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PATTERNS OF COLONIZATION AND SPECIES DISTRIBUTION FOR AZOREAN : EVOLUTION, DIVERSITY, RARITY AND EXTINCTION

Paulo A.V. Borges1, Clara Gaspar1, Ana M.C. Santos1, Sérvio Pontes Ribeiro1,2, Pedro Cardoso1,3, Kostas A. Triantis1,4 & Isabel R. Amorim1,5

1 Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Pico da Urze, 9700-042 Angra do Heroísmo, Portugal e-mail: [email protected] 2 Universidade Federal de Ouro Preto, Instituto de Ciências Exatas e Biológicas, Lab. Ecologia Evolutiva de Herbívoros de Dossel/DEBIO, campus Morro do Cruzeiro, 35400-000, Ouro Preto, MG, Brasil 3Smithsonian Institution, National Museum of Natural History, Washington, DC, USA Department of Biology, Texas State University, San Marcos, TX, USA 4Biodiversity Research Group, Oxford University Centre for the Environment, South Parks Road, Oxford, OX1 3QY, UK 5School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, England, UK

ABSTRACT Here we address a list of questions based on long-term ecological and biogeographical studies performed in the , a remote volcanic oceanic archipelago composed by nine islands. The target group are the arthropods, and the main habitat the Laurisilva, the Azorean native . Diversification of Azorean species is affected by island age, area and isolation. However, results obtained for over a decade show that distinct groups are differently affected by these factors, which has lead to the extreme diverse distribution patterns currently observed. Spatial distribution of arthropods in each island may be interpreted as caused by a typical “mass effect”, with many species following a “source-sink” dynamics. Truly regionally rare species are those that are habitat specialists, many of them being threatened endemic species. Although various endemics persist as sink populations in human-made habitats (e.g., exotic ), more than half of the original endemic forest arthropods may already have vanished or may eventually be driven to extinction in the future. Those species which have evolved in and are mainly found in native forests, have been dramatically affected by hitherto unrecognized levels of extinction debt, as a result of extensive destruction of native forest. We argue that immediate action to restore and expand native forest

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habitat is required to avoid a future of disastrous extinctions of a biologically unique fauna with an unique evolutionary history.

RESUMO Com base em estudos ecológicos e biogeográfi cos realizados nos Açores (um arquipélago remoto composto por nove ilhas vulcânicas) durante muitos anos de uma forma continuada, apresentamos um conjunto de questões. O grupo alvo são os artrópodes e o principal habitat é a Laurissilva, a fl oresta nativa dos Açores. A diversifi cação das espécies de artrópodes dos Açores é afectada pela idade das ilhas, área das ilhas e seu isolamento. No entanto, os estudos que decorreram durante os últimos dez anos mostram que os vários tipos de grupos taxonómicos e ecológicos são afectados de forma diferente por estes factores, tendo como consequência padrões de distribuição espacial únicos. A distribuição espacial dos artrópodes em cada ilha é causada for “efeitos de massa”, muitas espécies possuindo dinâmicas “fonte-sumidouro”. As espécies verdadeiramente raras à escala regional são aquelas que são especialistas de um particular habitat, muitas delas sendo espécies endémicas ameaçadas. Embora várias espécies endémicas persistam com populações sumidouro em habitats criados pelo Homem (e.g. fl orestas exóticas), mais de metade das espécies especialistas da fl oresta nativa já estão extintas ou poderão extinguir-se no futuro. De facto, aquelas espécies que evoluíram e apenas são encontradas nas fl orestas nativas, foram afectadas de forma dramática como resultado da destruição alargada das fl orestas nativas dos Açores. Defendemos que a única forma de evitar a extinção de uma fauna única das fl orestas nativas dos Açores será através de medidas de restauro desta fl oresta.

INTRODUCTION lated oceanic islands like the Galápagos, Hawaii and . harles Darwin and Alfred Their initial observations and CR. Wallace were both fasci- conclusions were seminal for nated by islands and the the formulation of comprehen- foundations of their evolutionary sive theorems and hypotheses theory were mostly based on on evolutionary mechanisms evidences obtained from iso- responsible for the maintenance

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and increase of biodiversity become fundamental to the following island colonization. understanding of the evolution, Since then, islands have been biology and ecology of regarded as natural laborato- and . Good examples ries for the study of evolution- are the now classic works of ary, ecological and ecosystems Carlquist (1974) and Williamson processes (Vitousek et al., 1995; (1981). Some important works Wagner & Funk, 1995; Clarke were published about island & Grant, 1996; Thornton, 1996; archipelagos, like the Atlantic Whittaker & Fernández-Palacios, Islands (Berry, 1992; Hounsome, 2007), due to their isolated 1993; Biscoito, 1995; Ashmole character and their depauperated & Ashmole, 2000; Fernández- and disharmonic faunas and floras Palacios & Martin Esquivel, (Carlquist, 1974; Williamson, 2002; Fernández-Palacios & 1981; Whittaker & Fernández- Morici, 2004; Serrano et al., Palacios, 2007). Changes in traits 2010), Hawaii (Wagner & Funk, related to defences and flight, 1995), Krakatau (Thornton & species radiation and endemism, Rosengren, 1988; Thornton, as well as occupation of vacant 1996), Pacific Islands (Keast & niches, are just some examples Miller, 1996) and Pitcairn Islands of important fundamental con- (Benton & Spencer, 1995). cepts in Evolutionary Ecology Special publications on evolu- developed as the result of data tion on islands (Clarke & Grant, obtained from island biology 1996; Emerson, 2002; Gillespie studies (Whittaker & Fernández- & Roderick, 2002) and one Palacios, 2007). Not surprisingly, unique on ecological function one of the most popular models (Biological Diversity and in ecological literature is the Ecosystem Function on islands “Theory of Island Biogeography” - Vitousek et al., 1995) have (MacArthur & Wilson, 1963, 1967), been published recently. More designed to explain patterns of than describing unusual body species richness on islands, but adaptations, such as wingless with wider applications, namely birds and giant, arborescent in biodiversity, conservation and herbs, recent studies emphasise management (Rosenzweig, 2004). how unique and distinct oceanic Studies of island species island ecosystems are. Special and their natural histories have attention is given to how fragile

