
SJG	620	359	76	21.17
TER	1224	731	52	7.11
SMG	1592	861	28	3.25
SMR	799	573	38	6.63

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Figure 2. — Frequency distribution of the number of new island records per species.

Table 3.

Total species and subspecies records for the Azores, new species and subspecies records during this study and increment for the most speciose classes and orders. Values for all islands are added, so richness may be up to 7 times higher than the archipelago's richness (as 7 islands were surveyed). (*)The Coleoptera families Staphylinidae and Zopheridae were not considered (see text).

	Total records	New records	New Records (%)
Class Arachnida	362	124	34.25
Order Pseudoscorpiones	19	5	26.32
Order Opiliones	12	11	91.67
Order Araneae	331	108	32.63
Class Diplopoda	67	24	35.82
Order Polydesmida	18	8	44.44
Order Polyxenida	0	0	0.00
Order Julida	44	12	27.77
Order Chordeumatida	5	4	80.00
Class Chilopoda	21	9	42.86
Order Scutigeromorpha	0	0	0.00
Order Lithobiomorpha	7	0	0.00
Order Scolopendromorpha	4	2	50.00
Order Geophilomorpha	10	7	70.00
Class Insecta	1012	189	18,68
Order Microcoryphia	13	4	30.77
Order Zygentoma	0	0	0.00
Order Ephemeroptera	6	0	0.00
Order Odonata	0	0	0.00
Order Blattaria	7	3	42.86
Order Orthoptera	10	0	0.00
Order Phasmatodea	0	0	0.00
Order Dermaptera	14	0	0.00
Order Psocoptera	75	40	53.33
Order Thysanoptera	76	6	7.89
Order Hemiptera	290	82	28.28
Order Neuroptera	7	3	42.86
Order Coleoptera (*)	361	36	9.97
Order Trichoptera	6	4	66.67
Order Lepidoptera	147	11	7.84

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The number of species identified for each of the 18 native forest fragments surveyed is shown in Fig. 3. The fragment with the highest species diversity is Serra de Santa Bárbara in Terceira island (S = 124), which is also the larger native forest area in the Azores. Remarkably, one of the smallest fragments, Pico Alto in Santa Maria island, is the second most diverse (S = 121).

Figure 3. — Number of species per native forest fragments. Island codes as in Table 1

BALA2 samples only added 4% of species to the previous BALA survey (Fig. 4). Interestingly, 59 samples collected in the first two years of survey (1999 and 2000) provided about 81% of the total species recorded in this study.

Figure 4. — Species accumulation curve for the 286 species of arthropods collected in 152 pitfall and beating samples between 1999 and 2011. The solid line corresponds to the chronological sample sequence and the dotted line is a randomized curve (1000 runs). Samples to the left of the vertical line were collected in BALA1 and to the right in BALA2.

The most abundant species

A total of 163744 individuals were identified as belonging to the 286 species (see Suppl. material 5 for the complete list of abundance per species). The ten most abundant species (Fig. 5) accommodate 56% of the total number of individuals and include mostly indigenous species (endemic or native non-endemic). The single introduced species is the millipede Ommatoiulus moreletii (Fig. 6). With exception of the millipede Ommatoiulus moreletii, the centipede Lithobius pilicornis pilicornis and the opilion Leiobunum blackwalli (Fig. 7) that are mostly soil epigean species, the other seven species live preferentially in the canopies of Azorean endemic trees. The moth Argyresthia atlanticella (Fig. 8) is particularly common in Juniperus brevifolia and Erica azorica; the spider Savigniorrhipis acoreensis (Fig. 9) is particularly abundant in Juniperus brevifolia, but can also be found in other plants

Figure 5. — The ten most abundant species in the database. END - endemic from Azores; NAT - native non-endemic species; INTR - species introduced in the archipelago.

Figure 6. — The millipede *Ommatoiulus* *moreletii* (Credit: Pedro Cardoso)

Figure 7. — The opilion *Leiobunum* *blackwalli* (Credit: Paulo A.V. Borges).

Figure 8. — The moth *Argyresthia* *atlanticella* (Credit: Paulo A.V. Borges)

Figure 9. — The spider *Savigniorrhipis* *acoreensis* (Credit: Paulo A.V. Borges)

Discussion

Cardoso et al. (2011) identified seven impediments in invertebrate conservation. Three of them are particularly relevant for our study: most species are undescribed (the Linnean shortfall), the distribution of described species is mostly unknown (the Wallacean shortfall), and the abundance of species and its variation in space and time are unknown (the Prestonian shortfall). We argue that with the BALA project we were able to contribute to overcome some of these impediments in the Azores. In fact, we show that as a result of the standardized sampling performed in Azorean native forests we were able to: i) decrease the Linnean shortfall, by increasing the number of described Azorean endemics (e.g. Blas and Borges 1999, Ribes and Borges 2001, Platia and Borges 2002, Quartau and Borges 2003, Borges et al. 2004, Borges and Wunderlich 2008, Crespo et al. 2013, Crespo et al. 2014, Borges et al. 2016); ii) decrease the Wallacean shortfall, by increasing the known distribution of many endemic and exotic species in the archipelago (e.g. Borges et al. 2005a, Borges et al. 2006, Cardoso et al. 2009, Meijer et al. 2011); and iii) decrease the Prestonian shortfall, by using standardized sampling, which allowed the comparison of species abundances in space and time as many of the same sites were sampled in two different time periods.

