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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Long-term monitoring across elevational gradients (III): vascular on () transect

DÉBORA S.G. HENRIQUES, R.B. ELIAS, M.C.M. COELHO, R.H. HÉRNANDEZ, F. PEREIRA & R. GABRIEL

Henriques, D.S., R.B. Elias, M.C.M. Coelho, R.H. Hernandéz, F. Pereira & R. Gabriel 2017. Long-term monitoring across elevational gradients (III): vascular plants on Terceira Island (Azores) transect. Arquipelago. Life and Marine Sciences 34: 1-20.

Anthropogenic disturbance often drives habitat loss, ecological fragmentation and a decrease in biodiversity. This is especially problematic in islands, which are bounded and isolated systems. In the Azores, human settlement led to a significant contraction of the archipelago’s original native forested areas, which nowadays occupy only small patches and are additionally threatened by the spread of invasive . Focusing on Terceira Island, this study aimed to assess the composition of vascular communities, and the abundance and distribution patterns of species in permanent 100 m2 plots set up in the best preserved vegetation patches along an elevational gradient (from 40 to 1000 m a.s.l.). Sampling yielded a total of 50 species, of which 41 are indigenous and nine are exotic. The richest and best preserved communities were found between 600 m and 1000 m, corresponding to Juniperus- Ilex montane forest and Calluna-Juniperus altimontane scrubland formations. Nonetheless, exotic species were prevalent between 200 m and 400 m, with clearly dominating the canopy. These results support the high ecological and conservation value of the vegetation formations found in the island’s upper half, while calling attention to the biological invasions and homogenization processes occurring at its lower half. Long-term monitoring in these plots will further reveal direction and rates of change in community composition, allowing for more informed management and conservation strategies in the island.

Key words: disturbances, elevation, subsp. azorica, , azorica, native vegetation, permanent plots, Pittosporum undulatum

Débora Henriques1,2(e-mail: [email protected]), R.B. Elias1,2, M.C. Coelho1,2, R.H. Hernández3, F. Pereira1,2 & R. Gabriel1,2. 1CE3C-Centre for Ecology, Evolution and Environmental Changes/ Azorean Biodiversity Group and Universty of the Azores – Faculty of Agricultural Sciences and Environment, PT-9700-042 Angra do Heroísmo,Portugal. 2Portuguese Platform for Enhancing Ecological Research & Sustainability (PEERS). 3University of La Laguna Department of . Botany, ES-3204 San Cristobal de La Laguna, Santa Cruz deTenerife, , Spain.

INTRODUCTION discrete and isolated entities, they are hotspots for many rare species with restricted distributions Islands tend to be less diverse than mainland (Kier et al. 2009). Focusing on insular floras, areas of similar size (Whittaker & Fernández- islands shelter exclusively about one quarter of all Palacios 2007), but it also seems that, being known plant taxa (Kreft et al. 2008). Nonetheless,

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anthropogenic pressure on these fragile CHARACTERIZATION OF TERCEIRA ISLAND ecosystems is leading to a decrease in the number Located at the coordinates 27º19’ W, 38º71’ N, in of endemics and an increase in the number of the Central Group of the Azores archipelago, introduced and invasive species (Sax et al. 2002). Terceira is the third largest (402 km2) of the nine In the Azores, five centuries of human occupation Azorean islands (Borges et al. 2009). It reaches led to a decrease estimated between 87% 1021 m a.s.l. of maximum elevation in the Santa (Monteiro et al. 2008) and 95% in the area Bárbara Volcanic Complex (Forjaz 2004), the occupied by native vegetation (Triantis et al. youngest of the four stratovolcanos that shape the 2010; Gaspar et al. 2011), seriously threatening island. According to Calvert et al. (2006), two of the continued existence of the remaining vascular these volcanoes have collapsed and are believed species endemic to the archipelago (around 35% to be extinct (Guilherme Moniz and Cinco Picos) of the total native vascular plant richness) (Silva but the other two are still considered active (Pico et al. 2010). Additionally, introduced species Alto and Santa Bárbara). Terceira is thus mostly already comprise around 80% of the formed by trachytes and pyroclastic material archipelago’s vascular flora (Silva et al. 2010), (cinders, ashes, pumices, tuffs) of trachyte with biological invasions and composition ( et al. 2007). thus converging to create a bleak scenario for the Human settlement in Terceira was strongly future of the Azorean vegetation. influenced by the geomorphology of the territory. In this context, this is the third paper on the As a major part of the island’s interior is occupied series “Long-term monitoring across elevational by volcanic cones and stratovolcanos, most gradients”, which aims to identify, characterize communities were forced to establish along the and monitor the vascular plant diversity of some coastal lowlands and river-valleys (Agostinho of the remaining fragments of native flora in 1942), and most of them are still located below several Azorean islands, using elevational 250 m a.s.l. (review in Silveira 2013). Presently, transects with a 200 m step. In order to do so, a Terceira's main economic activity is the rising of standardized methodology, thoroughly explained livestock and the production of dairy-based in the first paper of the series (Gabriel et al. products (INE 2011) and most of the natural 2014), was applied to Terceira Island during the vegetation that originally covered the island’s winter of 2012 and the spring of 2013. lower areas was destroyed in order to create The main purpose of this paper is to identify pastureland, used for rotational crops and grazing and characterize native vegetation patches in dairy cattle (Silveira 2013). Terceira, concerning their composition of The climate in Terceira can be considered mild, flowering plants, ferns and the richness of with high relative humidity values, regular habitats for bryophytes. We also determine a) if rainfall and strong wind regimes (Azevedo et al. the floristic composition of these plots is 2004). According to the observations registered in representative of the island’s indigenous vascular the Meteorological Station of Angra do diversity, b) if the vascular communities in the Heroísmo, the mean temperature values (at 74 transect show signs of elevation zonation, c) if meters a.s.l.) oscillate between 25° C in August and origin correlates with species and 15° C in February. Mean rainfall peaks in distribution patterns and d) how Terceira’s results January, at approximately 130 mm and it’s the compare to Pico’s. This analysis may contribute lowest in July, at circa 30 mm. At higher with information to research and conservation elevations, the model CIELO projects a mean topics of interest, such as the effectiveness of the annual rainfall of more than 2800 mm and native biodiversity protection measures minimum and maximum temperatures of, (associated with Terceira's Natural Park areas) or respectively, less than 6° C and 13 to 14° C for the identification of elevational zonation patterns the Santa Bárbara Mountain. The wind is most associated with differences in environmental likely to come from the SE and NW sectors variables in the island. (Azevedo et al. 2004).