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these ecosystems are and the with other archipelagos (e.g., need of urgent conservation ) resulted in it measures. receiving less attention (but see Here we describe the results Wallace, 1876). of a long-term ecological study Crotch (1867) comments on the on arthropods carried out in the almost complete indifference of Laurisilva, the native forest of naturalists towards the Azores, the Azores, a remote volcanic noting, as an example, that while oceanic archipelago. We address the English entomologist T.V. a list of questions arising from Wollaston intensively sampled the results obtained from a in archipelagoes of Madeira, number of studies performed in the Canaries and Cape Verde, the last ten years. he did little in the Azores. The historical lack of interest on AZOREAN NATURAL Azorean arthropods can, in HISTORY AND BIODIVERSITY part, be explained by the lack of knowledge of the faunistic Charles Darwin visited the composition of many Azorean Azores during the expedition taxa until recently (but see of the Beagle (September 1836) Borges et al., 2005a, 2010a), but (Keynes, 1988). Despite a dis- this trend is changing. Recently cussion on the mechanisms of there has been an increasingly dispersal, making reference to interest in the Azorean biota the neighbouring archipelago that is reflected in the raising of Madeira, and some mention number of publications on the to arborescence of azorica biogeography, ecology, applied (only studied recently by entomology, biospeleology and Ribeiro et al., 2003), he made systematics of its arthropods no significant comments about (see details below). The present the arthropods of the Azores. work shows the importance Although the Azores is an of evidence obtained from the isolated archipelago with a Azores for the understanding of diverse geological history and general island processes. a wide range of elevations, the The current estimate of terres- relatively low endemic richness trial species and/or subspecies in and the lack of remarkable the Azores is 6,164 (about 6,112 adaptive radiation compared species), of which 452 (411 spe-

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cies) are endemic (Borges et al., of native species by exotic ones 2010a) (see Table 1). Arthropods and climate change, may affect are the most diverse taxon with Azorean biodiversity and eco- about 2,298 species and subspe- system functioning. In the last cies, 266 of which are endemic ten years we have invested con- (Table 1; see also Borges et al., siderable effort to raise aware- 2010a). ness about the importance of Azorean arthropod biodiversity AZOREAN ARTHROPOD relative to the total biodiversity BIODIVERSITY: THE MAIN of the Azores and of the Atlantic QUESTIONS Biogeographic Region (see e.g., Borges et al., 2005a, 2008a, Invertebrates are generally 2010a). Our ultimate goal is to relegated to a secondary place in ensure that the highly diverse biodiversity conservation pro- endemic arthropods island bio- grams and there are sociologi- diversity conservation areas are cal, educational and scientific protected, in the hopes that this reasons for this (Cardoso et al., will halt, and hopefully reverse, 2011a, b). One significant fac- the general trend of biodiver- tor is the lack of communication sity decline in the Azores (see between scientists and stake- Triantis et al., 2010a). holders and overcoming this The BALA project (2000-2010; problem is essential for all ongo- Biodiversity of Arthropods from ing arthropod research projects. the Laurisilva of the Azores) Conservation of the Azorean (see Borges et al., 2000, 2005b; natural biodiversity requires the Gaspar et al., 2008), that sur- elaboration of a global and in- veyed arthropods distribution tegrated strategy based on the in Azorean native forests, was knowledge of current species an important step towards the distributions and how of cur- inclusion of arthropod groups in rent land-use will impact future biodiversity conservation plan- distributions (see e.g., Borges et ning in the Azores. The system- al., 2008; Cardoso et al., 2009b; atically collected data allowed Meijer et al., 2011). Consequently inferences to be made about the it is crucial to understand how biology, ecology, rarity and con- land overexploitation, increased servation status of the different tourist activities, displacement arthropod species. Transects

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TABLE 1. Total and endemic terrestrial diversity (species and subspecies) of the main groups of the Kingdoms Fungi, Chromista, Protoctista, Plantae and Animalia in the Azores (more details in Borges et al., 2010a). Kingdom and Phylum/ Common name Total Endemic Division FUNGI 1328 34 Zygomycota (Fungi) Zygomycete fungi 2 0 Ascomycota (Fungi) Sac fungi, Cup fungi 231 20 Ascomycota (Lichen) Lichen 775 10 Basidiomycota (Fungi) Basidiomycete fungi 307 4 Basidiomycota (Lichen) Lichen 6 0 Lichen (Fungi Imperfecti) Lichen 7 0 CHROMISTA 4 0 Oomycota Water molds 4 0 PROTOCTISTA 575 7 Bacillariophyta Diatoms 536 7 Amoebozoa Amoebae 39 0 PLANTAE 1590 80 Bryophyta Bryophytes 480 7 Anthocerotophyta Hornworts 5 0 Marchantiophyta Liverworts 164 1 Bryophyta Mosses 311 6 Tracheobionta Vascular Plants 1110 73 Lycopodiophyta Quillworts 7 1 Pterydophyta Ferns 69 6 Pinophyta Gymnosperms 4 1 Magnoliophyta Dicots and monocots 1030 65 ANIMALIA 2667 331 Platyhelminthes Flatworms 31 0 Nematoda Roundworms 131 2 Annelida Earthworms 22 0 Mollusca Slugs and snails 114 49 Arthropoda Arthropods 2298 266 Chordata (Vertebrata) Vertebrates 71 14 TOTAL 6164 452

