INTRODUCTIONTop
Oceanic islands, bathed by oligotrophic waters, are considered to be ecosystems with unexplored biodiversity and high endemism of several groups of marine organisms. Some remote and isolated islands are less influenced by anthropogenic impacts than coastal islands. These ecosystems are considered peculiar and pristine natural habitats, showing environmental transitional features that result in easily interpretable biogeographic and ecological patterns (Borregaard et al. 2016Borregaard M.K., Amorim I.R., Borges P.A.V., et al. 2016. Oceanic island biogeography through the lens of the general dynamic model: Assessment and prospect. Biol. Rev. 92: 830-853., Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685.). Moreover, oceanic islands are examples of disjunctions or hypothetical oceanographic discontinuities across a biogeographic transitional zone. Distinct hydrographic features promote physical breaks that can influence dispersal and connectivity between populations.
The Brazilian oceanic ecosystems are comprised of the Rocas Atol, Trindade e Martim Vaz, São Pedro e São Paulo, and Fernando de Noronha archipelagos. The focus of the present study is Trindade, a volcanic island located 1140 km off the coast of Brazil. There is much scientific interest in Trindade as an ecological model for environmental predictions and as a control area to be compared with other locations.
Seaweeds are key organisms in the sustainability of the entire trophic chain as primary producers and providers of biogenic habitats for several marine organisms. In addition, macroalgae assimilate nutrients and trace elements from seawater and are responsible for pH control (homeostasis) in the water column. For these reasons, macroalgae are sensitive bioindicators to changes in the physical and chemical patterns of seawater (Kordas et al. 2011Kordas R.L., Harley C.D.G., O’Connor M.I. 2011. Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol. 400: 218-226.). Studies on macroalgae diversity from Trindade Island were published by Richardson (1975)Richardson W.D. 1975. The marine algae of Trinidad, West Indies. Bull. Br. Mus. Nat. Hist. 5: 96-107., Pedrini et al. (1989)Pedrini A.G., Gonçalves J.E.A., Fonseca M.C.S., et al. 1989. A Survey of the Marine Algae of Trindade Island, Brazil. Bot. Mar. 32: 97-99. and Nassar (1994)Nassar C.A.G. 1994. An assessment to the benthic marine algae at Trindade Island, Espírito Santo, Brazil. Rev. Bras. Biol. 54: 623-629.. Villaça et al. (2006)Villaça R., Pedrini A., Pereira S., et al. 2006. Flora marinha bentônica das ilhas oceânicas brasileiras, In: Alves R., Castro J. (eds), Ilhas Oceânicas Brasileiras Da Pesquisa Ao Manejo. Ministério do meio ambiente, Brasilia, pp. 105-146. reported the last seaweed taxa compilation, listing 121 species, with 53% originating from the intertidal and shallow subtidal zones and 47% from the deeper subtidal zone.
Sea surface temperature (SST) and salinity are the main factors that determine the regional and local growth of seaweed, including at biogeographical boundaries. The variation in marine abiotic parameters may be due to natural variability as well as anthropogenic activity (Lifland 2003Lifland J. 2003. The North Atlantic Oscillation: climatic significance and environmental impact. EOS Trans. Am. Geophys. Union 84: 73.). The interannual variability in these parameters is the result of large-scale weather patterns, whereas anthropogenically induced variability is associated with circulation anomalies (atmospherical and marine) and abrupt changes in thermohaline and precipitation patterns.
Current global changes are inducing shifts in seaweed assemblages and ecosystem functionality (Parmesan 2006Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37: 637-669, Rosenzweig et al. 2008Rosenzweig C.D., Karoly M., Vicarelli P., et al. 2008. Attributing physical and biological impacts to anthropogenic climate change. Nature 453: 353-357., Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685.). Responses to climate change are particularly rapid and strong in marine ecosystems, especially in the intertidal zone where species often reside at their upper temperature-tolerance limits (Hoegh-Guldberg and Bruno 2010Hoegh-Guldberg O., Bruno J.F. 2010. The impact of climate change on the world’s marine ecosystems. Science 328: 1523-1528., Sorte et al. 2010Sorte C.J.B., Williams S.L., Carlton J.T. 2010. Marine range shifts and species introductions: comparative spread rates and community impacts. Global Ecol. Biogeogr. 19: 303-316.). The present study focuses on this zone. In oceanic ecosystems, considering abiotic shifts and their responses, species that fail to acclimatize physiologically (or evolve genetically) will either expand their distributional limits into new habitats or become extinct (Jueterbock et al. 2013Jueterbock A., Tyberghein L., Verbruggen H., et al. 2013. Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol. Evol. 3: 1356-1373.).
Reports of new records, including cryptogenic species, have a temporal limit in their interpretability, considering that species may expand their distributional ranges (Occhipinti-Ambrogi 2007Occhipinti-Ambrogi A. 2007. Global change and marine communities: alien species and climate change. Mar. Pollut. Bull. 55: 342-352.). This would result in geographical distribution shifts and reduction in endemism levels (Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685., 2020Pellizzari F.M., Rosa L.H., Yokoya N.S. 2020. Biogeography of Antarctic seaweeds facing climate changes. In: Gomez I., Huovinen P. (eds). Antarctic Seaweeds. Springer, Cham. pp. 83-102., Oliveira et al. 2020Oliveira M.C., Pellizzari F.M., Medeiros A., et al. 2020. Diversity of Antarctic seaweeds. In: Gomez I., Huovinen P. (eds). Antarctic Seaweeds. Springer, Cham. pp. 23-42. ), which can modify the structure of marine communities. According to Sangil et al. (2012)Sangil C., Sansón M., Afonso-Carillo J., et al. 2012. Changes in sub-tidal assemblages in a scenario of warming: proliferations of ephemeral benthic algae in the Canary Islands (eastern Atlantic Ocean). Mar. Environ. Res. 77: 120-128., abrupt changes in the abiotic parameters emerge as invasion windows for expanding the biogeographical distribution of marine species. Guo et al. (2005)Guo K., Taper M., Schoenberger M., et al. 2005. Spatial-temporal population dynamics across species range: from centre to margin. Oikos 108: 47-57. and Araújo et al. (2009)Araújo R., Bárbara I., Tibaldo M., et al. 2009. Checklist of benthic marine algae and cyanobacteria of northern Portugal. Bot. Mar. 52: 24-46. showed that distributional shifts are likely to be magnified for species from geographic boundaries, where organisms are at their ecophysiological tolerance limits. This suggests that the most effective method for predicting diversity changes is by monitoring boundary or marginal populations, such as the insular seaweed assemblages found in Trindade.
Several studies have reported changes in macroalgae diversity, mainly in coastal ecosystems (Iles et al. 2012Iles A.C., Gouhier T.C., Menge B.A., et al. 2012. Climate-driven trends and ecological implications of event-scale upwelling in the California Current System. Global Change Biol. 18: 783-796., Duarte et al. 2013Duarte L., Viejo R.M., Martínez B., et al. 2013. Recent and historical range shifts of two canopy-forming seaweeds in North Spain and the link with trends in sea surface temperature. Acta Oecol. 51: 1-10., Sjøtun et al. 2015Sjøtun K. Husa V., Asplin L. et al. 2015. Climatic and environmental factors influencing occurrence and distribution of macroalgae - a fjord gradient revisited. Mar. Ecol. Prog. Ser. 532: 73-88.). Insular areas have also been addressed, including studies in Tristan da Cunha (Saunders et al. 2019Saunders G.W., Brooks C.M., Scott S. 2019. Preliminary DNA barcode report on the marine red algae (Rhodophyta) from the British Overseas Territory of Tristan da Cunha. Cryptogam. Algol. 40: 105-117.), Ascension (Barnes et al. 2015Barnes DKA, Brown J, Brickle P, et al. 2015. Marine biodiversity of Ascension Island’s shelf; scientific support for a marine protected area. Unpublished JR15003 cruise report, British Antarctic Survey., Tsiamis et al. 2014Tsiamis K., Peters A.F., Shewring D.M., et al. 2014. Marine benthic algal flora of Ascension Island, South Atlantic. J. Mar. Biol. Assoc. UK 97: 681-688.), the Canary Islands (Afonso-Carrillo et al. 2007Afonso-Carrillo J., Sansón M., Sangil C., et al. 2007. New records of benthic marine algae from the Canary Islands (eastern Atlantic Ocean): morphology, taxonomy and distribution. Bot. Mar. 50: 119-127., Sanson et al. 2002Sanson M, Reyes J, Afonso-Carrillo J., et al. 2002. Sublittoral and Deep-Water Red and Brown Algae New from the Canary Islands. Bot. Mar. 45: 35-49., Haroun et al. 2002Haroun R.J., Gil-Rodríguez M.C., Díaz de Castro J. et al. 2002. A Checklist of the Marine Plants from the Canary Islands (Central Eastern Atlantic Ocean). Bot. Mar. 45: 139-169.) and the Azores islands, located in the southern and northern zones of the Mid-Atlantic Ridge (MAR), respectively, and Trindade between Brazil and MAR. Large-scale and mainly climate-driven distributional and biogeographical changes to temperate and polar ecosystems have been broadly reported (Sjøtun et al. 2015Sjøtun K. Husa V., Asplin L. et al. 2015. Climatic and environmental factors influencing occurrence and distribution of macroalgae - a fjord gradient revisited. Mar. Ecol. Prog. Ser. 532: 73-88., Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685., 2020Pellizzari F.M., Rosa L.H., Yokoya N.S. 2020. Biogeography of Antarctic seaweeds facing climate changes. In: Gomez I., Huovinen P. (eds). Antarctic Seaweeds. Springer, Cham. pp. 83-102., Oliveira et al. 2020Oliveira M.C., Pellizzari F.M., Medeiros A., et al. 2020. Diversity of Antarctic seaweeds. In: Gomez I., Huovinen P. (eds). Antarctic Seaweeds. Springer, Cham. pp. 23-42.). In addition to these changes, new molecular techniques are being used to investigate cryptic species and reorganize the macroalgal taxonomy, establishing increasingly accurate phylogenetic relationships. Classical taxonomy, supported by molecular techniques, uses conservationist tools to monitor population shifts and highlights new ecological trends, introductions and extinctions. For example, it has been widely used as a technique for predicting and mitigating natural or anthropic impacts on environments. However, recent checklists and ecological assays for tropical remote islands are scarce.