The increase in the number of islands from where each species is known and the distribution increase for many species within each island shows the importance of regional standardized surveys, which provided a major improvement in the knowledge of the distribution of arthropod species in the native forests of the Azores.

The fact that most diversity was captured during the first two years of the project reflects the importance of sampling a wide geographic range covering all the islands and the maximum number of sites. Increasing the number of samples per fragment (sampling performed in 2004) or replicating the sampling at a different time (29 sites in 2010 to 2011; BALA2 project) had a lesser impact in increasing our knowledge about biodiversity (Fig. 4).

The future agenda for surveying and monitoring Azorean arthropod biodiversity includes:

a) expanding the standardized survey of Azorean arthropods to other habitat types, mostly man-modified, an already on-going task for some of the islands (see e.g. Cardoso et al. 2009, Meijer et al. 2011, Cardoso et al. 2013, Florencio et al. 2013, Santos et al. 2010);

b) selecting study areas along a comprehensive environmental gradient where an optimal sampling strategy will be applied in order to sample the entire arthropod communities (All Taxa Biodiversity Inventory - ATBI). ATBIs are intensive sampling efforts to identify and record all living species that exist within a given area and simultaneously create a common and standardized biodiversity database (Lawton and Gaston 2001);

c) finishing the identification of many morphospecies. Good progress has been made with Staphylinidade (Borges et al. in prep.), but other taxa need further effort to reach proper identification;

d) increase sampling and update the current list of Azorean Hymenoptera and Diptera, which is clearly incomplete (Borges et al. 2010). The shortage of taxonomists who can adequately identify species (i.e. the so-called Taxonomic Impediment) has prevented advances in the knowledge for many diverse groups in the Azores, including these two.

e) contributing to the validation and updating of the pan-European checklists programs, including Fauna Europaea (Jong et al. 2014) and PESI (Jong et al. 2015) allowing a more general evaluation and comparison of species distributions and statuses.

This study advances the knowledge on the unique arthropod biodiversity of the Azores, but at the same time highlights the need for further surveys. We strongly believe that the BALA project will stimulate further research and conservation actions towards the preservation of Azorean biodiversity. Furthermore, we hope that all the taxa yet to be identified will entice taxonomist to join us in the endeavour of cataloguing all terrestrial arthropods of the most remote of the Macaronesian archipelagos, the Azores. The ongoing longterm research projects in Azores and the recent creation of the E-Repository ISLANDLAB will create new opportunities for biodiversity studies in Azores.

Supplementary Material

Supplementary material 1

Appendix 1 - Detailed data on the distribution and abundance of the studied species

Borges et al.

Data type: Occurrences and abundance

Brief description: Detailed data on the occurrences and abundances of the studied species. Data on species abundance in each individual sample (pitfall trap or canopy beating) for the 152 transects in eighteen protected areas and seven Azorean islands.

File: oo_114229.xlsx

biodiversity_data_journal-4-e10948-s001.xlsx^{(5.8MB, xlsx)}

Supplementary material 2

Appendix 2 - Metadata from Appendix 1

Borges et al.

Data type: Text in pdf

Brief description: METADATA from Appendix 1 – Detailed data on the distribution and abundance of the studied species

File: oo_114225.pdf

biodiversity_data_journal-4-e10948-s002.pdf^{(203.4KB, pdf)}

Supplementary material 3

Appendix 3 - Sites UTM coordinates

Borges et al.

Data type: Sites coordinates

Brief description: UTM coordinates (regions 25S for Flores and 26S for all other islands), altitude (meters) and supporting project of the studied transects in the Azores. Transect code according to island, reserve and transect number (see text)

File: oo_114224.xlsx

biodiversity_data_journal-4-e10948-s003.xlsx^{(12.7KB, xlsx)}

Supplementary material 4

Appendix 4. Complete list of new records per island.

Borges et al.

Data type: Occurrences

Brief description: The complete list of new records per island.

File: oo_114227.xlsx

biodiversity_data_journal-4-e10948-s004.xlsx^{(29.5KB, xlsx)}

Supplementary material 5

Appendix 5 -Abundance data

Borges et al.