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(150 m x 5 m) were randomly goals (noted below) were pur- placed within fragments of pro- sued: tected native forest. The number of transects per forest fragment Inventory of Azorean arthropods was set up using a logarithmic and diversity hotspots scale, assuming a species-area - list all arthropod taxa from relationship (SAR) with a slope the Azores (see Borges et al., (z) of 0.35 in a log-log scale (i.e., 2005c, 2010b); a 10 fold area increase implies - describe new taxa (Blas & a duplication of the number of Borges, 1999; Ribes & Borges, species): 2 transects were set 2001; Platia & Borges, 2002; up for 10 ha forest fragments, Quartau & Borges, 2003; 4 transects for 100 ha frag- Borges et al., 2004, 2007; ments and 8 transects for 1,000 Borges & Wunderlich, 2008); ha fragments. Consequently, - examine the shape and charac- higher sampling effort was ap- teristics of discovery curves plied to larger protected native in order to obtain a provi- forest areas (i.e. “proportional sional picture of the taxo- sampling”), making it possible nomic completeness of cur- to capture not only “area per se rent inventories and an esti- effects” but also unveil patterns mation of the amount of work that could be prevalent in larger still needed to attain taxo- areas, such as, spatial beta diver- nomic completeness (Lobo & sity. Borges, 2010). In this paper we compile - identify hotspots of species and synthesize the results of diversity in the Azores (e.g. recent research on the biodi- Borges et al., 2005b; Borges & versity and ecology of Azorean Gabriel, 2009). arthropods, which were at least partly based on data obtained Ecological patterns of species from long term projects (e.g., distribution and abundance BALA, “Biodiversity of cave (i.e. rarity) invertebrates”), and many oth- - test if the He & Gaston (2003) ers of shorter duration (e.g., abundance–variance–oc- Interfruta). During the last ten cupancy model accurately years several general questions predicts species distribution were raised and several specific across different spatial scales

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and whether endemic, na- arthropod species (Ribeiro & tive (non-endemic) and intro- Borges, 2010); duced species occupy differ- ent parts of the abundance– Evaluate the role of environmental variance–occupancy space variables (Gaston et al., 2006); - examine how a variety of biotic, - assess patterns of distribu- abiotic and anthropogenic fac- tion and species richness of tors infl uence endemic and in- canopy phytophagous in- troduced arthropod richness sect among islands and host on an oceanic island (Terceira) plants (see Ribeiro et al., 2005; (Santos et al., 2005; Borges et al., Santos et al., 2005); 2006); - describe patterns of rarity in - evaluate the degree to which one well-sampled island, i.e., environmental suitability as- Terceira, identifying types sessed with presence/absence of local pseudo-rare species models account for abun- (Borges et al., 2008); dance estimates (Jimenez- - explore patterns of diversity, Valverde et al., 2009); abundance and distribution of different taxonomic, colo- Effects of scale and sampling on nization and trophic groups species richness, beta diversity of arthropods in Azorean na- and density tive forests at different strata - analyze the effect of varia- and sites (Gaspar et al., 2008); tion in the size of sampling - test the “resource concentra- units on species richness es- tion hypothesis”, that pre- timations, and evaluate the dicts there is a positive rela- accuracy of the predictions tionship between the density obtained with various estima- of phytophagous or tors presently available when predator arthropods and the different strategies are used spatial distribution/abun- to group the same dataset dance of host plants (Ribeiro into different sized samples & Borges, 2010); (Hortal et al., 2006); - test if more abundant and - assess how differently beta widespread species are diversity measures for in- those that support popula- cidence data and pairwise tions of the rarest regional comparisons behave with re-

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gard to varying degrees of extending this to the rest of sampling effort, and recom- Macaronesia (Cardoso et al., mend diversity measures that 2010a; Triantis et al., 2010b); are relatively robust to un- - identify the biogeographi- dersampling (Cardoso et al., cal factors underlying spi- 2009a); der species richness in the - test the hypothesis that “host- Macaronesian region and habitat area” affects the fol- assessing the importance of lowing density esti- species extinctions in shaping mates: mean number per current diversity (Cardoso et canopy or reserve transects al., 2010a); (Ribeiro & Borges, 2010). - investigate whether there is a significant gain in in- Effect of disturbance in ecological formation if one uses non- communities parametric richness esti- - understand how several taxo- mators to build SAR models nomic and ecological attri- with standardized surveys butes of arthropod communi- data, rather than using the ties vary with respect to dif- observed number of species

ferent levels of disturbance (Sobs) (Borges et al., 2009); as well as assessing to what - investigate if species-area extent potential disturbance relationships from entire ar- factors are influencing site chipelagos are congruent integrity (Santos et al., 2005; with those of their constituent Cardoso et al., 2007); islands (Santos et al., 2010).