This study establishes an updated seasonal checklist, presenting new records of 60 species, and demonstrates the relationship between these records and abiotic parameters to discuss new trends in marine ecology facing environmental changes. The scarcity of recent studies on seaweed diversity and the absence of a temporal approach for Trindade or any other Brazilian oceanic island justify this contribution. We also provide a baseline for further comparative studies with other Atlantic oceanic islands that aim to re-evaluate aspects of macroalgae endemism, isolation, connections and biogeographical distributional shifts. Moreover, this database will be fundamental to the establishment of environmental monitoring plans in response to climatic and oceanographic changes.
MATERIALS AND METHODSTop
Study area
Trindade is located at 20°30′30″S, 29°19′30″W (Fig. 1), 1140 km east of Espírito Santo State. The Archipelago of Trindade and Martim Vaz recently became a Federal Environmental Protected Area (Decree 9312/2018). In 1957, the Brazilian Navy established the Oceanographic Station of Trindade Island, which has provided support for the claim of the area as an Exclusive Economic Zone. Since 2007, the Scientific Station of Trindade Island has supported research and conservation activities on the island, as well as this project.
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The island is the easternmost part of the Vitória-Trindade Ridge, an underwater volcanic chain (Almeida 2006Almeida F.F.M. de. 2006. Ilhas oceânicas brasileiras e suas relações com a tectônica atlântica. Terrae Didat. 2: 3-18. ), erected from the Atlantic abyss by mixed volcanic activity approximately three million years ago (Alves 1998Alves R.J.V. 1998. Ilha da Trindade & Arquipélago Martin Vaz: Um Ensaio Geobotânico. Serviço de Documentação da Marinha, Rio de Janeiro, 144 pp.). Almeida (2000Almeida F.M. de. 2000. A Ilha de Trindade. In: Schobbenhaus C., Campos D.A., et al. (eds), Sítios Geológicos e Paleontológicos do Brasil., 2002)Almeida F.F.M. de. 2002. Ilha de Trindade - Registro de vulcanismo cenozóico no Atlântico Sul. In: Schobbenhaus C., Campos D.A., et al. (eds), Sítios Geológicos e Paleontológicos do Brasil. DNPM/CPRM - Comissão Brasileira de Sítios Geológicos e Paleobiológicos (SIGEP), Brasilia, pp. 369-377. reports that Trindade, almost completely composed of volcanic and subvolcanic rocks, was formed between the end of the Pliocene and the Holocene (2.3 and 2.9 Ma). Pires et al. (2016)Pires G.L.C., Bongiolo E.M., Geraldes M.C., et al. 2016. New 40Ar/39Ar ages and revised 40K/40Ar* data from nephelinitic-phonolitic volcanic successions of the Trindade Island (South Atlantic Ocean). J. Volcanol. Geotherm. Res. 327: 531-538. presented a new age proposal for the formation of Trindade, coupled with previous petrological information, allowing the volcanic history of the island to be reconstructed (i.e. 3.9-0.25 Ma), distinguishing volcanic episodes and solving previous stratigraphic uncertainties. Volcanic activity in Trindade ceased completely by 0.25 Ma.
Trindade is 5.9 km long and 2.7 km wide, and is aligned NW-SE. The emerged area encompasses 13.5 km2 with a surrounding depth of approximately 5000 m. Five volcanic episodes gave rise to the oldest region (the north face) and a more recent region (the south face) (Calliari et al. 2016Calliari L.J., Pereira P.S., Short A.D., et al. 2016. Sandy Beaches of Brazilian Oceanic Islands. Brazilian Beach Syst. 17: 543-571.). Apart from some pyroclastic rocks, the rocks are mainly sodium-alkaline and silica rich, originating from undersaturated lavas. The coast along the island is composed of algal reefs, narrow volcanic rocky beaches, localized dunes, cones and slopes. The protrusions of volcanic rocks have formed several embayments surrounded by biogenic substrate mainly from corallinaceous algae beds. The beach lines (Fig. 2) consist of 76% rock or beachrock covered by biogenic substrate and 24% sand (Calliari et al. 2016Calliari L.J., Pereira P.S., Short A.D., et al. 2016. Sandy Beaches of Brazilian Oceanic Islands. Brazilian Beach Syst. 17: 543-571.).
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Figure 3 shows the temporal thermohaline pattern during the past 14 years (August 2004-August 2018) in the surroundings of Trindade, with higher minimum temperatures (winter) and lower salinities (during winter and summer) since 2012. In 2017, anomalies for this decade were observed for both parameters.
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Trindade’s climate ranges from tropical semi-humid to semi-arid. The rainfall regime is random with light rain but constant during the summer; during the late autumn/winter, cold fronts periodically reach the island (Almeida 2006Almeida F.F.M. de. 2006. Ilhas oceânicas brasileiras e suas relações com a tectônica atlântica. Terrae Didat. 2: 3-18.). The tropical climate is mitigated by the dominance of east (45%) trade winds. The annual average temperature is 25°C (maximum 32.3°C in February and minimum in August of 17.3°C). Based on the WAVEWATCH III model simulations (NOAA), waves arrive mainly from the south (33.7%) and southwest (23.4%), with an average height of 2.14 m. The tidal regime is semi-diurnal, with a micro-tidal range of 1.3 m. Calliari et al. (2016)Calliari L.J., Pereira P.S., Short A.D., et al. 2016. Sandy Beaches of Brazilian Oceanic Islands. Brazilian Beach Syst. 17: 543-571. discuss a higher frequency of meteorological fronts than previously reported, besides changes in the circulation patterns, and changes in the rainfall regime for Trindade surroundings.
Sampling methods and analysis of biological data
In contrast to other macroalgae assemblage studies along the Brazilian coast, previous studies in Trindade Island focused on the deep subtidal area, using dredged material obtained from short-term expeditions of the island surroundings. These studies mainly conducted sporadic and random samplings rather than using standardized methods.
Sampling surveys were supported by Brazilian Navy ships and occurred over four years, during the austral summer (January) and winter (July and August) of 2014, 2015, 2016 and 2017, eight cruises in total. Macroalgae and cyanobacteria specimens were sampled along 13 beaches (Fig. 1). The specimens (n=3, i.e. 3 specimens per species/beach) were collected by scraping the algal turfs and bedrock during spring tide along the intertidal zone. The cyanobacteria specimens were sorted among the collected turfs. Each site was sampled once per cruise each summer or winter. The sampling method performed at each site used quadrats (n=5, 0.5 m2) distributed every ±20 m along a 100 m transect. The shallow subtidal area was sampled using free diving. Fertile and entire specimens were collected along quadrats of 50×50 cm (n=5) distributed in linear transects (150 m) parallel to the coastline. A remotely operated vehicle (Guardian 2.1, France) was used to locate the calcareous algae beds up to 15 m deep, facilitating the samplings and observations of the spatio-temporal distribution.
In the laboratory, turf and beachrock samples were sorted, washed and fixed with formalin (4% diluted in seawater), for further taxonomic analysis of the vegetative and reproductive thalli through stereoscopic and optical microscopy with phase contrast and an image capture system (Olympus CX31). External morphological features such as colour, height, shape and size of holdfast and the type of branching were observed, annotated and photographed before fixation. For internal morphological observations, the material was dissociated (filamentous) or hand-sectioned (leafy and fleshy thalli) using scalpel blades and mounted on glass slides for microscopic observation. Calcareous specimens were decalcified with 5% hydrochloric acid and sectioned to observe the reproductive structures. Cryptic species or groups, when it was possible to obtain sufficient monospecific material among the turf (Fig. 4), were conditioned in silica gel for molecular analysis, using different markers for each algal group. Nomenclatural information and taxonomical status were applied following Guiry and Guiry (2020)Guiry M.D., Guiry G.M. 2020. AlgaeBase. World-wide electronic publication at http://www.algaebase.org. Exsiccate vouchers of the new records were deposited in the Herbarium of the Botanical Museum of Curitiba.