Data type: Abundance data

Brief description: Detailed abundance for each species in each of the 18 protected areas

File: oo_114228.xlsx

biodiversity_data_journal-4-e10948-s005.xlsx^{(28.9KB, xlsx)}

Acknowledgements

We are grateful to all researchers that collaborated in the field and lab work: Álvaro Vitorino, Anabela Arraiol, Annabella Borges, Ana Rodrigues, Francisco Dinis, Emanuel Barcelos, Hugo Mas, João Amaral, João Moniz, Lara Dinis, Paula Gonçalves, Sandra Jarroca and Luís Vieira. The Forest Services provided logistic support on each island. Acknowledgments are due to the taxonomists Fernando Ilharco, Ole Karsholt, Wolfgang Rücker and Richard zur Strassen who assisted with species identification. This work was funded by the Azorean Direcção Regional dos Recursos Florestais (Azorean Government / project 17.01-080203) and FCT- project PTDC/BIA-BEC/100182/2008 – “Predicting extinctions on islands: a multi-scale assessment”. Additional data was obtained from project ATLANTISMAR (DRCT–M2.1.2 /I/027/2011). CR was supported by FCT grant SFRH/BPD/91357/2012. AMCS was supported by a Marie Curie Intra-European Fellowship (IEF 331623 ‘COMMSTRUCT’) and by a Juan de la Cierva Fellowship (IJCI-2014-19502) funded by the Spanish ‘Ministerio de Economía y Competitividad’. Open Access was funded by national funds through FCT - Fundação para a Ciência e a Tecnologia in the frame of the project UID/BIA/00329/2013 (2015-2017).

Author contributions

PAVB, ARMS, JQ and KAT conceived the ideas; PAVB, CG, LC, FR, PC, FP, CR, IRA, CM, CA, GA, SPR, JH, AMCS, ABS, JW, JAQ, ARMS and KAT obtained samples; PAVB, CG, EM and LB prepared the databases; PAVB, LC, PC, HE, FI, VM, MTP, JR, AB, ABS, RzS, VV, JW, JAQ and ARMS performed taxonomic work and identified species; PAVB led the writing with substantial input from the other authors.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary material 1

Appendix 1 - Detailed data on the distribution and abundance of the studied species

Borges et al.

Data type: Occurrences and abundance

File: oo_114229.xlsx

biodiversity_data_journal-4-e10948-s001.xlsx^{(5.8MB, xlsx)}

Supplementary material 2

Appendix 2 - Metadata from Appendix 1

Borges et al.

Data type: Text in pdf

Brief description: METADATA from Appendix 1 – Detailed data on the distribution and abundance of the studied species

File: oo_114225.pdf

biodiversity_data_journal-4-e10948-s002.pdf^{(203.4KB, pdf)}

Supplementary material 3

Appendix 3 - Sites UTM coordinates

Borges et al.

Data type: Sites coordinates

File: oo_114224.xlsx

biodiversity_data_journal-4-e10948-s003.xlsx^{(12.7KB, xlsx)}

Supplementary material 4

Appendix 4. Complete list of new records per island.

Borges et al.

Data type: Occurrences

Brief description: The complete list of new records per island.

File: oo_114227.xlsx

biodiversity_data_journal-4-e10948-s004.xlsx^{(29.5KB, xlsx)}

Supplementary material 5

Appendix 5 -Abundance data

Borges et al.

Data type: Abundance data

Brief description: Detailed abundance for each species in each of the 18 protected areas

File: oo_114228.xlsx

biodiversity_data_journal-4-e10948-s005.xlsx^{(28.9KB, xlsx)}

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PERMALINK

New records and detailed distribution and abundance of selected arthropod species collected between 1999 and 2011 in Azorean native forests

Paulo AV Borges

Clara Gaspar

Luís Carlos Fonseca Crespo

François Rigal

Pedro Cardoso

Fernando Pereira

Carla Rego

Isabel R Amorim

Catarina Melo

Carlos Aguiar

Genage André

Enésima P Mendonça

Sérvio Ribeiro

Joaquín Hortal

Ana MC Santos

Luís Barcelos

Henrik Enghoff

Volker Mahnert

Margarida T Pita

Jordi Ribes

Arturo Baz

António B Sousa

Virgílio Vieira

Jörg Wunderlich

Aristeidis Parmakelis

Robert J Whittaker

José Alberto Quartau

Artur RM Serrano

Kostas A Triantis

Abstract Abstract

Background

New information

Introduction

Materials and methods

Figure 1.

Table 1.

Checklists

Checklist of the Studied Azorean Arthropods

Animalia

Arthropoda

Arachnida

Pseudoscorpiones

Chthoniidae

Chthonius ischnocheles

Ecological interactions

Native status

Distribution

Notes

Chthonius tetrachelatus

Ecological interactions

Native status

Distribution

Notes

Neobisiidae

Neobisium maroccanum

Ecological interactions

Native status

Distribution

Notes

Opiliones

Phalangiidae

Homalenotus coriaceus

Ecological interactions

Native status

Distribution

Notes

Leiobunum blackwalli

Ecological interactions

Native status

Distribution

Notes

Araneae

Araneidae

Gibbaranea occidentalis

Ecological interactions

Native status

Distribution

Notes