Biogeography of Azorean arthropods Surrogacy patterns in arthropods - investigate some biodiversity - evaluate the effectiveness of patterns relating to spider arthropods as predictors of distribution between islands, diversity for a wide range habitats, colonization status of taxonomic and non-taxo- and biogeographical origin nomic groups, for multiple (Borges & Wunderlich, 2008); measures of biodiversity and - study the factors promot- for different spatial scales ing diversification of several (Gaspar et al., 2010); Azorean arthropod groups - evaluate the effectiveness of (Borges & Hortal 2009) and cave-adapted arthropods as

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predictors of diversity of rare agement priority taxa in bryophytes in cave entrances Macaronesia and in the and the diversity of bacteria Azores, the so-called Top 100 in cave mats. (Cardoso et al., 2008; Martín et al., 2010). Conservation of Azorean arthropods - genetic characterization of - examine the relative value of 19 populations of endemic species forest fragments in seven of the to investigate their uniqueness Azorean islands to improve and examine how this informa- the conservation of Azorean tion could help in the prioriti- soil epigean arthropod biodi- zation of conservation eff orts. versity (Borges et al., 2005b; Gaspar et al., 2011); WHAT HAVE WE LEARNED - investigate the relationships SO FAR? between endemic and intro- duced arthropod richness, Inventory of Azorean arthropods to assess whether areas with and diversity hotspots high levels of endemic spe- The knowledge base of cies richness deter invasions Azorean arthropod biodiversity (Borges et al., 2006); is not uniform, and many - investigate the relevance of groups have not been adequate- current human-made habitats ly sampled. Furthermore, many (e.g. exotic forest; agroeco- groups have not received appro- systems) for the protection of priate taxonomic revision, due rare species (see Cardoso et to little traditional taxonomic al., 2009b, 2010b; Meijer et al., research being carried out in 2011); the last decade, and the lack of - test nestedness patterns of en- taxonomists familiar with the demic, native and introduced Azorean fauna (Amorim, 2005; species (Cardoso et al., 2010b); Borges et al., 2005a; Lobo & - quantify the magnitude and Borges, 2010). As with any other taxonomic distribution of ex- biome, solving this problem tinction debt in the Azores as is not simple since, for exam- an important step for effec- ple, traditional taxonomic work tive conservation planning has been neglected in the last (Triantis et al., 2010a); decades in Europe (see Boero, - list the 100 highest man- 2010). The most relevant effort

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to rectify the lack of taxonomic fragments play a much more expertise preventing advance important role than previously in biodiversity research was the thought (see Borges et al., 2005b; establishment of the “Azorean Borges & Gabriel, 2009). For Biodiversity Group” (http://cita. instance, based both on the angra.uac.pt/biodiversidade/), presence of unique species and that, among other things, is sup- high species richness, the Pico porting research on classical (as Alto region in the archipelago´s well as molecular) oldest island, Santa Maria, and ecology of arthropods of the is a hotspot of biodiversity Azores. Moreover, the web site (Borges et al., 2005b; Borges & “Azorean Biodiversity Portal” Gabriel, 2009). Over 57 endemic (http://www.azoresbioportal. arthropod species are known angra.uac.pt/) (see Borges et al., from Pico Alto (Santa Maria Isl.), 2010c) allows everyone to ac- i.e. 21% of the Azorean endemic cess updated information on arthropods occurring in an area Azorean biodiversity. As a di- representing <0.25% of Azorean rect outcome of this online data- native forests. Other relevant base many national and interna- areas occur on the islands of tional taxonomists have shown a São Miguel (Pico da Vara), growing interest in Azorean bio- Terceira (Terra Brava, Caldeira diversity and many new collabo- da Serra de Santa Bárbara), São rations have been established, Jorge (Topo), Pico (Caveiro, including taxonomic revisions Mistério da Prainha) and Flores (see Borges et al., 2010b) and (Morro Alto and Pico da Sé) (see additional field work to collect Borges & Gabriel, 2009; online specimens. at http://www.azoresbioportal. The results obtained during angra.uac.pt/files/publicacoes_ the BALA project (see above) Brochura BIODIVERSIDADE showed that some forest reserves AORES vFINAL.pdf). are clearly more diverse than Results obtained from oth- others, both in terms of alpha er studies, such as the survey and gamma diversities. The of subterranean invertebrates effect of forest fragmentation has (1999-2005) revealed the poor not been studied in detail (see stage of knowledge on the future work below), but the data Azorean cave invertebrates. For obtained suggests that small instance, the number of cave

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Trechus listed for the islands in- a clear dominance of generalist creased from 4 to 7, plus an epi- species in canopies of Azorean gean species in the same genus and , which holds (Borges et al., 2004; Amorim, also true for the overall spider 2005; Borges et al., 2007). and chewing insect communities in Terceira island (Borges et Ecological patterns of species dis- al., 2008). The observation of tribution and abundance (i.e. a widespread distribution of rarity) spiders on tree canopies in the The data for diverse species native forest could be explained assemblages at different spatial by their high dispersal ability scales, regardless of species and generalist feeding habits status, can be well described (Borges & Wunderlich, 2008). by an abundance-variance- Consequently, the abundance occupancy model (Gaston et al., of herbivorous insects seems 2006). Most importantly, we to be strongly affected by the observed that outliers include occurrence and population restricted specialized forest densities of spider species. endemic species (e.g. Trechus One particular plant species, terrabravensis and Cedrorum Erica azorica, has greater than azoricus azoricus) that only expected herbivore densities per occupy pristine native forest crown, possibly as it represents sites where they are quite enemy free/predictable space abundant (Gaston et al., 2006). (Ribeiro & Borges, 2010). In the We have found that free- case of agricultural habitats, we living herbivores insect in the found that both abundance and canopies of Azorean native species richness of predatory forests are mainly generalists, groups inhabiting the canopy as expected for a relatively of different fruit trees (apple, young and isolated volcanic orange, and peach trees) are archipelago (Ribeiro et al., 2005). negatively correlated with Interestingly, the proportion canopy volume, and positively of rare species is higher for correlated with tree density. herbivores insects than for On the other hand, herbivore predatory arthropods (Borges species, especially sucking insect et al., 2008). Ribeiro & Borges species, show the opposite trend (2010) also showed that there is (Santos et al., 2005).