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Morphological taxonomic identification was performed, using as comparative material specialized and illustrated descriptions of the species from the Brazilian oceanic islands (Villaça et al. 2006Villaça R., Pedrini A., Pereira S., et al. 2006. Flora marinha bentônica das ilhas oceânicas brasileiras, In: Alves R., Castro J. (eds), Ilhas Oceânicas Brasileiras Da Pesquisa Ao Manejo. Ministério do meio ambiente, Brasilia, pp. 105-146., 2010Villaça R., Carvalhal Fonseca A., Jensen V.K., et al. 2010. Species composition and distribution of macroalgae on Atol das Rocas, Brazil, SW Atlantic. Bot. Mar. 53: 113-122., Amado-Filho et al. 2012Amado-Filho G.M., Pereira-Filho G.H., Bahia R.G., et al. 2012. Occurrence and distribution of rhodolith beds on the Fernando de Noronha Archipelago of Brazil. Aquat. Bot. 101: 41-45., Burgos 2011Burgos D.C. 2011. Composição e estrutura das comunidades em macroalgas do infralitoral do arquipélago de Fernando de Noronha, Pernambuco - Brasil, com ênfase nas calcárias incrustantes. Universidade Federal Rural de Pernambuco. Tese de doutorado. 94 pp., Burgos et al. 2009Burgos D.C., Pereira S.M.B., Bandeira-Pedrosa M.E. 2009. Levantamento florístico das Rodofíceas do Arquipélago de São Pedro e São Paulo (ASPSP) - Brasil. Acta Bot. Brasilica 23: 1110-1118. , Pereira-Filho et al. 2011Pereira-Filho G.H., Amado-Filho G.M., Guimarães S.M.P.B., et al. 2011. Reef fish and benthic assemblages of the Trindade and Martin Vaz island group, SouthWestern Atlantic. Brazilian J. Oceanogr. 59: 201-212., 2012Pereira-Filho G.H., Amado-Filho G.M., Moura R.L., et al. 2012. Extensive Rhodolith Beds Cover the Summits of Southwestern Atlantic Ocean Seamounts. J. Coast. Res. 279: 261-269., 2015Pereira-Filho G., Veras P., Francini-Filho R., et al. 2015. Effects of the sand tilefish Malacanthus plumieri on the structure and dynamics of a rhodolith bed in the Fernando de Noronha Archipelago, tropical West Atlantic. Mar. Ecol. Prog. Ser. 541: 65-73.); southeastern (Cordeiro-Marino 1978Cordeiro-Marino M. 1978. Rodofíceas bentônicas marinhas do estado de Santa Catarina, Rickia. Séríe criptogâmica dos Arquivos de Botânica do Estado de São Paulo. Secretaria da Agricultura, Coordenadoria da Pesquisa de Recursos Naturais, Instituto de Botânica. São Paulo., Crispino 2007Crispino L.M.B. 2007. Benthic marine Cyanobacteria from the coast of São Paulo. PhD thesis, Instituto de Botânica da Secretaria de Estado do Meio Ambiente. São Paulo, Brasil. 154 pp., Coto 2007Coto A.C.S.P. 2007. Biodiversidade de Clorófitas Marinhas bentônicas do litoral do estado de São Paulo, Dissertação de Mestrado, Instituto de Botânica, Secretaria do Meio Ambiente, Programa de Mestrado em Biodiversidade Vegetal e Meio Ambiente. 171 pp.) and northeastern Brazil (Moura 2000Moura C.W.N. 2000. Coralináceas com genículo (Rhodophyta, Corallinales) do litoral do Brasil. Tese de doutorado. Instituto de Biociências. Universidade de São Paulo. 264 pp., Nunes 2005Nunes J.M.C. 2005. Rodofíceas marinhas bentônicas do estado da Bahia, Brasil. Tese de doutorado. Instituto de Biociências, Universidade de São Paulo. 410 pp., Nunes and Guimarães 2008Nunes J.M.D.C., Guimarães S.M.P.D.B. 2008. Novas referências de rodofíceas marinhas bentônicas para o litoral brasileiro. Biota Neotrop. 8: 89-100.); Florida (Littler and Littler 2000Littler D.S., Littler M.M. 2000. Caribbean reef plants: an identification guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. OffShore Graphics, Inc., Washington, DC., Wysor and Kooistra 2003Wysor B., Kooistra W.H.C.F. 2003. An annotated list of marine Chlorophyta from the Caribbean coast of the Republic of Panama. Nov. Hedwigia 77: 487-523., Dawes and Mathieson 2003Dawes J.C., Mathieson A.C. 2003. A Guide to the Seaweeds of Florida. J. Phycol. 38: 5-6.), the Caribbean islands (Semidey and Suárez 2013Semidey A., Suárez A.M. 2013. Adiciones a las macroalgas marinas de Cuba. Hidrobiologica 23: 440-442., García and Díaz-Pulido 2006García C.B., Díaz Pulido G. 2006. Dynamics of a macroalgal rocky intertidal community in the Colombian Caribbean. Bol. Invest. Mar. Costeras - INVEMAR 35: 7-18., Díez-García et al. 2013Diez García Y.L., Jover Capote A., Suárez Alfonso A.M., et al. 2013. Distribution of epiphytic macroalgae on the thalli of their hosts in Cuba. Acta Bot. Brasilica 27: 815-826.), Tristan da Cunha (Saunders et al. 2019Saunders G.W., Brooks C.M., Scott S. 2019. Preliminary DNA barcode report on the marine red algae (Rhodophyta) from the British Overseas Territory of Tristan da Cunha. Cryptogam. Algol. 40: 105-117.), Santa Helena and Ascension Island (Tsiamis et al. 2014Tsiamis K., Peters A.F., Shewring D.M., et al. 2014. Marine benthic algal flora of Ascension Island, South Atlantic. J. Mar. Biol. Assoc. UK 97: 681-688.); Ascension Islands (Barnes et al. 2015Barnes DKA, Brown J, Brickle P, et al. 2015. Marine biodiversity of Ascension Island’s shelf; scientific support for a marine protected area. Unpublished JR15003 cruise report, British Antarctic Survey.); and the Canary Islands (Sanson et al. 2002Sanson M, Reyes J, Afonso-Carrillo J., et al. 2002. Sublittoral and Deep-Water Red and Brown Algae New from the Canary Islands. Bot. Mar. 45: 35-49., Haroun et al. 2002Haroun R.J., Gil-RodrÌguez M.C., DÌaz de Castro J. et al. 2002. A Checklist of the Marine Plants from the Canary Islands (Central Eastern Atlantic Ocean). Bot. Mar. 45: 139-169., Afonso-Carrillo et al. 2007Afonso-Carrillo J., Sansón M., Sangil C., et al. 2007. New records of benthic marine algae from the Canary Islands (eastern Atlantic Ocean): morphology, taxonomy and distribution. Bot. Mar. 50: 119-127.).
Environmental data
SST, salinity and pH were selected as oceanographic set predictors to be compared with the biological data generated. Abiotic data were measured in situ along the sampled beaches during the winter and summer: SST and salinity were monitored using a multiparameter probe (Hexis, USA) and pH was measured by a portable pH meter. Rainfall and ultraviolet radiation data were obtained from the Trindade Island Meteorological Station database. The forecast of tidal amplitudes was obtained from the Hydrography and Navigation Office website, Brazilian Navy.
Statistical analysis
The Sorensen similarity index was used to construct a cluster dendrogram and compare the grouping and similarity/dissimilarity between faces and cruises (during summer and winter). A t-test was performed to test differences between the north and south faces. An orthogonal ANOVA was performed to test differences in seaweed richness between the north and south faces and between the summer and winter cruises. The seaweed richness data were tested for normality and transformed into log-normal data when the ANOVA constraint was not satisfied. For non-normal data, we assumed an alpha value of 0.01, as suggested by Underwood (1997)Underwood A.J. 1997. Experiments in ecology: Their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, 504 pp.. Tukey HSD was the chosen post-hoc test. All the analyses were performed using R statistical software (version 3.6.1) and R-Studio (1.2.5019) (R Core Team 2019R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.).
RESULTSTop
A total of 141 macroalgae species were identified at the 13 beaches sampled in Trindade Island. Sixty species represent new records, comprising 26 species of Chlorophyta, 9 species of Phaeophyceae and 25 species of Rhodophyta (Table 1). Three putative new species of calcareous algae are under investigation. In addition, 20 species of cyanobacteria were reported in the first time to the island, totalling 161 species from the intertidal to the shallow subtidal zones (Fig. 5).
Table 1. – New seaweed records: temporal checklist from Trindade Island. Information of location and habitat occurrence and previous records off Trindade are provided. 1, present; 0, absent; a.b.o.i, another Brazilian oceanic island.