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According to Silva et al. (2010) there are 1109 in Portugal has, understandingly, been the focus vascular plant taxa in the Azores, 61% of which of most elevational vegetation works. occur in Terceira (N = 674). Only about a quarter Nonetheless, Terceira Island has also served as of these species are endemic or native (N = 164; a stage for botanical research in the archipelago. 24%) but they represent almost 78% of the 210 Some works set on the island focus on the indigenous vascular plants known for the Azores. mapping and description of the native or endemic As recently described by Elias et al. (2016), vegetation (Dias 1989; Dias et al. 2004; Melo Terceira island has six natural vegetation belts: 2008), stressing the sensitivity of the region’s -Morella coastal woodlands; - endemic species to anthropogenic disturbances Morella lowland forests; Laurus submontane and the high conservation value of the Santa forests; Juniperus-Ilex montane forests; Juniperus Bárbara Mountain. Approaching the subject from montane woodlands and Calluna-Juniperus a different angle, other studies explore the altimontane scrublands. Taking into account their patterns and consequences of the spread of exotic potential distribution on the island, coastal species in Terceira’s protected areas (Silveira woodlands are more likely to occur in the coastal 2011; Goulart 2014), accentuating the negative areas of the south, east and central north, from the effects of species such as japonica coast up to 100 m a.s.l. Lowland forests are (Japanese red cedar), Hedychium gardnerianum found usually between 100 m and 300 m a.s.l., (Kahili ginger), Hydrangea macrophylla and but sometimes near the coast, and they could Pittosporum undulatum (Incenso ) on the occupy around 38% of the island. The potential island’s native vegetation. area of occupation of Laurus submontane forests is the interior of the island, between 300 and 600 MATERIAL AND METHODS m a.s.l. Lowland and submontane forests comprise the Azorean Laurel forests, the STUDY SITE AND SAMPLING DATES potentially dominant vegetation type in the A transect was set up entirely inside the limits of Azores (Elias et al. 2016). Unfortunately, as in the the Natural Park of Terceira (Regional Legislative other islands, these have declined dramatically in Decree no. 11/2011/A, of April 20) along the Terceira and only a few patches remain. The best western side of the island (Figure 1); the Natural preserved vegetation patches are found in the Park of Terceira aims to contain the best mountainous areas of the central and western preserved native vegetation areas and avoid parts of the island. Here, Juniperus-Ilex montane highly disturbed and modified areas. Thus, the forest is the dominant vegetation, still occupying selected transect encompasses not only one of the relatively large areas in Terra Brava, Pico Alto best preserved areas of the island, but the only and Santa Bárbara natural reserves. Juniperus protected area going continuously from the coast montane woodlands and Calluna-Juniperus to the summit. At each elevation, sites of altimontane scrublands occur in the western part homogeneous vegetation were sought after and of the island, mainly in the Santa Bárbara Natural two plots (10 m x 10 m) were set up inside those reserve, a part of Terceira Island Natural Park areas. The fieldwork was carried out in two (Regional Legislative Decree no. 11/2011/A, of stages. The first took place between the 26th and April 20). With a total extent of 95.78 km2, 28th of September 2012 and served the purpose of distributed among 20 terrestrial and marine areas, setting the 12 permanent plots in six elevations, the Park encompasses 88.35 km2 of the island’s from 40 m (Serreta lighthouse) to 1000 m (Santa landmass, which adds up to about one fifth (22%) Bárbara Mountain) at a 200 m elevational step of its total (Figure 1). (Figure 1), collect bryophytes and perform a preliminary assessment of the vascular species VEGETATION STUDIES IN TERCEIRA ISLAND present in each plot. This dataset was later A review of the history of vegetation zonation complemented with information on the vascular studies in the Azores is featured in the second species cover, during a second phase in May paper of this series (Coelho et al. 2016). Pico 2013. Island, with its mountain standing as the highest 3

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Fig. 1. Terceira Island transect, with the location of the six sampled elevational sites (1 – 40 m; 2 – 200 m; 3 – 400 m; 4 – 600 m; 5 – 800 m; 6 – 1000 m) and the delimitation of Terceira’s Natural Park protected areas.

SAMPLING METHODOLOGY CLIMATE DATA IN THE MOVECLIM TRANSECT The sampling methodology followed the Climate data was derived from the CIELO Model standardized BRYOLAT protocol (Ah-Peng et al. (Azevedo 1996; Azevedo et al. 1999a,b), a 2012, adapted by Gabriel et al. 2014) for the physically based model created to dynamically collection of bryophytes and small ferns along simulate the local climate in islands using environmental gradients, thoroughly described in information from a reference meteorological the first paper of this series (Gabriel et al. 2014). station. The variables we considered for this work Despite focusing on cryptogams, this were total annual precipitation, average annual methodology also includes the characterization of relative humidity and average annual temperature, several aspects of the surrounding vascular flora, derived from estimates for the last 30 years (Table such as presence, cover, height and diameter at 1). breast height of the largest . It was possible to identify the plants in the field and only a few DATA ANALYSIS voucher specimens were taken and deposited in Vascular species richness and cover were AZU (Herbarium of the University of the Azores, determined for each plot. The occurrence of a Angra do Heroísmo). Mid Domain Effect (MDE) (Colwell & Hurtt Nomenclature and taxonomy of the vascular 1994; Colwell & Lees 2000) was also assessed, flora, as well as species origin, follows Silva et al. both for indigenous and total richness of vascular (2010). Regarding the latter, species are divided plants. When the MDE occurs in bounded into five categories: Azores endemic (END), domains (such as islands), species distribution endemic (MAC), native non– ranges overlap more near the middle of the endemic (N) (which, together, are the indigenous elevational gradient, producing a hump-shaped species), naturalized species (NATU) (including richness pattern. exotic and invasive species) and casual species The disturbance index (D) (Cardoso et al. (CAS). 2013) was determined for each plot. This index