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In terms of rarity, four arthropods from very specific important types were detected habitats typical of volcanic in the Azores (see Borges et al., islands such as the Azores - lava 2008; Ribeiro & Borges, 2010): tubes and volcanic pits - revealed 1) dense and intermediately that cave adapted species rarity dense species; 2) truly rare vary as a function of cave species, which are rare on any abundance and the number that host species and with very low have actually been sampled (see population densities regionally; Amorim, 2005). For the most 3) pseudo-rare species found studied Azorean cave beetle in small numbers on a specific species, (in the genus Trechus) host tree, which are dense on some are found at high densities neighbouring tree species, i.e. at many sites (e.g., T. picoensis host-tourists; 4) pseudo-rare from Pico Isl. occurs in 9 caves species found in small numbers and 134 specimens have been on any tree species that are collected so far from the Torres common in other habitats on the lava tube), while others are only island, i.e., habitat-tourists. found at one site and despite Truly rare and specialist the amount of sampling efforts species should also be favoured involved only a few specimens by the presence of large have been collected (e.g., only quantities of resources, and 2 individuals of T. jorgensis are although large tree species have known from Bocas do Fogo pit similar numbers of rare species, in São Jorge Isl.). most of these species are truly rare on Juniperus brevifolia, Evaluate the role of environmental Laurus azorica and Erica azorica variables (see Ribeiro & Borges, 2010). We have shown for the soil Therefore, the high frequency arthropod fauna of native for- of E. azorica and J. brevifolia est in Terceira Island that abiotic populations throughout the (climatic and geomorphologi- Azorean native forest fragments cal) variables provided a better creates the opportunity for the explanation for the variation in survival of rare insect and spider endemic species richness than species populations on these anthropogenic ones, whereas hosts (Ribeiro & Borges, 2010). the inverse was observed with Other surveys focused on respect to introduced species

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richness (see Borges et al., 2006). several nonparametric estima- Concerning the abundance of tors presented certain insensi- species, Jimenez-Valverde et al., tivity to how samples are aggre- (2009) observed that Azorean ar- gated (Hortal et al., 2006). thropod species are highly influ- Cardoso et al., (2009a) dem- enced by land-use variables, in onstrated that beta diversity such a way that the climate fac- values are close to the real val- tors lose relevance and the cli- ues, when communities being matic suitability may be diluted compared approach sampling

in predicting local abundance completeness. However, the β-2 of species. However, in their index from Harrison et al., (1992) analysis of the arthropod com- should be used as the most con- munities associated with fruit sistent measure in cases in which orchards, Santos et al., (2005) the sampling completeness de- found a strong influence of both gree of a dataset is unknown. climatic and anthropogenic vari- In general, the three structural- ables on the abundance and di- ly most complex and abundant versity of different functional plant “host islands”, i.e., E. guilds. azorica, J. brevifolia and L. azorica, accumulated the highest Effects of scale and sampling in proportion of regionally rare species richness, beta diversity arthropod species, corroborating and density the “host as an island hypothesis” Arthropod data from BALA´s (Ribeiro & Borges, 2010). standardized sampling proto- col was used to evaluate the ef- Effect of disturbance in ecological fects of scale (across sites, for- communities est fragments and islands) and In broad terms current frag- sampling in species richness, ments of Azorean native forest beta diversity and density (see are not uniform in their conser- Hortal et al., 2006; Cardoso et al., vation status. In fact, Cardoso 2009a; Ribeiro & Borges, 2010). et al. (2007) clearly demon- Several estimators (ACE, Chao1, strated that when using an Index Jackknife1 and 2 and Bootstrap) of Biotic Integrity (IBI) adapted provided consistent estimations to the epigean arthropods of the of species richness, regardless of Azorean native forests, many sample grain size. In addition fragments of native forest would

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be considered highly disturbed. Hortal, 2009; but see Cardoso et More importantly, these au- al., 2010a). The main conclusion thors showed that most species was that due to the recent age thrived in highly disturbed sites of the archipelago (see Borges are of limited importance for & Hortal, 2009; Triantis et al., conservation efforts, and that 2010b) a simple area-age model the percentage of endemic spe- (AT) is adequate for the Azorean cies is significantly higher in fauna, and not the more com- pristine than in degraded sites. plex area-age-age2 (ATT2) first- ly proposed by Whittaker et al. Biogeography of Azorean arthropods (2008, 2009) within the context Borges & Brown (1999) of The General Dynamic Model showed that island geological of Oceanic Island Biogeography age was an important variable (GDM). In fact, when testing the explaining Azorean endemic GDM, Borges & Hortal (2009) arthropods species richness. showed that: i) cave species Recently, there has been in- appear to have evolved quite creased interest in the determin- quickly, producing a number of ing the importance of geologi- species during the initial stages cal age and other geographical of island development, when variables to explain patterns of cave systems formed by lava island diversity in Macaronesia tubes and volcanic pits were (e.g. Whittaker et al., 2008, 2009; abundant and pristine prior to Borges & Hortal, 2009; Borges et natural collapsing of structures; al., 2009; Cardoso et al., 2010a; ii) taxa with low dispersal abil- Triantis et al., 2010b). ity, particularly beetles, showed In most of these studies the strong negative relationships main observation was that a with the distance to Santa Maria, combination of islands’ area the oldest island and reservoir of and geological age are enough lineages either coming from the to provide a basic explanation mainland or remaining from the for the diversity of endemic ar- older archipelago composed of thropods in the Azores, in spite Santa Maria and the Northeast of some differences between part of São Miguel; iii) the diver- taxonomic or ecological groups sity of evolutionary responses in and the additional role of is- different organisms is so var- land relative isolation (Borges & ied that no general model, like