| Trindade | Previous Ocurrences off Trindade | ||||||
|---|---|---|---|---|---|---|---|
| Summer | Winter | Beach | Habitat | a.b.o.i. | Brazil Coast | Nearest occurrence off Brazil | |
| CYANOBACTERIA | |||||||
| Coleofasciculus chthonoplastes (Thuret ex Gomont) Siegesmund et al. | 1 | 0 | E | turf midlittoral | 0 | 1 | Canary Islands |
| Chamaecalyx sp. | 1 | 0 | T | turf midlittoral | 0 | 1 | Canary, S Portugal, Argentina |
| Leibleinia sp. | 1 | 0 | A | turf midlittoral | 0 | 1 | |
| Sirocoleum kurzii Gomont | 1 | 0 | PR | turf midlittoral | 0 | 1 | Canary /Argentina |
| Symploca sp. | 1 | 1 | A/PO | turf midlittoral | 0 | 1 | |
| Anabaena sp. | 1 | 0 | E | turf midlittoral | 0 | 1 | |
| Hydrocoryne spongiosa Schwabe ex Bornet & Flahault | 1 | 1 | A/PN | turf midlittoral | 0 | 1 | Caribbean Isls., Canary, Madeira |
| Nostoc commune Vaucher ex Bornet & Flahault | 1 | 1 | A/C /E/F/O | turf midlittoral | 0 | 1 | Canary /Argentina |
| Blennothrix lyngbyacea (Kutzing ex Gomont) Anagnostidis & Komarek | 1 | 1 | A/C | turf midlittoral | 0 | 1 | Caribbean, Canary, Madeira |
| Lyngbya confervoides C.Agardh ex Gomont | 1 | 1 | A/C/PN/PR | turf midlittoral | 0 | 1 | Caribbean, Canary, Madeira, Gough |
| Lyngbya majuscula Harvey ex Gomont | 1 | 1 | A | turf midlittoral | 1 | 1 | Canary |
| Oscillatoria sp. | 0 | 1 | A | turf midlittoral | 1 | 1 | |
| Phormidium cf. holdenii (Forti) Branco et al. | 1 | 0 | A | turf midlittoral | 0 | 1 | Caribbean, Canary, Madeira |
| Phormidium nigroviride (Thwaites ex Gomont) Anagnostidis & Komarek | 1 | 1 | A / E | turf midlittoral | 0 | 1 | Florida, Argentina, Canary |
| Calothrix sp. | 0 | 1 | A | turf midlittoral | 0 | 1 | |
| Rivularia atra Roth ex Bornet & Flahault | 1 | 1 | A/E | turf midlittoral | 0 | 1 | Caribbean/ Canary |
| Kyrtuthrix sp. (cf. maculans) | 0 | 1 | A | turf midlittoral | 0 | 1 | Canary |
| Scytonema sp. | 1 | 0 | E | turf midlittoral | 0 | 1 | |
| Spirulina major Kutzing ex Gomont | 1 | 0 | PO | turf midlittoral | 0 | 1 | Canary, Cuba, Argentina |
| Stigonema sp. | 1 | 0 | E | turf midlittoral | 0 | 1 | |
| Total 20 | 17 | 11 | |||||
| CHLOROPHYTA | |||||||
| Bryopsis hypnoides J.V.Lamouroux | 1 | 1 | A/L | upper subl., tidal pools | 0 | 1 | Canary, Azores, Caribbean |
| Caulerpa kempfii A.B.Joly & S.M.B.Pereira | 1 | 1 | E/A | beach rock | 0 | 1 | Caribbean |
| Chaetomorpha brachygona Harvey | 0 | 1 | C | midlittoral | 0 | 1 | Caribbean |
| Cladophora albida (Nees) Kutzing | 1 | 1 | A / O / PN | turf / beach rock | 1 | 1 | Canary, Azores, Caribbean |
| Cladophora brasiliana G.Martens | 1 | 0 | C / E / P | turf / beach rock | 0 | 1 | Caribbean |
| Cladophora catenata Kutzing | 1 | 1 | O/N | turf / beach rock | 0 | 1 | Gough Island , Caribbean |
| Cladophora coelothrix Kutzing | 1 | 1 | A / C / O | turf / beach rock | 0 | 1 | Ascension, St Helena |
| Cladophora corallicola Borgesen | 1 | 1 | A / C / P | upper subl., tidal pools | 0 | 1 | Caribbean |
| Cladophora dalmatica Kuttzing | 1 | 1 | A / C / F | turf / beach rock | 0 | 1 | Canary, Bermudas |
| Cladophora lehmanniana (Lindenberg) Kutzing | 1 | 0 | CA | turf / beach rock | 0 | 1 | Ascension, Cape Verde, Canary |
| Cladophora rupestris (Linnaeus) Kutzing | 0 | 1 | PN | turf / beach rock Midl. | 0 | 1 | Azores, Gough |
| Cladophora sericea (Hudson) Kutzing | 1 | 1 | A / E / PN | turf / beach rock Midl. | 0 | 1 | Canary Islands |
| Lychaete pellucida (Hudson) M.J.Wynne | 1 | 0 | A | upper subl., tidal pools | 0 | 0 | Azores, Gough, Canary, Cape Verde |
| Neostromatella monostromatica Wynne, Furnari & Nielsen | 1 | 1 | A / E / P | epiphyte of another algae | 0 | 1 | Canary |
| Parvocaulis parvulus (Solms-Laubach) Berger et al. | 1 | 1 | E / T | upper sublittoral rocks | 1 | 1 | Canary, Madeira, Caribbean |
| Prasiolales | 0 | 1 | A | upper eulittoral | 0 | 0 | N Atlantic, Mediterranean, New Zealand |
| Pseudorhizoclonium africanum (Kutzing) Boedeker | 0 | 1 | O | midlittoral | 0 | 1 | C Verde, Azores, Canary, Caribbean |
| Ulva chaetomorphoides (Borgesen) Hayden et al. | 1 | 0 | E | turf | 0 | 1 | Bermudas, Caribbean |
| Ulva clathrata (Roth) C.Agardh | 1 | 1 | A / PN | rock pools | 0 | 1 | Ascencion, Azores, Canary, Cape Verde |
| Ulva compressa Linnaeus | 0 | 1 | A | beachrocks,upper subl. | 0 | 1 | Ascencion, Canary, Cape Verde, Azores, |
| Ulva flexuosa Wulfen | 1 | 1 | A / E / PN | beachrocks,upper subl. | 1 | 1 | Ascencion, Canary, Caribbean, C Verde, Azores |
| Ulva linza Linnaeus | 0 | 1 | A | beachrocks,upper subl. | 0 | 1 | Caribbean, Azores, C Verde, Ascencion, Canary |
| Ulvella scutata (Reinke) R.Nielsen, C.J.O’Kelly & B.Wysor | 1 | 1 | A/E | epiphyte of another algae | 1 | 1 | Caribbean, Azores, Canary |
| Ulvella viridis (Reinke) R.Nielsen, C.J.O’Kelly & B.Wysor | 1 | 1 | A/C/E | epiphyte of another algae | 1 | 1 | Bermudas, Canary, Tristan da Cunha, Caribbean |
| Valonia aegagropila C.Agardh | 1 | 1 | A/E | upper subl., tidal pools | 1 | 1 | Canary |
| Valonia ventricosa J.Agardh | 1 | 1 | E | upper subl., tidal pools | 0 | 1 (N) | Ascencion, Caribbean, Bermuda, C Verde, Canary |
| Total 26 | 20 | 22 | |||||
| PHAEOPHYCEAE | |||||||
| Asterocladon rhodochortonoides (Borgesen) Uwai et al. | 1 | 0 | E | midlittoral and turf | 1 | 1 | Azores, Canary, St Helena |
| Dictyota ciliolata Sonder ex Kutzing | 1 | 1 | CA / E /O | rock pools, subl. rocks | 1 | 1 | Azores, Canary |
| Dictyota jamaicensis W.R.Taylor | 1 | 1 | E | rock pools, subl. rocks | 1 | 1 | Cape Verde; Caribbean Isls. |
| Ectocarpus fasciculatus Harvey | 1 | 1 | A / PN | midlittoral | 0 | 1 | Canary |
| Feldmannia indica (Sonder) Womersley & A.Bailey | 1 | 1 | A | beach Rock pools | 1 | 1 | Caribbean |
| Levringia brasiliensis (Montagne) A.B.Joly | 0 | 1 | E | beach rocks, rock pools | 0 | 1 | Ascension, Cape Verde |
| Padina antillarum (Kutzing) Piccone | 1 | 0 | PO / N | upper subl., tidal pools | 0 | 1 | Caribbean |
| Stypopodium zonale (J.V.Lamouroux) Papenfuss | 1 | 0 | E | rock pools, upper subl. | 1 | 1 | Caribbean, Ascencion, St Helena |
| Sphacelaria brachygonia Montagne | 1 | 1 | E / PR / L | midlittoral | 1 | 1 | Cape Verde |
| Total 9 | 8 | 6 | |||||
| RHODOPHYTA | |||||||
| Amphiroa anceps (Lamarck) Decaisne | 1 | 0 | E | turf, mid/upper subl. | 0 | 1 | South Africa |
| Amphiroa beauvoisii J.V.Lamouroux | 1 | 1 | N | mid/upper sublittoral | 1 | 1 | Azores, Canary, St Helena |
| Centroceras gasparrinii (Meneghini) Kutzing | 1 | 1 | A / PN | rock pools, sublittoral | 0 | 0 | Ascension, Caribbean |
| Ceramium brevizonatum H.E.Petersen | 1 | 1 | A / E / PN | turf and sublittoral rocks | 1 | 1 | Caribbean Isl. |
| Ceramium deslongchampsii Chauvin ex Duby | 1 | 1 | E / F | turf and upper sublittoral | 1 | 1 | Azore, Canary, St Helena |
| Ceramium diaphanum (Lightfoot) Roth | 1 | 1 | A / C | turf and sublittoral rocks | 1 | 1 | Ascension, St Helena, Canary, Azores, Caribbean |
| Ceramium luetzelburgii O.C.Schmidt | 1 | 0 | E / L | turf and sublittoral rocks | 1 | 1 | Caribbean (Martinica) |
| Ceramium tenerrimum (G.Martens) Okamura | 0 | 1 | PN | turf and upper sublittoral | 0 | 1 | Cape Verde, Ascencion, Canary |
| Champia minuscula A.B.Joly & Ugadim | 1 | 0 | E / F / PO | sublittoral rocks | 1 | 1 | Caribbean |
| Chondracanthus acicularis (Roth) Fredericq | 0 | 1 | C | turf | 1 | 1 | Azores, Canary, Caribbean |
| Grateloupia cf. filicina (J.V.Lamouroux) C.Agardh | 1 | 1 | C / N / F / PN | upper sublittoral | 0 | 1 | Azores, Canary, St Helena, C Verde, Caribbean |
| Halymenia vinacea M.Howe & W.R.Taylor | 0 | 1 | O | sublittoral | 1 | 1 | Canary |
| Hildenbrandia rubra (Sommerfelt) Meneghini | 1 | 1 | E | mid till upper sublittoral | 1 | 1 | Ascension, Canary, Caribbean |
| Hydrolithon cf. farinosum (J.V.Lamouroux) Penrose & Chamberlain | 0 | 1 | L / O | sublittoral | 0 | 1 | Ascension, St Hel., Azores, Canary, C Verde, Caribbean |
| Jania capillacea Harvey | 0 | 1 | A | turf, mid and upper subl. | 1 | 1 | Ascension, Azores, Canary, St Hel., C Verde, Caribbean |
| Jania pumila J.V.Lamouroux | 1 | 1 | A | turf and upper subl. | 1 | 1 | Ascension, Azores, Canary, St Hel., C Verde, Caribbean |
| Lithophyllum prototypum (Foslie) Foslie | 1 | 1 | C | sublittoral | 1 | 1 | Caribbean |
| Melanothamnus tongatensis (Harvey ex Kutz.) Diaz-Tapia & Maggs | 1 | 1 | A/C/E/P | turf and upper subl. | 0 | 0 | Bermudas, Panama |
| Melyvonnea erubescens (Foslie) Athanasiadis & Ballantine | 1 | 1 | E | sublittoral | 1 | 1 | Caribbean, Canary, Cape verde |
| Palisada perforata (Bory) K.W.Nam | 1 | 1 | A / PN | mid-turf, upper subl. | 1 | 1 | Ascencion, Canary, Bermudas |
| Peyssonnelia sp. | 1 | 1 | C / E | mid, upper subl. | 1 | 1 | Canary, C Verde, Caribbean |
| Polysiphonia sertularioides (Grateloup) J.Agardh | 1 | 0 | A / E / P | mid-turf, upper subl. | 0 | 0 | Canary, Caribbean isls. |
| Pterocladiella sanctarum (Feldmann & Hamel) Santelices | 1 | 1 | L / PN | mid-turf, upper subl. | 0 | 1 | Caribbean isls. |
| Taenioma perpusillum (J.Agardh) J.Agardh | 1 | 1 | A | turf | 0 | 1 | Azores, Canary, C Verde, Caribbean |
| Vertebrata foetidissima (Cocks ex Bornet) Diaz-Tapia & Maggs | 1 | 1 | A/C | mid-turf, upper subl. | 0 | 0 | Azores, Caribbean, C Verde |
| Total 25 | 20 | 21 | |||||
|
The new seaweed records from Trindade indicate higher richness of Phaeophyceae and Cyanobacteria in summer and of Chlorophyta and Rhodophyta in winter, although no significant difference was observed between the summer and winter cruises (Fig. 5). Of Rhodophyta, 5 taxa were restricted to the winter, 4 were restricted to the summer and 16 were common to the summer and winter. Of Chlorophyta, 6 taxa were restricted to the winter, 4 were restricted to the summer, and 16 were common to the summer and winter. Finally, of Phaeophyceae, 1 species was restricted to the winter, 3 species were restricted to the summer, and 5 were common to the summer and winter.
