Lobophora (Dictyotales) Species Richness, Ecology and Biogeography Across the North-Eastern Atlantic Archipelagos and Description of Two New Species1
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J. Phycol. 56, 346–357 (2020) © 2019 Phycological Society of America DOI: 10.1111/jpy.12956 LOBOPHORA (DICTYOTALES) SPECIES RICHNESS, ECOLOGY AND BIOGEOGRAPHY ACROSS THE NORTH-EASTERN ATLANTIC ARCHIPELAGOS AND DESCRIPTION OF TWO NEW SPECIES1 Christophe Vieira2 Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281 (S8), Ghent B-9000, Belgium Filipe Henriques Centro de Ciencias^ do Mar (CCMAR), Universidade do Algarve, Gambelas, 8005-139 Faro, Portugal MARE-Marine and Environmental Sciences Centre, Quinta do Lorde Marina, Sıtio da Piedade, 9200-044 Canicßal, Madeira Island, Portugal Sofie D’hondt Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281 (S8), Ghent B-9000, Belgium Ana I. Neto GBA-cE3c, Azorean Biodiversity Group-Centre for Ecology, Evolution & Environmental Changes, Faculdade de Ciencias^ e Tecnologia, Departamento de Biologia, Universidade dos Acßores, Rua da M~ae de Deus, 9500-321 Ponta Delgada, S~ao Miguel, Acßores, Portugal Carmen H. Almada Faculdade de Ciencias^ e Tecnologia, Universidade de Cabo Verde, Campus do Palmarejo, CP – 279, Praia, Santiago - Cabo Verde Manfred Kaufmann Marine Biology Station of Funchal, Faculty of Life Sciences, University of Madeira, 9000-107 Funchal, Madeira, Portugal Interdisciplinary Center of Marine and Environmental Research-CIMAR/CIIMAR, University of Porto, Novo Edificio do Terminal de Cruzeiros do Porto de Leixoes,~ Avenida General Norton de Matos, 4450-208 Matosinhos, Portugal Marta Sanson, Carlos Sangil Departamento de Botanica, Ecologıa y Fisiologıa Vegetal, Universidad de La Laguna, Canary Islands, Spain and Olivier De Clerck Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281 (S8), Ghent B-9000, Belgium The brown alga Lobophora (Dictyotales, (L. caboverdeana sp. nov., L. canariensis, L. dagamae Phaeophyceae) is an important macroalga in the sp. nov., L. delicata, L. dispersa, L. littlerorum, and L. North-eastern Atlantic archipelagos (i.e., schneideri). Lobophora spp. from Macaronesia are Macaronesia). Notably in the Canaries it can morphologically and ecologically distinguishable. In dominate benthic assemblages. While the genus has the Canaries, L. schneideri dominates the photophilic been the subject of several ecological studies in the assemblages from the intertidal to 20-30 m depth. Canaries, no study has yet been conducted to assess Lobophora dagamae sp. nov. grows in less illuminated species-level diversity of Lobophora in Macaronesia. shallow habitats, and replaces L. schneideri from 30 to We reassessed the diversity of Lobophora in ~80 m. Lobophora canariensis also has a wide vertical Macaronesia, reporting the presence of seven species distribution, from the intertidal to deep waters, while L. delicata, L. dispersa and L. littlerorum grow in shallow waters. The dominance of species with an 1 Received 1 August 2019. Accepted 31 October 2019. First Pub- upright habit versus prostrate or crustose species may lished Online 18 December 2019. Published Online 10 February 2020, Wiley Online Library (wileyonlinelibrary.com). be mediated by the pressure of herbivores. Four 2Author for correspondence: e-mail: [email protected]. Editorial species have an amphi-Atlantic distribution: L. Responsibility: C. Lane (Associate Editor) 346 LOBOPHORA DIVERSITY, ECOLOGY AND DISTRIBUTION IN MACARONESIA 347 littlerorum, L. canariensis, L. delicata, and L. schneideri. eastern Canaries are slightly affected by Northwest Lobophora schneideri and L. delicata are furthermore African upwelling. In contrast, Cape Verde Islands distributed in the Mediterranean Sea. By sampling a have nutrient–enriched waters because of the pivotal region in the Atlantic, this study significantly strong upwelling plume from the coast of Senegal improves our knowledge of Lobophora biogeography and Mauritania (Hoepffner et al. 2014). in the Atlantic Ocean. Macaronesia constitutes a Seaweed assemblages vary drastically along this lati- species–poor region for Lobophora where no tudinal gradient, with communities dominated by diversification events occurred, and a region of cold-temperate taxa in the northernmost archipelago overlap between the Greater Caribbean and the Indo- of the Azores, a mixture of species with colder and Pacific. warmer affinities in Madeira and the Canaries, and a dominance of tropical taxa in the southernmost Cape Key index words: barcoding; cox3; Macaronesia; phy- Verde Islands (Sangil et al. 2018). The Dictyotales logeny; molecular taxonomy Bory de Saint-Vincent (Phaeophyceae), apart from Abbreviations: cox3, mitochondrial encoded cyto- the crustose coralline algae, are the dominant chrome c oxidase III gene; DNA, deoxyribonucleic macroalgae in Macaronesia. Lobophora is one of the acid; psbA, chloroplast encoded photosystem II pro- most ecologically important genera, though impor- tein D1; rbcL, chloroplast encoded ribulose-1,5- tant differences in abundance exist between and biphosphate carboxylase