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the one proposed by Whittaker could be studied as four data and colleagues (Whittaker et al., points when testing the relation- 2008, 2009) is able to predict the ship between species richness patterns and processes of diver- and area. Borges et al. (2009) sification. found that if data comes from Spiders apparently follow a standardized surveys (as is the different pattern from the one case of BALA data), the slope observed for most arthropod and goodness of fit for species groups. Analyzing the biogeo- area relationships obtained with graphical factors underlying estimated values (using non- spider species richness in the parametric estimators; see also Macaronesian region Cardoso Hortal et al., 2006) were not sig- et al. (2010a) showed that for nificantly different from those the Azores, island area and the obtained from observed species proportion of remaining natural richness. forest were the best predictors Molecular data generated for of species richness. The effect of a few Azorean endemic arthro- island age on species richness, pods groups (the beetles Trechus if important in diversification and Tarphius, and the butter- processes, has nowadays been fly ) and their neigh- masked by the effect of native boring insular and continental . Triantis congeneric species reveal that et al. (2010b) found that the AT the Azorean taxa form mono- model was the most parsimoni- phyletic clades (Fujaco et al., ous for explaining diversity pat- 2003; Amorim, 2005). This sup- terns of indigenous, endemic, ports single colonization events single island endemic and pro- of the Azores, as expected for portion of single island endemic such remote oceanic island. If beetles and arthropods in the true, then the diversification Azores, corroborating the re- currently observed within these sults of Borges & Hortal (2009). groups would be the result of in- Santos et al. (2010) observed tra archipelago speciation from that archipelagos follow the single ancestors, as opposed of same island species–area rela- multiple arrivals of distinct line- tionships (ISAR) as their consti- ages (Amorim et al., subm.). tuent islands, which means that Nevertheless, the possibility that the Macaronesian archipelagos multiple colonization events oc-

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curred but have gone extinct described species known from cannot be completely dismissed. the Azores is continuously ris- ing (Borges et al., 2010a), but a Surrogacy patterns in arthropods great proportion are recently Gaspar et al. (2010) evaluated introduced ones, that tend to the effectiveness of taxonomic, exhibit lower densities, less spa- colonization and trophic groups tial density variance, and oc- of arthropods from native forests cupy fewer sites than native and of the Azores archipelago as sur- endemic species (Gaston et al., rogates of the diversity of other 2006). On Terceira island, non- arthropod groups. The results indigenous species are mainly indicated that spiders (Araneae) limited to those sites under an- and true bugs () may thropogenic influence located be more promising surrogates mainly on low to medium alti- of arthropod diversity for the tude areas or, when in high-alti- Azorean native forests at the tude forests, in marginal areas of transect, fragment and island the few forest remnants (Borges scales (Gaspar et al., 2010). As et al., 2006). For example, the spiders are easy to identify, protection of forest specialists, abundant in both terrestrially like the ground-beetles Trechus and within tree canopies (Borges terrabravensis and Cedrorum azo- & Wunderlich, 2008; Borges ricus azoricus (see Gaston et al., et al., 2008; Gaspar et al., 2008) 2006) requires the management and probably good indicators of invasive species, to avoid of futures trends for other taxa them entering the pristine native (Cardoso et al., 2010a), we sug- forest sites, such as those found gest the use of this group for fu- in Serra de Santa Bárbara (see ture rapid monitoring studies in also Borges et al., 2006; Cardoso Azorean forests. et al., 2007). The impacts of land use Conservation of Azorean arthropods changes are severe (Borges et al., Human activities and inva- 2008; Cardoso et al., 2009) and sive species are among the most many Azorean endemic forest important factors impacting dependent species are on the Azorean arthropod communi- edge of extinction (Triantis et al., ties (Godman, 1870; Borges et 2010a). Despite the fact that un- al., 2006, 2008). The number of managed exotic forests are pro-

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viding alternative habitat suit- could explain the nested pat- able for some endemic species tern for endemics. (forest specialist arthropods, Interestingly, hardly any ex- particularly saproxylic beetles otic insect or spider were able from S. Maria Island; Meijer to colonize the native forest can- et al., 2011), most endemic for- opy habitat (Borges et al., 2008; est specialist arthropods are Borges & Wunderlich, 2008), so restricted to native forests and are not widespread in all the only have sink populations in Azorean habitats. For instance, semi-natural grasslands or ex- the Azorean Laurisilva seems otic forests (Borges et al., 2008; that has not yet been colonized Cardoso et al., 2009; Triantis et by any of the invasive ant spe- al., 2010a). cies found adjacently to hu- Endemic and introduced man constructions. Spiders are species were all found to be the most abundant terrestrial highly nested in habitats of predators in the Azores (Borges Terceira Island. Indeed, native & Wunderlich, 2008; see also forests and intensively man- Gaspar et al., 2008), particular- aged pastures seem to be the ly in forests, and may serve as main drivers of species compo- early indicators for future disap- sition at any site, having most- pearance patterns of other insu- ly endemic and introduced lar taxa (Cardoso et al., 2010a). species, respectively (Cardoso The most disturbed study sites et al., 2010b). This result im- in the Azores were found on the plies that there is a predictable islands of Faial (Cabeço do Fogo), pattern of species loss and gain Flores (Caldeiras Funda, Rasa), from natural forests to exotic Pico (Lagoa do Caiado), São forests, semi-natural pastures Jorge (Pico Pinheiro), São Miguel and finally intensively man- (Atalhada, Graminhais, Pico da aged pastures, as suggested Vara), Santa Maria (Pico Alto) by the nestedness analysis and Terceira (Algar do Carvão, (Cardoso et al., 2009b; 2010b). Matela, Pico do Galhardo), The roles of selective extinction while the pristine areas were on (see also Triantis et al., 2010a), Terceira (Terra Brava, Biscoito as is exemplified by a gradi- da Ferraria, Caldeira da Serra de ent of disturbance (Cardoso et Santa Bárbara), Pico (Caveiro, al., 2007), and habitat change Mistério da Prainha) and Flores