Table 1 describes the presence (1) and absence (0) of new benthic macroalgae records from Trindade in summer and winter and the occurrence and habitat of each taxon along the southern (S) and northern (N) Trindade beaches: S (A, Andradas [20°30′37″S, 29°18′30″W]; T, Tartarugas [20°31′02″S 29°18′17″W]; P, Parcel [20°31′17″S 29°18′06″W]; PR, Príncipe [20°31′10″S 29°18′44″W]; L, Lixo [20°31′23″S 29°19′30″W]; F, Farilhões [20°31′32″S 29°19′49″W]); and N (E, Eme [20°30′49″S 29°20′22″W]; C, Calheta [20°30′29″S 29°18′41″W]; PO, Portugueses [20°30′21″S 29°19′01″W]; CA, Cabritas [20°29′38″S 29°19′51″W]; O, Orelhas [20°29′38″S 29°20′30″W]; PN, Ponta Norte [20°29′13″S 29°20′17″W]; N, Noroeste [20°30′18″S 29°20′36″W]). A comparative list of taxa occurrence is presented for the Brazilian coast, another Brazilian oceanic island and Caribbean, North Atlantic and South Atlantic Islands. In Table 1, a genus with no species ID refers to a genus that was not previously recorded for Trindade. In addition, a complementary checklist of species cited in previous studies and sampled in the present report is presented as supplementary material.
In general, considering the total richness and taxa diversity from Trindade, the most representative macroalgae group was Rhodophyta, represented by 24 families, dominated by Rhodomelaceae, Ceramiaceae and Corallinaceae. Calcareous, crustose, and branched specimens and conforming turf beds (tangled with Ceramiales and Bryopsidales, over-branched calcareous specimens) were dominant in Trindade. Rhodophyta was composed of 22% calcareous algae (Corallinaceae and Hapalidiaceae), forming rhodolith beds. Chlorophyta comprised 16 families, mainly dominated by Cladophoraceae, Caulerpaceae and Ulvaceae. Eleven families represented Phaeophyceae, with Dictyotaceae as the most representative (Supplementary material Fig. S1).
Cyanobacteria constituted 100% of the new records for the island and 13% of the total richness. Of these, 9 taxa were exclusive to the summer, 3 were exclusive to the winter, and 8 were common to both summer and winter (Supplementary material Table S1, Fig. 5). Filamentous cyanobacteria represented 11 families, dominated by Oscillatoriaceae and Nostocaceae.
Considering the total richness of Rhodophyta, Chlorophyta and Phaeophyceae, a cluster of similarity (Fig. 6) was formed with the populations from the south and north faces, showing ca. 78% similarity.
|
Considering the abiotic data measured during the samplings (Table 2), higher temperatures salinities and UV max were recorded during the summer. The temperature ranges on the south face were 22.0±2.2°C and 27.5±2.0°C in winter and summer, respectively; those on the north face were 22.8±1.0°C to 27.8±1.0°C. The salinity on the south face ranged from 36.5±3.0 to 39.5±1.5 psu in winter and summer, respectively; that on the north face varied from 37.0±2.0 to 38.0±2.0. The pH showed higher values in summer (8.3±0.3) than in winter (8.2±0.5).
Table 2. – Abiotic data (Mean±SD) monitored in situ from Trindade Island (Southern Brazil, South-Western Atlantic), during the summer and winter cruises in 2014 and 2015, comparing the south and north faces.
| Trindade island (BR) | South Summer/Autumn | South Winter/Spring | North Summer/Autumn | North Winter/Spring |
|---|---|---|---|---|
| Sea Surface Temperature (°C) | 27.5±2 | 22±2.2 | 27.8±1 | 22.8±1 |
| Salinity (psu) | 39.5±1.5 | 36.5±3 | 38±2 | 37±2 |
| pH | 8.3±0.3 | 8.2±0.2 | 8.3±0.1 | 8.2±0.3 |
| Wind Speed (km/h) | 6±2 | 11±3 | 6±2 | 11±3 |
| Precipitation (mm) | 40±20 | 150±50 | 40±20 | 150±50 |
| UV Max | 8±2 | 5±1 | 9±1 | 6±1 |
Minimum monthly rainfall values were recorded in spring/summer and maximum values in autumn/winter. UV radiation (more shaded) was 5±1 in winter and 8±2 in summer on the south face, compared with 6±1 in winter and 9±1 in summer on the north face. The seasonal differences between the north and south faces were not significant (p=0.74). Principal component analysis was performed using abiotic and richness data, but no exclusive factor was found to clearly influence the diversity.
DISCUSSIONTop
New records, taxonomic status and perspectives
The mid- and shallow sublittoral zones and the algal turfs from Trindade Island had never been extensively and seasonally sampled before, and the present study resulted in a significant increase in new records (approximately 35%). The greatest contribution is that of the 60 new records of seaweeds, representing an advancement in the understanding of Trindade macroalgae assemblages and suggesting the island as a candidate for a hotspot in the southwestern Atlantic (Table 1 and S1).
The present study recorded 141 species of macroalgae. According to Villaça et al. (2006)Villaça R., Pedrini A., Pereira S., et al. 2006. Flora marinha bentônica das ilhas oceânicas brasileiras, In: Alves R., Castro J. (eds), Ilhas Oceânicas Brasileiras Da Pesquisa Ao Manejo. Ministério do meio ambiente, Brasilia, pp. 105-146., 13 taxa from the sublittoral zone (Chaetomorpha nodosa Kützing, Codium decorticatum Woodward, Chamaedoris peniculum (J. Ellis & Solander) Kuntze, Siphonocladus tropicus (P. Crouan & H. Crouan) J. Agardh, Caulerpa mexicana Sonder ex Kützing, C. prolifera (Roth) Kützing, Avrainvillea nigricans Decaisne, Halimeda incrassata (J. Ellis) J.V. Lamouroux, Rhipilia sp., Arthrocardia flabellata Kützing (Manza), Liagora ceranoides J.V. Lamouroux, Ceramium comptum Borgesen, Bryocladia thyrsigera (J. Agardh) F. Schmitz) were not identified here. In addition, Pereira-Filho et al. (2011)Pereira-Filho G.H., Amado-Filho G.M., Guimarães S.M.P.B., et al. 2011. Reef fish and benthic assemblages of the Trindade and Martin Vaz island group, SouthWestern Atlantic. Brazilian J. Oceanogr. 59: 201-212. added another 6 new occurrences to the list, also not recorded in our survey (Champia parvula (C. Agardh) Harvey, Dasya brasiliensis Oliveira Filho & Braga, Heterosiphonia crassipes (Harvey) Falkenberg, Porolithon onkodes (Heydrich) Foslie, Phymatolithon masonianum Wilks & Woelkerling, and Spongites sp.), the last three species being Corallinales, also from subtidal zone. Thus, the seaweed richness of Trindade comprises 160 species (Table S1, previous listed species). Reviewing the species found by previous studies but absent in ours, we may hypothesize some explanations: 1) the deeper subtidal was not our sampling zone focus; 2) some of these species may have been misidentified in the previous study; or 3) some species are becoming rare, with potential for local extinction.
Considering the last hypothesis, Dasya brasiliensis, an endemic species described from Brazil, had the last citation by Moura et al. (2015)Moura C.W.N., Alves A.M., Santos A.A., et al. 2015. Checklist of phytobenthos from Boipeba Island, Bahia, Brazil, emphasizing the morphological features of Nitophyllum pinctatum (Rhodophyta, Ceramiales). Check List 11: 1704.. Bryocladia thyrsigera and Arthrocardia flabelatta seem to be becoming rare. B. thyrsigera, an Atlantic species, was last listed in Brazil by Pellizzari et al. (2014)Pellizzari F.M., Bernardi J., Silva E.M., et al. 2014. Benthic marine algae from the insular areas of Paraná, Brazil: new database to support the conservation of marine ecosystems. Biota Neotropica 14: e20130011., and A. flabellata, previously listed from South America and Africa, was last cited by Silva et al. (1996)Silva P.C., Basson P.W., Moe R.L. 1996. Catalogue of the Benthic Marine Algae of the Indian Ocean. University of California Press.. Regarding Spongites, few valid species remain globally in the genus, and in Brazil the only record was for Trindade (Pereira-Filho et al. 2011Pereira-Filho G.H., Amado-Filho G.M., Guimarães S.M.P.B., et al. 2011. Reef fish and benthic assemblages of the Trindade and Martin Vaz island group, SouthWestern Atlantic. Brazilian J. Oceanogr. 59: 201-212.). The other two Corallinales species mentioned were recently cited from Bahia, NE Brazil (Jesionek et al. 2016Jesionek M.B., Bahia R.G., Hernández-Kantún J., et al. 2016. A taxonomic account of non-geniculate coralline algae (Corallinophycidae, Rhodophyta) from shallow reefs of the Abrolhos Bank, Brazil. Algae 31: 317-340., Costa Jr. et al. 2002Costa Jr. O.S., Attrill M.J., Pedrini A.G., et al. 2002. Spatial and seasonal distribution of seaweeds on coral reefs from Southern Bahia, Brazil. Bot. Mar. 45: 346-355.). Most of the green species mentioned are conspicuous in subtidal tropical and subtropical zones.