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Table 1. Brief characterization of the six sampled sites [12 Plots] in Terceira Island: Geographic data, climatic data [rain (total annual); relative humidity (average annual) and temperature (average annual) (Azevedo 1996; Azevedo et al. 1999a,b)], biological data and disturbance index [minimum 0; maximum 100 (Cardoso et al. 2013)]. Site codes: standard elevation (a.s.l.) and plot number.

takes into account landscape configuration and The list of vascular plant species present in each defines an anthropogenic disturbance gradient plot together with their average percentage cover that varies from 0 (no disturbance at all, may be observed in Table 2. In order to indicating the presence of pristine natural forests) characterize the vegetation communities, a brief to 100 (maximum possible disturbance, indicating description of the six sampled sites is presented in a prevalence of urban/industrial uses) (Table 1). the following section; with the plots illustrated on Figure 2. RESULTS PLOT DESCRIPTION A total of 12 plots were sampled in Terceira Island, set along six elevational sites. Rainfall and relative humidity increase along the gradient, while temperature decreases, as well as the disturbance index (Table 1).

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Fig. 2. Vegetation appearance along the altitudinal gradient set up in Terceira Island: a) 40 m; b) 200 m; c) 400 m; d) 600 m; e) 800 m; f) 1000 m.

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Table 2. List of vascular plant species registered in each of the 12 plots of Terceira Island and their average percentage cover. Species marked with an asterisk (*) occur in four or more elevations. Nomenclature and colonization status (Col.) are according to Silva et al. (2010) (N, native non–endemic species; END, endemic species to Azores; MAC, endemic species to Macaronesia; CAS, casual species; NATU, naturalized species [NATU-1: most noxious invasive species, according to Silva et al. 2008]). (Site codes according to Table 1)

Site codes

Division Class Order Family Species Col. 0040P1 0040P2 0200P1 0200P2 0400P1 0400P2 0600P1 0600P2 0800P1 0800P2 1000P1 1000P2 Lycopodiophyta Selaginellopsida Selaginellales Selaginellaceae Selaginella kraussiana (Kunze) A. Braun N 19 5 1 2 3 Pteridophyta Polypodiopsida Cyatheales Culcitaceae * Culcita macrocarpa C. Presl N 4 2 41 75 14 31 50 15 Hymenophyllales Hymenophyllacea e Hymenophyllum tunbrigense (L.) Sm. N 10 10 26 30 6 1 Hymenophyllum wilsonii Hook. N 44 88 20 32 Polypodiales Aspleniaceae Asplenium onopteris L. N <1 Blechnaceae *Blechnum spicant (L.) Sm. N <1 1 5 5 5 2 16 23 Dennstaedtiaceae *Pteridium aquilinum (L.) Kuhn N 1 <1 14 11 22 22 1 1 Dryopteridaceae Dryopteris aemula (Aiton) O. Kuntze N 1 5 1 6 1 7

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Site codes

Division Class Order Family Species Col. 0040P1 0040P2 0200P1 0200P2 0400P1 0400P2 0600P1 0600P2 0800P1 0800P2 1000P1 1000P2 *Dryopteris azorica (Christ) Alston END 1 <1 7 5 12 12 3 9 1 Elaphoglossum semicylindricum (Bowdich) Benl MAC 3 2 2 1 Polypodiaceae Polypodium azoricum (Vasc) R. Fern. END 2 <1 Pinophyta Pinopsida Pinales

Cupressaceae Cryptomeria japonica (L. fil.) D. Don NATU <1 2 *Juniperus brevifolia (Seub.) Antoine END 3 19 29 23 57 88 57 88 81 Magnoliophyta Liliopsida Asparagales

Orchidaceae Platanthera pollostantha R.M.Bateman & M.Moura END <1 <1 Poales

Cyperaceae Carex echinata Murray N <1 Carex hochstetteriana Gay ex Seub. END <1 Carex pilulifera L. subsp. azorica (Gay) Franco & Rocha Afonso END 1 3 Carex sp. 9

Eleocharis multicaulis (Sm.) Desv. N 1 6 Juncaceae Luzula purpureosplendens Seub. END 3 2 9 15 24 15 Agrostis sp. 1

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Site codes

Division Class Order Family Species Col. 0040P1 0040P2 0200P1 0200P2 0400P1 0400P2 0600P1 0600P2 0800P1 0800P2 1000P1 1000P2 Deschampsia foliosa Hack. END 3 7 22 petraea Guthn. ex Seub. END <1 Holcus rigidus Hochst. END 2 3 Hordeum murinum L. subsp. leporinum (Link) Asch. & Graebn. NATU <1 Zingiberales

Zingiberaceae Hedychium gardnerianum Sheppard ex Ker-Gawl. NATU-1 1 3 6 12 2 <1 Magnoliopsida Apiales

Araliaceae azorica Carrière END <1 3 Pittosporaceae Pittosporum undulatum Vent. NATU-1 4 60 67 72 63

Aquifoliaceae * Ilex perado Aiton subsp. azorica (Loes.) Tutin END 9 4 44 22 8 29 Boraginales

Boraginaceae Myosotis maritima Hochst. ex Seub. END 1

Caryophyllaceae maritima G. Don fil. N <1 Dipsacales

Adoxaceae treleasei Gand. END <1 2

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Site codes

Division Class Order Family Species Col. 0040P1 0040P2 0200P1 0200P2 0400P1 0400P2 0600P1 0600P2 0800P1 0800P2 1000P1 1000P2

Ericaceae Calluna vulgaris (L.) Hull N 1 9 19 14 17 * Hochst. ex Seub. END 54 84 34 24 30 34 14 <1 *Vaccinium cylindraceum Sm. END 11 6 13 22 8 16 5 3 Myrsinaceae *Myrsine africana L. N 30 14 18 21 7 36 5 <1 Primulaceae Lysimachia azorica Hornem. ex Hook. END 11 10 3 1 2 4 Fagales