within archipelagos (Sangil et al. 2018). Lobophora populations colonize rocky substrates from the inter- tidal to deep subtidal, at least to 80 m depth (C. San- Located between 14° N and 39° N, 32° W and gil, pers. obs.). In the Canary Islands and Madeira, 13° W, the Macaronesian biogeographic region Lobophora frequently dominates and monopolizes shal- (i.e., North-eastern Atlantic archipelagos) lies low subtidal macroalgal assemblages. There, growth along a latitudinal gradient of ~ 2850 km. Mac- and size of Lobophora populations are strongly con- aronesia comprises four archipelagos, the Azores, trolled by the grazing of the sea urchin Diadema africa- Madeira, the Canary, and Cape Verde Islands num (Sangil et al. 2011). Urchin barrens replace (Fig. 1). All islands are of volcanic origin and Lobophora communities in places where overfishing have emerged from the ocean basin at various has allowed the demographic burst of D. africanum points in time. Ocean currents, notably the Azores (Sangil et al. 2012). While the genus has been the and Canary currents (branches of the North object of several ecological studies in this region, no Atlantic current) link these archipelagos creating a comprehensive taxonomic study has yet been con- route for the spread of marine coastal organisms ducted in Macaronesia assuming until 2016 that indi- from North to South. In addition, the North viduals of L. variegata constituted all the populations Equatorial current and counter-current and the studied. In 2016, Aglaozonia canariensis was transferred Mauritanian current directly affect the Cape Verde to Lobophora (as L. canariensis; Vieira et al. 2016), thus archipelago (Arıstegui et al. 2009). Latitudinal bringing the number of documented species in the changes in sea surface temperature (SST) can Canary Islands to two. A recent study showed that the exceed 6°C (Table 1). Colder and mesotrophic Mediterranean Sea accounted only three Lobophora waters surround the Azores. In Madeira and west- species including one obvious lessepsian migrant (L. ern Canaries the waters are oligotrophic, while the lessepsiana Vieira et al. 2018). In contrast, the Greater a bcAzores Madeira Porto Santo Azores b São Miguel Madeira Madeira c 200 km 50 km Canaries d deCanaries Cape Verde La Palma Tenerife Cape Verde La Gomera e El Hierro Gran Canaria 1000 km 200 km 200 km Santiago FIG. 1. Map of sampling localities in the Macaronesian archipelagos (a). Sampling was performed in the Azores (b), Madeira (c), Can- aries (d), and Cape Verde (e). 348 CHRISTOPHE VIEIRA ET AL. TABLE 1. Summary of the geographic position, oceanographic conditions and richness of herbivores in the Macaronesian archipelagos (see Sangil et al. 2018 for references). Azores Madeira Canaries Cape Verde Latitude 39.72 to 36.92N 33.10 to 32.40N 29.41 to 27.63N 17.21 to 14.80N Longitude À31.79 to À24.77W À17.26 to À16.27W À18.16 to À13.33W À25.36 to À22.66W SSTmin 15.39–16.40°C 17.47–18.14°C 18.06–19.87°C 21.82–23.51°C SSTmean 18.42–19.46°C 20.30–21.10°C 20.22–22.14°C 23.95–24.90°C Water Mesotrophic Oligotrophic Oligotrophic Mesotrophic À À À À Productivity Nitrate 1.2–1.6 lmolÁL 1 Nitrate 0.67–0.73 lmolÁL 1 Nitrate 0.56–0.68 lmolÁL 1 Nitrate 1.39–1.850 lmolÁL 1 À À À À Chl a 0.16-0.29 mgÁm 3 Chl a 0.11-0.16 mgÁm 3 Chl a 0.12-0.18 mgÁm 3 Chl a 0.25-0.39 mgÁm 3 Herbivores Poorly diversified Poorly diversified Poorly diversified Diversified 3 urchins species 4 urchins species 4 urchins species 5 urchins species 5 fish species 5 fish species 5 fish species 11 fish species Caribbean stands as the diversity hotspot for the captured using a Fujifilm X10 digital camera attached to a genus Lobophora in the North Atlantic with 18 species Leica DM500 (Leica Microsystems, Wetzlar, Germany) micro- and a high level of endemism (Vieira et al. 2017, un- scope. Voucher specimens were dried as herbarium exsiccate and deposited in either BR (Herbarium of the Botanic Gar- published, Camacho et al. 2019). This study focused den Meise, Belgium) or TFC (Herbarium of the University of on Macaronesia to improve our understanding of La Laguna, Canaries), in some cases, specimens were pre- diversity and biogeography of the genus Lobophora in a served in a 4% formaldehyde solution with seawater for pivotal region in the Atlantic. To reassess the species anatomical examination. diversity of Lobophora, we conducted a wide-ranging molecular-based taxonomic study across the Mac- RESULTS aronesian archipelagos, documented Macaronesian Lobophora species ecology and analyzed how these spe- Phylogenetics trees generated by Bayesian infer- cies relate among archipelagos and to other Atlantic ence and maximum likelihood analyses based on regions. cox3, pbsA and rbcL markers resolved the Macarone- sian sequences in seven distinct clades that were – MATERIALS AND METHODS previously documented (Figs. 2, S1 S5 in the Sup- porting Information). These clades are not Taxon sampling. Sampling was performed in the four restricted to Macaronesia. Five clades correspond to archipelagos (i.e., Azores, Madeira, Canary, and Cape Verde L. canariensis, L. delicata, L.