Climate change is inducing shifts in species ranges across the globe and monitoring them is crucial. Straub et al. (2019)Straub S.C, Wernberg T, Thomsen M.S., et al. 2019. Resistance, Extinction, and Everything in Between - The Diverse Responses of Seaweeds to Marine Heatwaves. Front. Mar. Sci. 6: 763. argue that the “marine heatwaves” have been associated to changes in primary productivity, community composition and biogeography of seaweeds, which control ecosystem function and services. The authors compiled several observations related to resistance, bleaching, changes in abundance, species invasions and local to regional extinctions. More records existed for canopy-forming kelps, bladed and filamentous turf-forming seaweeds than for canopy-forming fucoids, geniculate coralline turf and crustose coralline algae. Turf-forming seaweeds, especially invasive seaweeds, generally increased in abundance after a marine heat wave, whereas native canopy-forming typically declined in abundance. In contrast, Buonomo et al. (2018)Buonomo R., Chefaouib R.M., Lacidac R.B., et al. 2018. Predicted extinction of unique genetic diversity in marine forests of Cystoseira spp. Mar. Environ. Res. 138: 119-128. announced the predicted extinction of unique genetic diversity in marine forests of Cystoseira spp. in the Mediterranean Sea, whose habitats are becoming more limited. Thomsen et al. (2019)Thomsen M.S., Mondardini L., Alestra T., et al. 2019. Local Extinction of Bull Kelp (Durvillaea spp.) Due to a Marine Heatwave. Front. Mar. Sci. 6: 84. also report local extinction of bull kelp (Durvillaea spp.) due to a marine heatwaves.
Marine vegetational habitats are the most sensitive descriptors for assessing environmental changes. Porzio and Buia (2020)Porzio L., Buia M.C. 2020. Long-term changes (1800-2019) in marine vegetational habitats: Insights from a historic industrialised coastal area. Mar. Environ. Res. (preproof). detected a severe loss of Fucales and seagrass meadows in the Gulf of Pozzuoli (Italy), demonstrating that human-made coastline seems to be the leading cause of vegetational habitat regression. Gorman et al. (2019)Gorman D., Horta P., Flores A.V., et al. 2019. Decadal losses of canopy-forming algae along the warm temperate coastline of Brazil. Global Change Biol. 26: 1446-1457. report decadal losses of canopy-forming algae along 1000 km of Brazilian coast, using meta-analysis to examine long-term changes (a time span of 48 years) in the cover and biomass of Sargassum spp. The authors revealed major declines independent of seasons, suggesting overall losses of 52%, particularly at sites exhibiting the greatest degree of coastal warming and the highest population and those located in semi-enclosed sheltered bays. In addition, the authors also observed enhance of turf-forming assemblages (filamentous and articulated coralline).
In contrast to data reported for other global coastal areas, species rarity, reduction and replacement of biomass, local extinctions or the predominance/substitution of specific groups of macroalgae has not yet been observed in Trindade, a remote and uninhabited island. Coastal and insular ecosystems show different mechanisms for responding to impacts, mainly because in insular oceanic areas turf forms the main natural assemblages due to oligotrophic conditions, and its biomass is not a suitable indicator of changes in these areas, particularly if it is used isolated. However, because of lower direct anthropogenic impacts they suffer, remote islands are key indicators of meteorological and oceanographic changes.
The higher richness observed in our study, compared with previous ones (summarized in Villaça et al. 2006Villaça R., Pedrini A., Pereira S., et al. 2006. Flora marinha bentônica das ilhas oceânicas brasileiras, In: Alves R., Castro J. (eds), Ilhas Oceânicas Brasileiras Da Pesquisa Ao Manejo. Ministério do meio ambiente, Brasilia, pp. 105-146. ), is primarily associated with our sampling effort focused along the intertidal and shallow subtidal zones (different from previous studies); and for the fact that our data were obtained seasonally on several Trindade beaches, being the first spatio-temporal assessment for the island. Previous studies obtained mainly dredged samples from greater depths, which is a destructive method and may have resulted in underestimated results and in an unspecified area (Pedrini et al. 1989Pedrini A.G., Gonçalves J.E.A., Fonseca M.C.S., et al. 1989. A Survey of the Marine Algae of Trindade Island, Brazil. Bot. Mar. 32: 97-99., Yoneshigue-Valentin et al. 2005Yoneshigue-Valentin Y., Fernandaes D.P., Pereira C.B., et al. 2005. Macroalgas da Plataforma Continental da Ilha da Trindade e Martin Vaz (Brasil). Conference paper X Reunião Brasileira de Ficologia. Série Livros 10, Museu Nacional.).
The low standardization and randomness of the past samplings may have played a role in the observation of higher richness in this study. In addition, the majority of the new records were small and inconspicuous specimens from algal turf, whose presence may have gone unnoticed until the current implementation of large-scale sampling.
Molecular data are essential for current taxonomical approaches, especially for cryptic seaweed species (including cyanobacteria), and their lack may lead to an underestimation of species richness. However, in some specific cases such as the present study, classical morphological taxonomy may not be considered an inconsistent tool, particularly due to the difficulty of isolating sufficient unialgal material from the entangled turf assemblage in a low-resource laboratory on the island (Fig. 3). Furthermore, a posteriori in vitro culture of the target specimens on return from the island would be necessary to obtain sufficient cryptic material for molecular analysis. However, cryptic species culture is not always successful and may represent difficulties in studying turf assemblages. As an example of current diversity issues, Hildenbrandia rubra has over 70 genetic groups sampled in the Northern Hemisphere attributable to this morphological species (Mathieson and Dawes 2017Mathieson A.C., Dawes J.C. 2017. Seaweeds of the Northwest Atlantic. Univ. of Massachusetts Press. 798 pp.). The morphological identities are a conundrum, even to taxonomic experts who grasp what species are present and taxonomically valid. However, the focus on non-conspicuous or cryptic species is due to several introduction events and the progression of the exogenous species, which has thus far been undetected owing to its morphological similarities with conspicuous and native species. For this reason, continuous monitoring is fundamental, and classic morphological-assisted studies are essential because of their low cost, particularly where higher richness is prevalent, and because of the difficulty of sampling monospecific specimens from complex macroalgae assemblages such as turfs. Moreover, only a few groups of global diversity are considered cryptic and should be the target of molecular studies, providing reliability and satisfying the demand for morphological identification.
The richness of Chlorophyta in Trindade surpasses that of any other oceanic island in the Atlantic. In the present survey, 9 species of Cladophora were identified. Miranda-Alves (2015)Miranda-Alves A. 2015. O Gênero Cladophora (Chlorophyta) no Litoral do Brasil: Estudos morfotaxonômico e molecular. PhD thesis. Univers. Estadual de Feira de Santana (Bahia). 290 pp. identified 22 Cladophoraceae species in the coast of Brazil, 19 species of Cladophora and 3 species of Willeella. This molecular study identified new records that need to be described: C. coelothrix of Brazil (nom. prov.) and C. laetevirens of Brazil (nom. prov.), C. prolifera of Brazil (nom. prov.), C. rupestris of Brazil (nom. prov.), and another 3 species of Cladophora (named sp. 2 to sp. 4). The author mentions that morphological characteristics confirmed only five species on the Brazilian coast: C. brasiliana, C. corallicola, C. sericea, C. socialis, and C. vagabunda. Based on these results, the need for further molecular studies to better understand the phylogenetic relationships of the group became evident. Our research team is currently studying cryptic Chlorophyta from the southern Atlantic oceanic islands in detail.
Specimens of Prasiolales were also identified in Trindade. Although its distribution is concentrated in temperate and polar eutrophic waters, and it is considered cryptic, Prasiola sp. associated with other benthic macroalgae in salt lagoons from Venice (Italy, Mediterranean Sea) was reported to occur by Miotti et al. (2005)Miotti C., Curiel D., Rismondo A., et al. 2005. First report of a species of Prasiola (Chlorophyta: Prasiolaceae) from the Mediterranean Sea (Lagoon of Venice). Sci. Mar. 69: 343-346.. This suggests the need for a molecular investigation of this group in the Atlantic Ocean islands, owing to the possibility of geographical distribution expansion to warmer areas and/or introduction. Cryptic species among seaweed groups have been reported in several molecular studies: Hesperophycus and Pelvetiopsis (Neiva et al. 2017Neiva J., Serrão E.A., Anderson L., et al. 2017. Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweeds. Evol. Biol. 17: 30.); Colpomenia sinuosa (Lee et al. 2013Lee K.M., Boo S.M., Kain (Jones) J.M., et al. 2013. Cryptic diversity and biogeography of the widespread brown alga Colpomenia sinuosa (Ectocarpales, Phaeophyceae). Bot. Mar. 56: 15-25.); and Polysiphonia morrowii (Geoffroy et al. 2012Geoffroy A., Gall L.L., Destombe C. 2012. Cryptic introduction of the red alga Polysiphonia morrowii Harvey (Rhodomelaceae, Rhodophyta) in the North Atlantic Ocean highlighted by a DNA barcoding approach. Aquat. Bot. 100: 67-71.). In addition, Saunders et al. (2019)Saunders G.W., Brooks C.M., Scott S. 2019. Preliminary DNA barcode report on the marine red algae (Rhodophyta) from the British Overseas Territory of Tristan da Cunha. Cryptogam. Algol. 40: 105-117., using a DNA barcode, studied Rhodophyta diversity from Tristan da Cunha. Ceramium secundatum, Colaconema caespitosum, Helminthocladia calvadosii and Porphyra mumfordii were suggested as species that increased their biogeographic distribution, probably because of human activity.