Myricaceae Morella faya (Aiton) Wilbur N 14 24 14 24 19 22

Gentianaceae scilloides (L. fil.) Samp. N <1 Lamiales

Oleaceae (Tutin) Knobl. END 14 23 Plantago lanceolata L. NATU <1 Scrophulariaceae Sibthorpia europaea L. N 1

Lauraceae * (Seub.) Franco END 16 <1 9 41 27 8 14 Persea indica (L.) C. K. Sprengel NATU <1 Malpighiales

Hypericaceae foliosum Aiton END <1 Myrtales

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Site codes

Division Class Order Family Species Col. 0040P1 0040P2 0200P1 0200P2 0400P1 0400P2 0600P1 0600P2 0800P1 0800P2 1000P1 1000P2 Myrtaceae *Metrosideros excelsa Sol. ex P. Gaertn. NATU <1 16 11 3 5 2 19 9 19 Psidium littorale Raddi CAS <1 <1 Rosales

Rhamnaceae azorica V. Grubov END 1 <1 Rosaceae Potentilla anglica Laich. N 1 1 1 Rubus ulmifolius Schott NATU <1 Saxifragales

Crassulaceae horizontalis (Guss.) DC. N <1 <1 Umbilicus rupestris (Salisb.) Dandy N <1 9 1

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Site 1 (~40 m) − Serreta lighthouse − Both plots perado subsp. azorica (33%) and V. cylindraceum consist of coastal vegetation including (18%). Ilex specimens reach up to 8 m high in the monostratified and poor floristic communities, emergent canopy layer. The most abundant composed almost entirely of Erica azorica species in both plots’ understory layers are M. (around 69% mean cover) (Table 2) and, in a africana, Lysimachia azorica and the smaller percentage, Morella faya (ca. 19%). A pteridophytes Culcita macrocarpa, P. aquilinum few other species, namely Festuca petraea, and Hymenophyllum tunbrigense. Plot 1 shows a Hordeum murinum, Pittosporum undulatum, higher taxonomic diversity in the understory, with Myosotis maritima, Sagina maritima, the presence of five species absent from plot 2. Metrosideros excelsa, Plantago lanceolata and The only species present in plot 2 and absent Umbilicus horizontalis are also present, despite from plot 1 is E. azorica, with 14% total cover. covering a minimal percentage of the plots Site 5 (~800 m) – Lagoa do Pinheiro trail – In (around 1%). The vegetation has a relatively low both plots, J. brevifolia dominates the landscape stature and the maximum canopy height (73% cover) accompanied by I. perado subsp. registered in the plots is 3 m, corresponding to azorica, V. cylindraceum and L. azorica, several E. azorica specimens. completing the canopy line with a maximum Site 2 (~200 m) − Canada das Covas, Serreta – height of 4 m. Below the tree line, the main These communities are dominated by the exotic species present are M. africana, L. P. undulatum (64% mean cover), accompanied by purpureosplendens and the ferns Hymenophyllum E. azorica, M. faya and Picconia azorica. Other wilsonii, H. tunbrigense and C. macrocarpa. Plot tree species such as Metrosideros excelsa, Laurus 1 proved to be more diverse than Plot 2, with azorica and Ilex perado subsp. azorica are also three more species, including the Azorean present in the uppermost vegetation layer. The endemic orchid Platanthera pollostantha understory scrub vegetation is quite sparse (Bateman et al. 2013). (around 8%) but also dominated by an exotic Site 6 (~1000 m) – Santa Bárbara Mountain – species, Hedychium gardnerianum, with 2% Vegetation is composed almost exclusively by mean cover. Nevertheless, the ferns Asplenium dwarfed, semi-prostrate J. brevifolia specimens onopteris, Pteridium aquilinum, Dryopteris (occupying around 85% of the plots), growing in azorica and Polypodium azoricum are also dense patches with a maximum height of 1.6 m. present, each one covering about 1% of the plots. Also present in the scrub patches are C. vulgaris, Plot 2 included a specimen of Juniperus V. cylindraceum and M. africana. The herbaceous brevifolia, a new record for the island at this layer is mainly composed by L. elevation. Maximum canopy height was 5.6 m. purpureosplendens, Deschampsia foliosa and the Site 3 (~400 m) – Carneiro Peak – As in the pteridophytes C. macrocarpa, H. wilsonii and previous site (site 2, Canada das Covas, Serreta), Blechnum spicant. Plot 2 proved to be more both plots at this elevation show clear signs of diverse than plot 1, containing five more species, disturbance, with an even higher percentage of P. with emphasis for the presence of P. micrantha. undulatum (68%) dominating the canopy, along This was the only site in our transect where no with smaller percentages of the indigenous E. exotic species were found, being entirely azorica, J. brevifolia, Morella faya, composed by indigenous taxa. cylindraceum and the exotic Metrosideros excelsa (8%). In the understory, the plots are covered by PATTERNS OF RICHNESS AND DISTRIBUTION OF Myrsine africana, Calluna vulgaris, H. VASCULAR PLANTS gardnerianum and the pteridophytes P. aquilinum The six elevational sites surveyed resulted in a list and D. azorica. In Plot 1 we also registered the of 52 taxa — 2 identified only to the level presence of Selaginella kraussiana (19%). The — representing around 8% of all vascular taxa canopies reached 6.6 m. reported for the island. From the 50 species Site 4 (~600 m) – Lagoinha Peak – These identified, 41 were indigenous species (21 END, floristically diverse communities are dominated 1 MAC and 19 N) and nine were exotic. by J. brevifolia (40%), L. azorica (34%), Ilex There are 11 species present in four or more