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(Morro Alto, Pico da Sé) islands al., 2010). Arthropods represent (Cardoso et al., 2007; Gaspar et 17 species of the 100 most impor- al., 2011). tant Macaronesian taxa (Martín Invasive plant species are the et al., 2010) and 24 of the 100 most important drivers in terms most important in the Azores of ecological and ecosystem (Cardoso et al., 2008). This list change in the Azores (Borges et will be used to determine those al., 2010d) and the spread of spe- new species to be included in cies like Hedychium gardneranum, the revision of the NATURA Hydrangea macrophylla, Rubus 2000 list of Azorean priority spe- ulmifolius, Pittosporum undula- cies for conservation (Paulino tum, arborea (see Silva & Costa, pers. comm.). This will Smith, 2006; Hortal et al., 2010) be an important step towards is of great concern. Areas of the inclusion of arthropods in high conservation value due conservation initiatives for the to the presence of single island Azorean archipelago, includ- endemics, such as Pico Alto on ing several new areas based on Santa Maria and Pico da Vara the occurrence of unique arthro- on São Miguel, are now heav- pod species (e.g. Atalhada in ily disturbed by invasive plants. São Miguel; Pico Alto in Santa Human driven ecosystem distur- Maria; Fontinhas in Terceira) bances have to be minimized and (see Gaspar et al., 2011). special measures by the Azorean Government are already being Future work in the conservation of applied for the control of inva- Azorean biodiversity sive plants in several islands. The study of arthropod ecol- The ongoing projects in Pico da ogy in the Azores has proven to Vara (S. Miguel) to manage areas be a valuable tool for designing of special importance for birds biodiversity conservation plans are good examples of active con- in the archipelago. However, servation in the Azores (e.g. Ceia any hope for a successful man- et al., 2009; Heleno et al., 2009). agement and conservation pro- A list of Azorean threatened gram of endemic fauna and taxa, based on both protec- flora must meet local economic tion priority and management interests. Local people, with di- feasibility, has been drawn up rect interest in the use of land (Cardoso et al., 2008; Martín et for agriculture have a higher

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impact on the sustainability of be used to periodically monitor the Azorean habitats than policy the overall diversity of the areas. makers, managers and conserva- tionists altogether. Several ini- FUTURE RESEARCH AND tiatives, resulting from outcomes CONCLUDING REMARKS of the BALA project, have been undertaken through organized The islands of the Azores have seminars and meetings as well undergone dramatic changes in as brochures and books (Borges land-use and their biodiversity & Gabriel, 2009; Cardoso et al., is now under serious threat (see 2009c) in recent years increasing Borges et al., 2008). With the public understanding of why current knowledge on Azorean value arthropod biodiversity arthropod biodiversity it is now and thus to protect their habi- possible to address more com- tats. The information on arthro- plex issues, such as being able pod diversity and distribution to: provided by the BALA project 1) predict species extinctions and parallel studies is being using the available informa- used by the regional government tion of species abundance to define and give legal status to on Azorean islands (see also the designated areas for protec- Triantis et al., 2010a) and com- tion. The next steps would be to pare data obtained in 1999- establish management plans for 2000 with new data that was the areas, including the estab- collected in 2010 (FCT Project lishment of periodic diversity PTDC/BIA-BEC/100182/2008 monitoring plans for these zones – “Predicting extinctions on to determine the effectiveness of islands: a multi-scale assess- the conservation strategies ad- ment); opted to date. The management 2) evaluate the extent and the and monitoring plans should mechanisms through which include: i) the identification of fragmentation of natural specific threats to the protected habitats affects species com- areas, ii) the definition of practi- munities. To do this, we will cal measures to minimize these build a relevant framework to threats, and iii) the selection evaluate and compare habi- of specific groups of organisms tat size effects on the species and sampling methods that can richness of native versus ex-

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otic free-living herbivore in- should play important function- sects and predatory spiders. al roles in native communities. We anticipate that these re- Time scale, whether it is sults will advance in species– hours, days, months or years, area relationship modelling has seldom been explored in techniques, that are crucial the previous projects, despite for both theoretical and con- the fact it will also influence the servation applications in the way diversity and distribution Azores (see a recent appli- of arthropods is perceived, and cation in Guilhaumon et al., hence, may provide additional 2008); information that is important 3) the study of species-environ- for conservation planning. A ment relationships, as islands study is currently exploring spi- are especially good places to der diversity in a native forest address these questions; fragment at different hours of 4) identify evolutionary signifi- the day (Cardoso, unpublished cant units for conservation by data). Furthermore, a com- generating mitochondrial and parison of data from 2000 with nuclear molecular datasets of those from 2010 (FCT Project several arthropod endemic PTDC/BIA-BEC/100182/2008 species (e.g., FCT - PTDC/ – “Predicting extinctions on is- BIA-BEC/104571/2008 project lands: a multi-scale assessment; – “What can the Macaronesian Triantis et al., 2010a) will also islands teach us about specia- offer valuable insights on the ef- tion? A case study of Tarphius fect of time scale on the diversity beetles and Hipparchia butter- and distribution of arthropods flies”). in the Azores. Further studies, using dif- The patterns and causes of ar- ferent sampling techniques, thropod rarity in Azorean native should be carried out to im- forests should continue to be ex- prove our knowledge of the di- plored in detail to distinguish versity and distribution of less between arthropod species that known groups of arthropods, are truly rare from those that are such as Hymenoptera, Diptera, rare at a given time, as this has Collembola and Acari, these less major implications for the defi- known groups of arthropods nition of the most effective con- are diverse and abundant and servation strategies.