Halymenia vinacea and Grateloupia cf. filicina are also new records for Trindade. Azevedo (2016)Azevedo C. 2016. Diversidade e Filogenia da Ordem Halymeniales (Rhodophyta) no litoral do Brasil. PhD thesis. Instituto de Biociências da Universidade de São Paulo. Departamento de Botânica. 217 pp., studying the phylogeny of Halymeniales from the Brazilian coast, stated that the taxonomy of the group is problematic, possibly including misidentifications. The author demonstrated the existence of wide cryptic and pseudo-cryptic diversity, as well as novel species and genera, and revealed the presence of non-native Rhodophyta. The rare and delicate new turf records of Melanothamnus tongatensis, Polysiphonia sertularioides and Vertebrata foetidissima are not just limited to the Brazilian coast but occur widely in the Canary, Azores and Cape Verde islands and in the Caribbean Sea, which also suggests the extension of their geographical distribution to Trindade.
Oliveira et al. (2009)Oliveira V.P, Fernandes D.R.P., Figueiredo N.M., et al. 2009. Four new additions to the marine flora of Fernando de Noronha Archipelago, tropical western South Atlantic Ocean. Checklist 5: 210-215. listed the new occurrence of Blidingia marginata, Halimeda gracilis, Dictyota caribaea and Sargassum hystrix var. buxifolium to Fernando de Noronha Archipelago, which not only represents new additions to the area but also demonstrates a geographical distribution extension of the species to the tropical SW Atlantic Ocean.
Only a single species of Sargassum was recorded to Trindade, S. vulgare v. nanum, not conspicuous on the island. The lack of other Fucales and the common presence of Dictyotales coincide with a recent massive dispersion of benthic algae off Trindade and on the Brazilian coast. According to Sissini et al. (2017b)Sissini M.N., Barreto M.B.B., Szechy M.T.M., et al. 2017b. The floating Sargassum (Phaeophyceae) of the South Atlantic Ocean - likely scenarios. Phycologia 56: 321-328., the floating Sargassum biomass that reached the northern Brazilian coast and Fernando de Noronha archipelago in 2014 and 2015 (peaking 98 kg m–2 wet weight) was molecularly identified as Sargassum natans and S. fluitans. Satellite images did not support the hypothesis of slicks moving south from the Sargasso Sea (northern Atlantic Ocean). The author discussed that there is probably a matrix of holopelagic Sargassum in the central Atlantic Ocean, and biomass accumulation should be considered the result of the combination of physico-chemical seawater conditions and biological interactions, as well as environmental stress. Meanwhile, these floating islands are a fundamental element of the biogeography and macroecology of tropical environments, which may provide connectivity among the marine biodiversity from Atlantic reef environments by transporting associated phycoflora and fauna to other areas, including remote islands.
Regarding cyanobacteria, in Brazil, there is only one thesis published specifically for marine filamentous cyanobacteria (Crispino 2007Crispino L.M.B. 2007. Benthic marine Cyanobacteria from the coast of São Paulo. PhD thesis, Instituto de Botânica da Secretaria de Estado do Meio Ambiente. São Paulo, Brasil. 154 pp.), with sporadic references to the Noronha and Abrolhos archipelagos. In this study, which presents the first checklist for remote areas in the southern Atlantic, 20 taxa (9 genera and 11 species) of filamentous cyanobacteria were identified permeating the turf. These organisms inhabit diversified and extreme environments and may indicate environmental changes (Crispino and Sant’Anna 2006Crispino L.M.B., Sant’anna C.L. 2006. Cianobactérias marinhas bentônicas de ilhas costeiras do Estado de São Paulo, Brasil. Rev. Bras. Bot. 29.). Following Sangil et al. (2012)Sangil C., Sansón M., Afonso-Carillo J., et al. 2012. Changes in sub-tidal assemblages in a scenario of warming: proliferations of ephemeral benthic algae in the Canary Islands (eastern Atlantic Ocean). Mar. Environ. Res. 77: 120-128., cyanobacteria can be opportunistic where seawater warming has taken place, and a higher biomass of cyanobacteria was also documented in the shallow waters of Puerto Rico, Caribbean Sea (Stielow and Ballantine 2003Stielow S., Ballantine D.L. 2003. Benthic cyanobacterial, Microcoleus lyngbyaceus, blooms in shallow, inshore Puerto Rican seagrass habitats, Caribbean sea. Harmful Algae 2: 127-133.).
Considering the new seaweed records for Trindade and the establishment of an updated taxonomic database, this study recommends possible cryptic groups as the target for further molecular studies aiming to elucidate new trends in macroalgae dispersion patterns due to thermohaline and ocean current changes.
Higher richness vs. abiotic changes: bridging or introductions?
An increase in the area of biogeographic distribution of a given species and new occurrences of species or algal groups that had not previously been reported for a given area have been largely associated with the current environmental changes. There is a large focus on the effects of higher SST and concurrent distributional shifts of seaweed assemblages, and several studies suggest large-scale meteorological and oceanographic changes as a potential driver of biota changes (Sangil et al. 2012Sangil C., Sansón M., Afonso-Carillo J., et al. 2012. Changes in sub-tidal assemblages in a scenario of warming: proliferations of ephemeral benthic algae in the Canary Islands (eastern Atlantic Ocean). Mar. Environ. Res. 77: 120-128., Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685.).
The local abiotic data sampled in Trindade Island are not sufficient to support short-term thermohaline changes (Table 2) or significant differences between data from the south and north faces of the island. However, on the basis of historical data (Fig. 2), temperature and salinity seem to be dynamic parameters in the surroundings of Trindade. These trends may be consequences of a complex oceanic circulation in the area (Fig. 1), but it is also noteworthy that recent thermohaline anomalies (2017) might have long-term effects on the seaweed assemblages in Trindade.
Our data showed a high Chlorophyta richness among the southern Atlantic islands. This opportunistic group deserves attention as a bioindicator of changes. Similarly, Afonso-Carrillo et al. (2007)Afonso-Carrillo J., Sansón M., Sangil C., et al. 2007. New records of benthic marine algae from the Canary Islands (eastern Atlantic Ocean): morphology, taxonomy and distribution. Bot. Mar. 50: 119-127. reported that a subtidal algae bed in the Canary Islands has undergone changes, indicated by the proliferation of the ephemeral green algae Pseudotetraspora marina, a recent and probably introduced species reported for the eastern Atlantic Ocean. Sangil et al. (2012)Sangil C., Sansón M., Afonso-Carillo J., et al. 2012. Changes in sub-tidal assemblages in a scenario of warming: proliferations of ephemeral benthic algae in the Canary Islands (eastern Atlantic Ocean). Mar. Environ. Res. 77: 120-128. associated the shifts in the distribution and biomass of ephemeral species with the 2°C warming in the SST resulting from the weakening of the cold Canary current.
In addition, some new records listed in Trindade include potential cryptogenic species (of unknown origin), such as Feldmannia indica, Dictyota jamaicensis, Melanothamnus tongatensis and Parviphycus trinitatensis. Meanwhile, F. indica is widespread in warmer seas (Guiry and Guiry 2020Guiry M.D., Guiry G.M. 2020. AlgaeBase. World-wide electronic publication at http://www.algaebase.org) and, according to Tronholm et al. (2013)Tronholm A., Afonso-Carrillo J., Sansón M., et al. 2013. Taxonomy of the Dictyota ciliolata-crenulata complex (Dictyotales, Phaeophyceae), Phycologia 52: 171-181., Dictyota jamaicensis has been reinstated as an amphi-Atlantic species (Caribbean-Brazil-Cape Verde/Africa), suggesting that the new record for Trindade may also “bridge” this distribution.
Overall, a greater similarity of Trindade seaweed assemblages (Table 3) to phycoflora of Ascension (Tsiamis et al. 2014Tsiamis K., Peters A.F., Shewring D.M., et al. 2014. Marine benthic algal flora of Ascension Island, South Atlantic. J. Mar. Biol. Assoc. UK 97: 681-688.) and to those of other Brazilian oceanic islands, i.e. those between latitudes 27-29°N and 20-21°S, was observed. Some similarities to assemblages from areas of higher latitudes in the Northern Hemisphere (such as the Azores and Cape Verde islands) were also observed. However, poor similarity to assemblages from islands of the Southern Hemisphere (Gough and Tristan da Cunha) was observed. Despite the need for confirmation by population and biogeographic genetics studies, the thesis that Trindade seaweed diversity has been irradiated from the Caribbean Sea is supported. In addition, considering the current environmental changes, the connectivity between these areas previously considered remote is increasing.
Table 3. – Comparison of studies from the southern Atlantic oceanic islands, considering macroalgae richness by groups (Rhodophyta, Phaeophyceae and Chlorophyta).
In addition to temperature and salinity, pH values were the abiotic data that most differed from the standard values for the surroundings of Trindade (expected range, 8.05-8.10; data source, research.noaa.gov/acidification). The observed pH was constant and homogeneous throughout Trindade (approximately 8.3), although higher than the expected range. Trindade exhibits high seaweed richness, but few species contribute to the total coverage. In some oceanic islands, rhodoliths and crustose calcareous algae may reach a biomass of approximately 70% (Brasileiro et al. 2016Brasileiro P.S., Pereira-Filho G.H., Bahia R.G., et al. 2016. Macroalgal composition and community structure of the largest rhodolith beds in the world. Mar. Biodivers. 46: 407-420.). The higher pH observed is probably related to the dominance of calcareous specimens, which may form an ‘alkaline ring’ surrounding the island, a biopredictor that can be interpreted as a positive anomaly in contrast with global trends of acidification and deserves further investigation.