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elevations along the gradient (Table 2, species Selaginellopsida is represented by only one marked with an asterisk), showing a broader species (S. kraussiana), present between 400 m distribution range than the remaining taxa and and 800 m. In the Division Pteridophyta (the accounting for c. one fifth of the total vascular ferns), the Class Polypodiopsida is present in all richness along the transect. Six of these 11 levels except in the lowest (40 m). The highest species are Azorean endemics (the trees J. number of species is attained at 600 m and 800 m, brevifolia, I. perado subsp. azorica, E. azorica, L. with seven and eight species present, respectively. azorica, V. cylindraceum and the fern D. azorica,) The Division Pinophyta (the ) and its and four are native to the archipelago (the ferns B. Class Pinopsida have two representatives in this spicant, C. macrocarpa, and P. aquilinum, as well transect (J. brevifolia and C. japonica). The first as the M. africana) (Silva et al. 2010). one is present from 200 m until the summit of Concurrently, there are ten species occurring Santa Bárbara mountain and the second one was solely in the gradient’s last 200 m, all of which only identified at 400 m but is not indigenous are indigenous, five being endemic. One is the (Table 2; Figure 3). Polypodiopsida H. wilsonii and the remaining are As expected, since we selected a priori only all herbaceous Liliopsida, (Platanthera native vegetation patches, there is a higher micrantha, Carex echinata, C. pilulifera subsp. diversity of indigenous (END, MAC and N), azorica, Eleocharis multicaulis, Deschampsia rather than exotic (NATU, CAS) species all foliosa, Holcus rigidus, Centaurium scilloides, throughout the transect. In our plots, exotic europaea and Potentilla anglica). On species richness reaches its maximum at 200 m, the opposite extreme, there are 13 species being almost negligible (less than 1%) in the restricted to the first 200 m, five of which are remaining elevations and completely absent at exotics. However, notwithstanding these clear 1000 m. Indigenous species are present at every signs of disturbance, this lower elevational strip elevation, although their maximum relative exclusively features the endemic “Pau-branco” richness peak occurs at the highest end of the (Picconia azorica), a regionally common but gradient, between 600 m and 1000 m, where endangered species due to clear-cuts and grazing greater number of endemics (both from the cattle (Schäfer 2005). Azores and Macaronesia) were found (Table 1; The most diverse plant group along the transect Figure 4). corresponds to the Division Magnoliophyta (the Indigenous species richness is lowest between flowering plants or Angiosperms), represented by 200 m and 400 m, increasing and reaching a two Classes: Liliopsida and Magnoliopsida, both plateau in the highest three sites. This pattern present in all sites. Liliopsida’s highest diversity does not conform to the existence of a Mid- is attained at 1000 m (N = 8). Magnoliopsida is Domain Effect (MDE) (Figure 5), with the the main component of the vascular flora, being richness peak occurring above the middle of the more diverse than any other Class in all levels. gradient and the number of species in the 200 m Maximum diversity is attained at 200 m, with 13 and 400 m sites being quite lower than a fit to the species present (Figure 3). model would require. Similar results were In the Division Lycopodiophyta (the oldest obtained for all the species taken together, extant vascular plant division, at around 410 including exotics (not shown). million years old) (Schooley 1997), the Class

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Fig. 3. Number of vascular plants per class at each studied standard elevation.

Fig. 4. Proportion of species: indigenous (END, endemic species to Azores; MAC, endemic species to Macaronesia; N, native species); exotic (NATU, naturalized species; CAS, casual species) along the Terceira transect.

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Fig. 5. Mid Domain Effect (MDE) test for the distribution of indigenous species on the Terceira Island transect. The dotted black line represents the observed species richness and the grey lines delimit the 95% confidence interval.

DISCUSSION plot 1 probably corresponds to a coastal scrubland (like the ones described by Dias, 1996) typical of The main objective of this paper was to describe the transition zone between the terrestrial and some areas of native vegetation in Terceira with marine ecosystems (Elias et al. 2016). Plot 2 has a respect to their vascular flora, ascertaining the higher canopy height and Morella faya becomes current richness and distribution patterns of these more abundant, so this community is more similar taxa along the island’s elevational gradient. Since to the typical Erica-Morella woodlands. Only ten environmental trends in elevation are usually vascular plant species were found among those reflected in changes in the structure, composition Erica bushes, (the lowest richness value along the and diversity of the vegetation, it would be gradient), and they also represent one of the expected to find distinct zones along the transect lowest heights of the vegetation, possibly as a as a response to the increasing elevation. result of their exposure to the sea winds (cf. Dias Accordingly, these vascular plants show clear et al., 2005). More than a third of the species signs of elevational zonation, with a natural identified at this elevation are exotic (H. layering of various vegetation types occurring at murinum, P. undulatum, P. lanceolata and M. different elevations due to vertical differences in excelsa), but are present in fairly low abundances, environmental conditions (particularly suggesting this is a somewhat well preserved temperature and precipitation). patch of coastal indigenous vegetation. The sampled coastal vegetation of Serreta At 200 m the vegetation resembles that of lighthouse (station 1, 40 m a.s.l.) belongs to the highly degraded Picconia-Morella Lowland Erica-Morella Coastal Woodland vegetation belt, Forest (Elias et al. 2016) dominated by the exotic as proposed by Elias et al. (2016). Nevertheless, P. undulatum. In fact, besides the presence of M.

