Abstract
Coralline red algae (CRA) are key players in the construction and maintenance of biogenic reefs, and they have important functional roles in ecological systems in the Southwestern Atlantic (SWA). Like many other marine organisms, CRA are currently affected by global and local stressors, but little is known about their biodiversity and the environmental drivers that influence their distribution patterns in the SWA. In the present study, we quantified the species richness of CRA in six ecoregions within the SWA using DNA-based species delimitation methods. We then verified their distribution and identified the main drivers shaping the macroecological patterns of richness and β-diversity. We found 79 phylogenetic species that belong to the three main CRA orders (Sporolithales, Corallinales, and Hapalidiales), in the tropical and warm temperate SWA. Temperature, nutrients, and water current velocity were the main environmental drivers of CRAs in the evaluated ecoregions. The Eastern Brazil ecoregion stands out due to its high richness, exclusive species, β-diversity between ecoregions, and as a transitional zone of the SWA. The results of our study have several important practical implications with repercussions for monitoring actions and conservation planning for the coastal region. These results show that each ecoregion has unique characteristics, and the mesophotic habitat is of primary importance because it harbors species that are not found in other habitats, and because it provides structural connectivity with shallower habitats.
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References
Adey WH, Steneck RS (2001) Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae. J Phycol 698:677–698
Allen AP, Gillooly JF, Savage VM, Brown JH (2006) Kinetic effects of temperature on rates of genetic divergence and speciation. Proc Natl Acad Sci U S A 103:9130–9135
Amado-Filho GM, Maneveldt GW, Pereira-Filho GH, Manso RCC, Bahia RG, Barros-Barreto MB, Guimarães SMPB (2010) Seaweed diversity associated with a Brazilian tropical rhodolith bed | Diversidad de macroalgas asociada con un manto de rodolitos tropical de Brasil. Cienc Mar 36:371–391
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Assis J, Coelho NC, Lamy T, Valero M, Alberto F, Serrão EA (2016) Deep reefs are climatic refugia for genetic diversity of marine forests. J Biogeogr 43:833–844
Assis J, Tyberghein L, Bosch S, Verbruggen H, Serrão EA, de Clerck O (2018) Bio-ORACLE v2.0: extending marine data layers for bioclimatic modelling. Glob Ecol Biogeogr 27:277–284
Aued AW, Smith F, Quimbayo JP, Cândido DV, Longo GO, Ferreira CEL, Witman JD, Floeter SR, Segal B (2018) Large-scale patterns of benthic marine communities in the Brazilian province. PLoS ONE 13:1–15
Ayres-Ostrock LM, Valero M, Mauger S, Oliveira MC, Plastino EM, Guillemin ML, Destombe C (2019) Dual influence of terrestrial and marine historical processes on the phylogeography of the Brazilian intertidal red alga Gracilaria caudata. J Phycol 55:1096–1114
Bahia RG, Amado-Filho GM, Maneveldt GW, Adey WH, Johnson G, Marins BV, Longo LL (2014) Sporolithon tenue sp. nov. (Sporolithales, Corallinophycidae, Rhodophyta): a new rhodolith-forming species from the tropical southwestern Atlantic. Phycol Res 62:44–54
Bahia RG, Amado-Filho GM, Maneveldt GW, Adey WH, Johnson G, Jesionek MB, Longo LL (2015) Sporolithon yoneshigueae sp. nov. (Sporolithales, Corallinophycidae, Rhodophyta), a new rhodolith-forming coralline alga from the southwest Atlantic. Phytotaxa 224:140–158
Barbera C, Bordehore C, Borg JA, Glémarec M, Grall J, Hall-Spencer JM, Huz C, Lanfranco E, Lastra M, Moore PG, Mora J, Pita ME, Ramos-Esplá AA, Rizzo M, Sánchez-Mata A, Seva A, Schembri PJ, Valle C (2003) Conservation and management of northeast Atlantic and Mediterranean maërl beds. Aquat Conserv 13:S65–S76
Barroso CX, da Cruz Lotufo TM, Matthews-Cascon H (2016) Biogeography of Brazilian prosobranch gastropods and their Atlantic relationships. J Biogeogr 43:2477–2488
Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
Bettignies T, Wernberg T, Gurgel CFD (2018) Exploring the influence of temperature on aspects of the reproductive phenology of temperate seaweeds. Front Mar Sci 5:1–8
Bjork M, Mohammed SM, Bjorklund M, Semesi A (1995) Coralline algae, important coral-reef builders threatened by pollution. Ambio 24:502–505
Bonaldo RM, Hay ME (2014) Seaweed-coral interactions: variance in seaweed allelopathy, coral susceptibility, and potential effects on coral resilience. PLoS ONE 9:30–34
Briggs JC (1974) Marine zoogeography. McGraw-Hill, New York
Briggs JC (1995) Global biogeography. Elsevier, Amsterdam
Caldeira K, Wickett M (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:1–12