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ACKNOWLEDGEMENTS summarized in this manuscript: “Identification of genetically We are grateful to all of the distinct populations of Azorean researchers that collaborated endemic arthropod species for in the field and laboratory dur- biodiversity conservation in ing BALA and other recent pro- the archipelago” (Ref: Direcção jects: Álvaro Vitorino, Anabela Regional da Ciência e Tecnologia Arraiol, Ana Rodrigues, Artur - DRCT M2.1.2/I/017/2007), Serrano, Carlos Aguiar, Catarina “Consequences of land-use Melo, Francisco Dinis, Genage change on Azorean fauna and André, Emanuel Barcelos, flora - the 2010 Target” (Ref: Fernando Pereira, Hugo Mas, DRCT M.2.1.2/I/003/2008), the João Amaral, João Moniz, EU projects INTERREGIII B Joaquín Hortal, Lara Dinis, Paula “ATLÂNTICO” (2004-2006) and Gonçalves, Sandra Jarroca and BIONATURA (2006-2008). PAVB Luís Vieira. The Forest Services is currently being supported provided local support on each by the FCT project PTDC/BIA- island. Acknowledgments are BEC/100182/2008 – “Predicting due to all of the taxonomists extinctions on islands: a multi- who assisted in the identifi- scale assessment” and FCT pro- cation of the morphotypes: ject PTDC/BIA-BEC/104571/2008 Andrew Polaszek, António Bivar - “ What can the Macaronesian Sousa, Artur Serrano, Arturo islands teach us about specia- Baz, Célia Mateus, Fernando tion? A case study of Tarphius Ilharco, Henrik Enghoff, John beetles and Hipparchia butter- Noyes, Jordi Ribes, José A. flies”. CG is supported by the Quartau, Jörg Wunderlich, Kees DRCT BPD 1.1.2/FRCT with the van Achterberg, Maria dos Anjos project: “Agriculture, habitat Ferreira, Mário Boieiro, Ole fragmentation, indicator species Karsholt, Richard Strassen, and conservation of endemic Volker Manhert and Virgílio fauna and flora in the Azores Vieira. Field work for BALA – the 2010 Target”. AMCS was project was also funded by the supported by the grant SFRH/ Azorean Direcção Regional dos BD/21496/2005. SPR is grant- Recursos Florestais (Proj. 17.01- ed by the Brazilian Council of 080203). More recent projects Science and Technology, CNPq. were also relevant to the results PC is supported by the grant

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FCT- SFRH/BPD/40688/2007. KT Boletim do Museu Municipal do is supported by the grant FCT – Funchal, Sup. 4: 1-785. SFRH/BPD/44306/2008. IRA is BLAS, M., & P.A.V. BORGES, 1999. A supported by a grant from FGF new species of Catops (Coleoptera: (PTDC/BIA-BEC/104571/2008). Leiodidae, Cholevinae) from the Azores with remarks on the Maca- LITERATURE CITED ronesian fauna. Elytron, 13: 173-184. BOERO, F., 2010. The Study of Species AMORIM, I.R., 2005. Colonization in the Era of Biodiversity: A Tale of and diversifi cation on oceanic islands: Stupidity. Diversity, 2: 115-126. forest Tarphius and cave-dwelling BORGES, P.A.V., C. AGUIAR, J. Trechus beetles of the Azores, 282 pp. AMARAL, I.R. AMORIM, G. Ph.D. dissertation. Department of ANDRÉ, A. ARRAIOL, A. BAZ, F. Ecology and Evolutionary Biology, DINIS, H. ENGHOFF, C. GASPAR, University of California, Los F. ILHARCO, V. MAHNERT, Angeles. C. MELO, F. PEREIRA, J.A. AMORIM, I., B. EMERSON, P.A.V. QUARTAU, S. RIBEIRO, J. RIBES, BORGES & R. WAYNE, (subm.). A.R.M. SERRANO, A.B. SOUSA, Phylogeography and molecular R.Z. STRASSEN, L. VIEIRA, phylogeny of Macaronesian island V. VIEIRA, A. VITORINO & J. Tarphius: why so few species in the WUNDERLICH, 2005b. Ranking Azores?. Journal of Biogeography. protected areas in the Azores using ASHMOLE, P., & M. ASHMOLE, 2000. standardized sampling of soil epi- St. Helena and Ascension Island: a gean arthropods. Biodiversity and natural history. Anthony Nelson, Conservation, 14: 2029-2060. Oswestry, England. BORGES, P.A.V., E.B. AZEVEDO, A. BENTON, T.G., & T. SPENCER BORBA, F.O. DINIS, R. GABRIEL (eds.), 1995. The Pitcairn Islands: & E. SILVA, 2010d. Ilhas Oceânicas. Biogeography, Ecology and Prehistory. In: PEREIRA, H.M., T. DOMINGOS Academic Press, London. & L. VICENTE (eds.), Portugal BERRY, R.J., 1992. The signifi cance of Millenium Ecosystem Assessment, pp. island biotas. Biological Journal of the 461-508. Escolar Editora, Lisboa. Linnean Society, 46: 3-12. BORGES, P.A.V., & V.K. BROWN, 1999. BISCOITO, M.C. (ed.), 1995. Eff ect of island geological age on Proceedings of the 1st Symposium the arthropod species richness of of “Fauna & Flora of the Atlantic Azorean pastures. Biological Journal Islands” Funchal - October 1993. of the Linnean Society, 66: 373-410.

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