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faya, this is the only site where Picconia azorica Juniperus-Ilex Montane Forest belt (Elias et al. is present in our transect. The species M. faya, P. 2016) but seems to be an azonal community azorica, E. azorica and L. azorica are equally (probably determined by the presence of thick abundant in the landscape, with approximately pumice downfall deposits in the geological 20% cover each. At 400 m, we find trees of E. substrate and exposure to the westerlies) clearly azorica and M. faya and of M. africana dominated by J. brevifolia. This kind of formation and C. vulgaris each occupying around a fifth of is confined to areas of extreme wetness and the area of each plot. This site is in the Laurus strong winds, typically occurring on mountainous submontane forest belt, but nowadays Laurel areas, where J. brevifolia forms a continuous forests are very rare in their pristine state (Dias layer (Dias et al. 2005). The epiphytic flora is 1996, Elias et al. 2016), due not only to the well developed and bryophytes were found to invasion of introduced species (as demonstrated completely envelop most branches. in our plots by P. undulatum, M. excelsa and H. Finally, in Santa Bárbara mountain, at 1000 m, gardnerianum) but also by the conversion of we find Calluna-Juniperus montane scrublands forest to pastureland. (sensu Dias, 1996) that belong to the Calluna- At 600 m, in Lagoinha Peak, we find what Juniperus altimontane scrubland belt (Elias et al. seems to be a transition area between the Laurus 2016) with J. brevifolia and C. vulgaris submontane forest and Juniperus-Ilex montane dominating a superbly well-preserved landscape, forest belts. In fact, according to Elias et al. with no exotic species. This kind of formation (2016), this is usually the altitudinal limit appears on mountain ridges with high amounts of between submontane and montane forests. Both rainfall and strong winds, that force the kinds of vegetation co-occur in areas of high vegetation to be dwarfed and semi-prostrate (Dias atmospheric humidity and rainfall with a high et al. 2005). degree of soil saturation. In the Laurus forests This transect, which was intended specifically this saturation is sporadic (although moisture to cover the best preserved areas of indigenous content in the soil is permanent), while in the vegetation in the island for each of the six Juniperus-Ilex forests the forest floor is often sampled elevations, managed to encompass 22 formed by Sphagnum moss carpets, which is endemics (21 species endemic to the Azores and more or less constantly saturated (Dias et al. one to Macaronesia) and 19 non-endemic natives, 2005; Gabriel & Bates 2005). Juniperus-Ilex bringing the indigenous richness of vascular Montane Forests are confined to areas of high plants along the transect to a total of 41 species. cloud cover and extremely high humidity, which Given that the indigenous vascular flora of in most islands can be found above 500 m, whilst Terceira adds up to a total of 164 taxa, 58 of Laurus Submontane Forests predominate which (35%) are endemic to the Azores and seven immediately below the permanent clouds (Silva to Macaronesia (Silva et al. 2010), we managed to 2007). The vegetation, despite showing signs of sample 25% of the island’s indigenous vascular transition, can be classified as a Juniperus-Ilex flora in an area corresponding to less than 1% of formation at its lowest elevational limit. It is the island’s total surface. Furthermore, only nine represented by I. perado subsp. azorica trees exotic species were found, two of them with emerging up to 8 m high above a canopy invasive behaviour (Hedychium gardnerianum dominated by J. brevifolia and V. cylindraceum. and Pittosporum undulatum), both classified as The herbaceous ground layer is largely dominated problematic invasive species in Macaronesia by pteridophytes and, as with all cloud forests, the (Silva et al. 2008). epiphytic flora is well developed. Laurus Overall, vascular plant richness increases with Submontane Forest vegetation is sparsely elevation up to 600 m and then reaches a plateau represented by L. azorica in the canopy and H. in the last three sites (Figure 3). This constant azorica, D. azorica and D. aemula in the pattern at high elevations is quite rare in the undergrowth. literature. To our knowledge, it was only reported At 800 m, alongside the trail to Lagoa do once, for terrestrial ferns in the last 1600 m of a Pinheiro, the vegetation is now fully inside the 2600 m elevational gradient in Costa Rica

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(Watkins Jr. et al. 2006), showing no significant elevational gradient is half the length of Pico’s, correlation to any of the explanatory variables this difference might be partly due to the fact that examined. In our study, which is based on very Pico’s gradient manages to cover a broader set of few non-randomly selected plots, it might be an vegetation types and thus potentially capture artefact of the sampling methodology and more diversity. For example, sub-alpine and disappear with denser sampling. alpine scrublands, found in Pico Mountain above As expected, the flowering plants, the largest 1200 m included two indigenous species and most diverse group within the kingdom (Daboecia azorica and Thymus caespititius) that plantae (Mauseth 2014) were predominant all were absent from lower elevations. Nonetheless, throughout the transect, being present at all both transects capture only a small part of the elevations. Class Magnoliopsida constitutes the whole indigenous flora (a quarter to a third), majority of the overstory vegetation along the which begs for caution against the generalization gradient and presents its richness maximum at of the resulting patterns. To complement our 200 m (Figure 3). This coincides with the findings, we suggest the future establishment of presence of exotic species found in our plots more than one permanent transect per island, exclusively at this elevation (Psidium littorale, which would result in a more comprehensive Rubus ulmifolius and indica) on highly native vegetation sample. disturbed vegetation patches, due to the high Also, contrary to Pico’s clear richness degree of human intervention on the landscape. maximum at 600 m, Terceira’s transect yields a Liliopsida, mostly herbs and grasses, constitute, richness plateau between 600 m and 1000 m. along with the ferns (Polypodiopsida), most of the Despite some composition similarities between understory vegetation of the plots. the two islands at 600 m (co-dominance of L. Polypodiopsida are more numerous between azorica and I. perado subsp. azorica, both falling 600-800 m in the transect, where the high and in the Juniperus-Ilex montane forests category), closed canopies provide their ideal shade and Pico’s 600 m site has a lower disturbance index moisture conditions. The same is true for S. than Terceira’s (15% against 25%), appearing to kraussiana (Lycopodiophyta), also common to be better preserved. Furthermore, comparing both wet and shady places, except coastal regions islands, the considerably higher cover of J. (Schäfer 2005) and present in our transect brevifolia at this elevation in Terceira further between 400-800 m. supports our assessment that the 600 m site in As for variation in species richness patterns Terceira is in a transition area between Laurus according to their origin, it is worth noticing that Submontane Forest and the Juniperus-Ilex more than half (N = 6) of the wider ranged Montane Forest found at 800 m, which could species along the gradient are Azorean endemics explain the less abrupt decline in richness (Table 2, species marked with an asterisk). between 600 m and 800 m when compared with According to Schäfer (2005), many Azorean Pico’s. endemics are characterized by a wide ecological These results support the fact that terceira’s and elevational range and in our transect, all of mid-high elevation vegetation patches (from 600 these show elevational ranges equal to or broader m to 1000 m), much like pico’s (coelho et al. than 600 m, testifying in favour of Schäfer’s 2016), are important reservoirs of endemic hypothesis. Nevertheless, their presence is by no vascular species richness and are still relatively means abundant within the island, mostly due to well preserved. From the coast up to 400 m we the competition with invasive species like the find very few remnants of native vegetation due Himalayan H. gardnerianum and the Australian P. to habitat destruction (caused by human undulatum. disturbance and forest conversion to pasturelands) In comparison with the transect and the ones that prevail are being severely (Coelho et al. 2016) the Terceira transect modified by the invasion of exotic species. captured a lower percentage of the island’s Considering that all our plots fall within the indigenous vascular plant diversity (35% for Pico, boundaries of Terceira island Natural Park, it is 25% for Terceira). Bearing in mind that Terceira’s important to keep monitoring vegetation 17