Articulated calcareous algae (e.g. Jania and Amphiroa spp.) at Trindade constitute algae ‘turf’ mats, often the primary coverage of benthic biogenic oligotrophic habitats. In addition, calcareous crustose and rhodoliths establish extensive beds at the island. According to Sissini (2013)Sissini M.N. 2013. Hapalidiaceae (Corallinophycidae, Rhodophyta) no litoral brasileiro. Dissertação de mestrado. Centro de Ciências Biológicas, Universidade Federal de Santa Catarina. 147 pp., its calcareous algae are dominated by Mesophyllum erubescens, M. engelhartii, Mesophyllum sp. and Lithothamnion sp. Two new putative species are under investigation using molecular markers. Corallinaceae are among the oldest known rhodophyte fossils, and it would be surprising to find endemic species in Trindade in this family, particularly because of the relatively recent volcanic events at the island. In this survey, 3 encrusting species were identified and 10 were articulated. However, the identification of corallines from Brazil (Mesophyllum species in particular) is indeed in a poor state. Lithophyllum (Titanoderma) prototypum was identified at Trindade and also reported for Abrolhos Bank (Jesionek et al. 2016Jesionek M.B., Bahia R.G., Hernández-Kantún J., et al. 2016. A taxonomic account of non-geniculate coralline algae (Corallinophycidae, Rhodophyta) from shallow reefs of the Abrolhos Bank, Brazil. Algae 31: 317-340.). This species is not conspicuous at Trindade; it is restricted to a depth of 2-10 m and is generally sampled as a non-fertile single specimen. Further investigation is needed to solve this taxonomic impasse.
The seaweed richness of Trindade was underestimated, and the distributional limits of some new records are probably shifting, highlighting the importance of long-term monitoring of the Brazilian oceanic islands. The spatio-temporal differences and high richness of cyanobacteria and Chlorophyta demand further investigation to establish phylogenetic relationships and detailed correlations with the abiotic oscillations. In addition, the richness enhancement of a given group of organisms may appear at a first glance to be a positive aspect, but it may also be an indicator of change in an area with biogeographical isolation, especially when it is accompanied by low endemism.
Connectivity and low endemism: facing current environmental trends
The present data were permeated by the low endemism of seaweeds at Trindade Island. The interaction of distinct water masses (Fig. 1) results in a complex mosaic of physical and chemical seawater conditions, featuring the co-occurrence of tropical, subtropical and warm-temperate species. These data may also corroborate Trindade’s geological data. Pires et al. (2016)Pires G.L.C., Bongiolo E.M., Geraldes M.C., et al. 2016. New 40Ar/39Ar ages and revised 40K/40Ar* data from nephelinitic-phonolitic volcanic successions of the Trindade Island (South Atlantic Ocean). J. Volcanol. Geotherm. Res. 327: 531-538. report that the last volcanic phase occurred in post-glacial times, which would indicate the last activity to have occurred approximately 25000 years ago. These data may justify the low endemism reported in the phycoflora from Trindade, suggesting that the organisms may have successfully dispersed to Trindade and to Brazil from the Caribbean.
Biogeographic island models have emerged from the study of terrestrial organisms. Considering oceanic ecosystems, seaweeds may expand their distribution using “stepping-stones” and currents, with abiotic features similar to their origins providing more possibilities for speciation (Pinheiro et al. 2017Pinheiro H.T., Bernardi G., Simon T., et al. 2017. Island biogeography of marine organisms. Nature 549: 82-85.). Remote islands are natural laboratories for elucidating biotic changes. This list of new macroalgae records suggests that marine ecosystems respond to isolation differently than terrestrial organisms. The distribution of Trindade assemblages seems to reflect the complex circulation of the Subtropical Gyre, receiving influences from the Brazil, South Atlantic, and South Equatorial currents and vortices from the Agulhas Current and the Angola-Benguela Front (Sissini et al. 2017aSissini M.N., Oliveira M.C., Horta P.A., et al. 2017a. Macroalgas da Ilha da Trindade, in: PROTRINDADE: Programa de Pesquisas Científicas na Ilha Da Trindade - 10 Anos de Pesquisas. SECIRM, Brasilia, pp. 99-108.). Meanwhile, Trindade has been described as an ecotone (Horta et al. 2001Horta P.A., Amancio E., Coimbra C.S., et al. 2001. Considerations on the distribution and origin of the marine macroalgal Brazilian flora. Hoehnea 28: 243-265.), i.e. a transition area that, in theory, limits the beginning and end of populations of different origins. Our data suggest Trindade is a ‘transit’ zone, where low endemism may be a result of complex connectivity relationships. Moreover, this species transit is corroborated by algal species that are expanding their distribution limits from these areas previously considered “isolated”.
In recent decades, climate change has caused profound biological changes across the planet. However, there is a large disparity of data between hemispheres and a scarcity of studies using seaweeds as proxies (Pellizzari et al. 2017Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685., Santos-Silva et al. 2018Santos-Silva M.C., Machado E.C., Wallner-Kersanacha M., et al. 2018. Background levels of trace elements in brown and red seaweeds from Trindade, a remote island in South Atlantic Ocean. Mar. Poll. Bull. 135: 923-931.). Sorte et al. (2010)Sorte C.J.B., Williams S.L., Carlton J.T. 2010. Marine range shifts and species introductions: comparative spread rates and community impacts. Global Ecol. Biogeogr. 19: 303-316., Hoegh-Guldberg and Bruno (2010)Hoegh-Guldberg O., Bruno J.F. 2010. The impact of climate change on the world’s marine ecosystems. Science 328: 1523-1528., and Wernberg et al. (2011aWernberg T., Russell B.D., Thomsen M.S., et al. 2011a. Seaweed Communities in Retreat from Ocean Warming. Curr. Biol. 21:1828-1832., b)Wernberg T., Russell B.D., Moore P.J., et al. 2011b. Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J. Exp. Mar. Biol. Ecol. 400: 7-16. showed evidence of the rearrangement of entire communities rather than mere changes in individual species. Seaweed population changes can have severe impacts on the entire food web, and for this reason there is a major challenge in interpreting the results, including our data.
As summarized by Jueterbock et al. (2013)Jueterbock A., Tyberghein L., Verbruggen H., et al. 2013. Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecol. Evol. 3: 1356-1373., environmental changes may cause several impacts on seaweed populations: 1) distributional shifts; 2) higher herbivory pressure; 3) higher phenotypic plasticity and adaptive responses due to thermal change; 4) higher competitive interactions and habitat loss; and 5) changes in dispersion patterns and greater invasive potential. As already discussed by Pellizzari et al. (2017)Pellizzari F.M., Silva M.C., Medeiros A., et al. 2017. Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol. 40: 1671-1685. and Sanches et al. (2016)Sanches P.F., Pellizzari F.M., Horta P.A. 2016. Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Circumpolar Current. J. Sea Res. 110: 29-38. for Antarctic islands, it is possible that Trindade is also experiencing changes in macroalgal richness and distribution because of a new trend towards higher connectivity of areas previously considered biogeographically isolated. This study listed new records of non-endemic (including cryptic and cryptogenic) species, drawing attention to the effects of current abiotic changes and proposing an updated taxonomic baseline for future comparative studies in tropical areas.
According to Straub et al. (2019)Straub S.C, Wernberg T, Thomsen M.S., et al. 2019. Resistance, Extinction, and Everything in Between - The Diverse Responses of Seaweeds to Marine Heatwaves. Front. Mar. Sci. 6: 763., although a relatively small number of studies have described impacts of marine heat waves on seaweed, the broad range of documented responses highlights the necessity of better baseline information regarding seaweed distributions and performance, and the need to study specific parameters that affect the vulnerability and resilience of seaweeds to these increasing climatic perturbations. A major challenge will be to disentangle impacts from co-occurring potential stressors, including altered current patterns, increasing herbivory, changes in transparency and nutrient concentration, solar radiation and desiccation stress in the intertidal zone.
Trindade is an oceanic island that has the potential to facilitate the treatment of important biological issues. Further studies establishing a baseline for species diversity using molecular data would confirm information on new biogeographic issues facing current environmental changes. Moreover, several putative invasive species could also be confirmed. Considering that some regions of the islands are geologically young, endemism may also have been underestimated. Finally, Trindade may be an interesting model for studying transoceanic re-colonization pathways.
ACKNOWLEDGEMENTSTop
The authors thank the Brazilian Navy of the 1st Naval District and the Secretariat of the Interministerial Commission for Sea Resources (SECIRM), which provided logistical and operational support through the Coast Patrol Vessels. Special thanks are due to Commanders Costa-Abrantes and Felipe Santos, Trindade Island Research Programme (PROTRINDADE/SECIRM). Lorena Karvat, Camila Santos Pinto and Amanda Porrua are thanked for their sampling and technical efforts. Dr Nair Sumie Yokoya (Botanical Institute of São Paulo) is thanked for valuable comments that improved the manuscript. We are grateful to Fundação Araucária for research grants - process no. 947/2013 (UENP-UNESPAR) and 006/2016 ID 4113 (Project activity 4130.0001 UNESPAR). We would also like to thank Editage (http://www.editage.com) for English language editing.
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SUPPLEMENTARY MATERIAL
The following supplementary material is available through the online version of this article and at the following link:
http://scimar.icm.csic.es/scimar/supplm/sm05036esm.pdf
Table S1. – List of seaweed species already reported from Trindade Island, southwestern Atlantic, complementary to the new occurrences recorded in the present study.
Fig. S1. – Larger and conspicuous seaweeds that grow on top of the turf and rhodolith beds along the midlittoral and shallow sublittoral (A, Dictyotales; B, Caulerpa verticillata; C, Tribe Laurencieae). Scale = 1 cm.