Vascular plants on Terceira Island transect

composition in these areas and take current and Management 40: 393–403. future trends into account when evaluating and Azevedo, E.B., M.C. Rodrigues & J.F. Fernandes 2004. redefining management and conservation Climatologia. Pp. 25–48 in: Forjaz, V. H. (Eds). strategies. Atlas Básico dos Açores. Observatório Vulcanológico e Geotérmico dos Açores.[in Portuguese]. ACKNOWLEDGEMENTS Bateman, R.M., P.J. Ruddall & M. Moura 2013. Systematic revision of Platanthera in the The authors would like to acknowledge the Azorean archipelago: Not one but three species, financial support granted by the research project including arguably ’s rarest MOVECLIM (M2.1.2/F/04/2011/NET) and also orchid. PeerJ 1:e218. by projects ISLANDBIODIV (NETBIOME/ 0003/ Borges, P.A.V., E.B. Azevedo, A. Borba, F.O. Dinis, R. Gabriel & E. Silva. 2009. Ilhas Oceânicas. Pp. 2011), IMPACTBIO (DRCT–M2.1.2/I/005/2011) 463–510 in Pereira, H.M., T. Domingos & L. and ATLANTISMAR (DRCT-M2.1.2/I/027/2011). Vicente (Eds) Ecossistemas e bem-estar humano - Besides, DSGH and MCMC were funded by ph.d. Avaliação para Portugal do Millenium Ecosystem Grants M3.1.2/F/051/2011 and M3.1.2/F/051/2011, Assessment. Escolar Editora, Lisboa. 736 pp. from the “Fundo Regional para a Ciência e [Oceanic Islands; in Portuguese]. Tecnologia”, Regional Government of the Azores Calvert, A.T., R.B. Moore, J.P. McGeehin & A.M. and PROEMPREGO. The team is grateful to the Rodrigues da Silva 2006. Volcanic history and Director of the Natural Park of Terceira Island, 40Ar/39Ar and 14C geochronology of Terceira Eng. Sónia Alves, and to the Director of the Island, Azores, Portugal. Journal of Volcanology and Geothermal Research 156: 103–115. research group CITA–A — “Centro de Cardoso, P., F. Rigal, S. Fattorini, S. Terzopoulou & Investigação e Tecnologias Agrárias – Açores”, P.A.V. Borges 2013. Integrating Landscape Doutor João Madruga, for logistic assistance. The Disturbance and Indicator Species in Conservation authors wish to thank Pedro Cardoso for Studies. PLoS ONE 8: 1–10. estimating disturbance data for each site. Coelho, M.C., R.B. Elias, J. Kluge, F. Pereira, D.S.G. Henriques, S.C. Aranda, P.A.V. Borges, et al. REFERENCES 2016. Vascular plants on Pico Island transect. Long-term monitoring across elevational gradients (II): vascular plants on Pico Island (Azores) Agostinho, J. 1942. Clima dos Açores. Açoreana 3: transect. Arquipelago. Life and Marine Sciences 35–65. [Azorean climate; in Portuguese] 33: 21–44. Ah-Peng, C., N. Wilding, J. Kluge, B. Descamps- Colwell, R.K. & G.C. Hurtt 1994. Nonbiological Julien, J. Bardat, M. Chuah-Petiot, D. Strasberg, et Gradients in Species Richness and a Spurious al. 2012. Bryophyte diversity and range size Rapoport Effect. The American Naturalist 144: distribution along two altitudinal gradients: 570–595. Continent vs. island. Acta Oecologica 42: 58–65. Colwell, R.K. & D.C. Lees 2000. The mid-domain Azevedo, E.B. 1996. Modelação do clima insular à effect: geometric constraints on the geography of escala local. Modelo CIELO aplicado à ilha species richness. Trends in Ecology & Evolution Terceira. PhD Thesis, Universidade dos Açores. 15: 70–76. 247 pp. [Insular climate modeling at the local scale. Dias, E. 1989. Flora e vegetação endémica na ilha CIELO model applied to Terceira Island; in Terceira, Açores. MSc Dissertation. University of Portuguese] the Azores. 71 pp. [Flora and endemic vegetation Azevedo, E.B., L.S. Pereira & B. Itier 1999a. of Terceira Island, Azores; in Portuguese] Simulation of local climate in islands environments Dias, E. 1996. Vegetação natural dos Açores. Ecologia using a GIS integrated model. In: Musy A., L.S. e sintaxonomia das florestas naturais. PhD Thesis, Pereira & M. Fritsch (Eds). Emerging Technologies University of Azores. 302 pp. [Natural vegetation for Sustainable land Use and Water Management of the Azores; in Portuguese] 2nd Inter–Regional Conference Environment- Dias, E., R.B. Elias & V. Nunes 2004. Vegetation Water, Lausanne Switzerland. CD–ROM Paper 7.4. mapping and nature conservation: a case study in Azevedo, E.B., L.S. Pereira & B. Itier 1999b. Terceira Island (Azores). Biodiversity and Modelling the local climate in island environments: Conservation 13: 1519–1539. water balance applications. Agricultural Water Dias, E., C. Mendes, C. Melo, D. Pereira & R.B. Elias

18

Henriques et al.

2005. Azores Central Islands vegetation and flora Mauseth, J.D. 2014. Botany: An Introduction to Plant field guide. Quercetea 7: 123–173. Biology. Jones & Bartlett Learning, Burlington, Elias, R.B, A. Gil, L. Silva, J.M. Fernández-Palacios, MA. 696 pp. E.B. Azevedo & F. Reis 2016. Natural zonal Melo, C. 2008. Critérios de Avaliação da Integridade vegetation of the Azores Islands: characterization Ecológica das Áreas da Rede Natura 2000. Caso and potential distribution. Phytocoenologia Estudo da Serra de Santa Bárbara. MSc 46(2): 107-123. Dissertation. University of the Azores.137 pp. Forjaz, V.H. 2004. Atlas Básico dos Açores. [Evaluation criteria for the ecological integrity of Observatório Vulcanológico e Geotérmico dos Natura 2000 areas. Case study of Santa Bárbara Açores. Ponta Delgada. 112 pp. [Basic Atlas of the Mountain; in Portuguese]. Azores; in Portuguese] Monteiro, R., S. Furtado, M. Rocha, M. Freitas, R. Gabriel, R. & J.W. Bates 2005. Bryophyte community Medeiros, J.V. Cruz. 2008. O Ordenamento do composition and habitat specificity in the natural Território nos Açores: Política e Instrumentos. forests of Terceira, Azores. Plant Ecology 177: Secretaria Regional do Ambiente e do Mar, 125–144. Direcção Regional do Ordenamento do Território e Gabriel, R., M.C. Coelho, D.S.G. Henriques, P.A.V. dos Recursos Hídricos. Ponta Delgada. 159 pp. Borges, R.B. Elias, J. Kluge & C. Ah-Peng 2014. [Territorial planning in the Azores: policies and Long-term monitoring across elevational gradients instruments; in Portuguese] to assess ecological hypothesis: a description of Mooney, H.A. & E.E. Cleland 2001. The evolutionary standardized sampling methods in oceanic islands impact of invasive species. Proceedings of the and first results. Arquipelago. Life and Marine National Academy of Sciences of the United States Sciences 31: 45–67. of America 98: 5446–51. Gaspar, C., K.J. Gaston, P.A.V. Borges & P. Cardoso Regional Legislative Decree no. 11/2011/A, of April 2011. Selection of priority areas for arthropod 20. Creation of the Natural Park of Terceira Island conservation in the Azores archipelago. Journal of [Cria o Parque Natural da Terceira]. Diário da Insect Conservation 15: 671–684. República, 1ª série, 78: 2355-2373. Goulart, H.F.S. 2014. Plantas vasculares invasoras no Sax, D.F., S.D. Gaines & J.H. Brown 2002. Species Parque Natural da Ilha Terceira: caracterização e invasions exceed extinctions on islands worldwide: monitorização do controlo de Pittosporum a comparative study of plants and . The undulatum. MSc Dissertation. University of the American Naturalist 160: 766–783. Azores. 98 pp. [Invasive vascular plants in Terceira Schäfer, H. 2005. Endemic vascular plants of the Island Natural Park: characterization and Azores: an updated list. Hoppea 66: 275–283. monitoring of Pittosporum undulatum; in Schooley, J. 1997. Introduction to Botany. Delmar Portuguese] Publishers, New York. 406 pp. INE 2011. Recenseamento agrícola 2009 - Análise dos Silva, J. 2007. Árvores e Florestas de Portugal – principais resultados. Instituto Nacional de Açores e Madeira, a Floresta das Ilhas. Público, Estatística, I.P. Lisboa. 185 pp. [Agricultural Comunicação Social, SA e Fundação Luso- census 2009 - Analysis of main results; in Americana para o Desenvolvimento. Lisboa. 335 Portuguese] pp. [Trees and forests of Portugal - Azores and Kier, G., H. Kreft, T.M. Lee, W. Jetz, P.L. Ibisch, C. Madeira, the forest of the islands; in Portuguese]. Nowicki, J. Mutke, et al. 2009. A global Silva, L., M. Moura, H. Schäfer, F. Rumsey, E.F. Dias assessment of endemism and species richness 2010. List of Vascular Plants (Tracheobionta). Pp. across island and mainland regions. Proceedings of 117–146 in: Borges, P.A.V., A. Costa, R. Cunha, the National Academy of Sciences of the United R. Gabriel, V. Gonçalves, A. F. Martins, I. Melo, et States of America 106: 9322–9327. al. A List of the Terrestrial and Marine Biota from Kreft, H., W. Jetz, J. Mutke, G. Kier, & W. Barthlott the Azores. Princípia, Cascais. 432 pp. 2008. Global diversity of island floras from a Silva, L., E. Ojeda Land & J.L. Rodríguez–Luengo macroecological perspective. Ecology Letters 11: (Eds) 2008. Invasive Terrestrial Flora & Fauna of 116–27. Macaronesia. TOP 100 in Azores, Madeira and Madeira, M., J. Pinheiro, J. Madruga & F. Monteiro Canaries. ARENA, Ponta Delgada. 546 pp. 2007. Soils of volcanic systems in Portugal. Pp. Silveira, L.M.A. 2013. Aprender com a História: 69–81 in: Ó. Arnalds., H. Óskarsson, F. Bartoli, P. Modos de Interacção com a Natureza na Ilha Buurman, G. Stoops & E. García-Rodeja (Eds). Terceira (Do Povoamento ao século XX). Principia, Soils of Volcanic Regions in Europe. Springer, Cascais. 357 pp. [Learning from history: Ways of Berlin. 644 pp. interacting with nature on Terceira Island (from

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Vascular plants on Terceira Island transect

settlement to the 20th century); in Portuguese] Watkins Jr., J.E., C. Cardelús, R.K. Colwell & R.C. Silveira, S.A.F 2011. Impacte de Pittosporum Moran 2006. Richness and distribution of ferns undulatum na vegetação natural dos Açores: o along an elevational gradient in Costa Rica. estudo de um caso na Ilha Terceira. MSc American Journal of Botany 93: 73–83. Dissertation. University of the Azores. 57 pp. Whittaker, R.J., & J.M. Fernández-Palacios 2007. [Impact of Pittosporum undulatum in the Azorean Island Biogeography: Ecology, Evolution, and native vegetation: the case study of Terceira Island; Conservation. Oxford University Press, Oxford. in Portuguese]. 416 pp. Triantis, K.A., P.A.V. Borges, R.J. Ladle, J. Hortal, P. Received 04 Oct 2016. Accepted 21 Nov 2016. Cardoso, C. Gaspar, F. Dinis, et al. 2010. Published online 28 Apr 2017. Extinction debt on oceanic Islands. Ecography 33: 285–294.

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