Carvalho VF, Assis J, Serrão EA, Nunes JM, Batista AA, Batista MB, Barufi JB, Silva J, Pereira SMB, Horta PA (2019) Environmental drivers of rhodolith beds and epiphytes community along the South Western Atlantic coast. Mar Environ Res 154:104827
Carvalho VF, Silva J, Anderson AB, Bastos EO, Cabral D, Gouvêa LP, Peres L, Martins CDL, Silveira-Andrade VM, Sissini MN, Horta PA (2020) When descriptive ecology meets physiology: a study in a South Atlantic rhodolith bed. J Mar Biol Assoc U K 100(3):1–14
Cheal AJ, MacNeil MA, Cripps E, Emslie MJ, Jonker M, Schaffelke B, Sweatman H (2010) Coral-macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29:1005–1015
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143
Costa GB, Ramlov F, de Ramos B, Koerich G, Gouvea L, Costa PG, Bianchini A, Maraschin M, Horta PA (2019a) Physiological damages of Sargassum cymosum and Hypnea pseudomusciformis exposed to trace metals from mining tailing. Environ Sci Pollut Res Int 26:36486–36498
Costa IO, Jesus PB, Jesus TDS, Souza PS, Horta PA, Castro Nunes JM (2019b) Reef-building coralline algae from the Southwest Atlantic: filling gaps with the recognition of Harveylithon (Corallinaceae, Rhodophyta) on the Brazilian coast. J Phycol 55:1370–1385
de Oliveira Soares M, Lucas CC (2018) Towards large and remote protected areas in the South Atlantic Ocean: St. Peter and St. Paul´s Archipelago and the Vitória-Trindade seamount chain. Mar Policy 93:101–103
de Cerqueira Veras P, Pierozzi-Jr I, Lino JB, Amado-Filho GM, de Senna AR, Santos CSG, de Moura RL, Passos FD, Giglio VJ, Pereira-Filho GH (2020) Drivers of biodiversity associated with rhodolith beds from euphotic and mesophotic zones: insights for management and conservation. Perspect Ecol Conserv 18:37–43
de Souza Tâmega FT, Perna GHH, Spotorno-Oliveira P, Riosmena-Rodríguez R, de Arruda Gonçalves JE (2017) A unique free-living geniculate coralline algal bed formation. Mar Biodivers 47:373–374
Delgado O, Lapointe BE (1994) Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13:151–159
Díaz S, Settele J, Brondízio ES, Ngo HT, Agard J, Arneth A, Balvanera P, Brauman KA, Butchart SHM, Chan KMA, Garibaldi LA, Ichii K, Liu J, Subramanian SM, Midgley GF, Miloslavich P, Molnár Z, Obura D, Pfaff A, Polasky S, Purvis A, Razzaque J, Reyers B, Chowdhury RR, Shin Y-J, Visseren-Hamakers I, Willis KJ, Zayas CN (2019) Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366:eaax3100
Diaz-Pulido G, Mccook LJ, Dove S, Berkelmans R, Roff G, David I, Weeks S, Evans RD, Williamson DH, Hoegh-guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PloS ONE 4:e5239
Ekman S (1953) Zoogeography of the Sea. Sidgwick and Jackson, London
Floeter SR, Behrens MD, Ferreira CEL, Paddack MJ, Horn MH (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Mar Biol 147:1435–1447
Floeter SR, Rocha LA, Robertson DR, Joyeux JC, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G (2008) Atlantic reef fish biogeography and evolution. J Biogeogr 35:22–47
Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850
Foster MS (2001) Rhodoliths: between rocks and soft places. J Phycol 37:659–667
Fragkopoulou E, Serrão EA, Horta PA, Koerich G, Assis J (2021) Bottom trawling threatens future climate refugia of rhodoliths globally. Front Mar Sci 7:1246
Fredericq S, Krayesky-Self S, Sauvage T, Richards J, Kittle R, Arakaki N, Hickerson E, Schmidt WE (2019) The critical importance of rhodoliths in the life cycle completion of both macro- and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Front Mar Sci 5:1–17
Gabrielson PW, Hughey JR, Diaz-Pulido G (2018) Genomics reveals abundant speciation in the coral reef building alga Porolithon onkodes (Corallinales, Rhodophyta). J Phycol 54:429–434
García D, Martínez D (2012) Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc R Soc B 279:3106–3113
Gherardi DFM, Bosence DWJ (2001) Composition and community structure of the coralline algal reefs from Atol das Rocas, South Atlantic, Brazil. Coral Reefs 19:205–219
Ghosh AK, Sarkar S (2013) Diversification of the family Sporolithaceae: a case of successful survival in the perspective of cretaceous-tertiary mass extinctions in India. Natl Acad Sci Lett 36:215–224
Gouvêa LP, Schubert N, Martins CDL, Sissini M, Ramlov F, de Oliveira Rodrigues ER, Bastos EO, Freire VC, Maraschin M, Carlos Simonassi J, Varela DA, Franco D, Cassano V, Fonseca AL, Barufi JB, Horta PA (2017) Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnol Oceanogr 62:2056–2075
Graham MH, Kinlan BP, Druehl LD, Garske LE, Banks S (2007) Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc Natl Acad Sci U S A 104:16576–16580
Grall J, Hall-Spencer JM (2003) Problems facing maërl conservation in Brittany. Aquat Conserv 13:S55–S64
Hall-Spencer JM, Moore PG (2000) Scallop dredging has profound, long-term impacts on maërl habitats. ICES J Mar Sci 57:1407–1415
Henriques MC, Coutinho LM, Riosmena-Rodríguez R, Barros-Barreto MB, Khader S, Figueiredo MAO (2014) Three deep water species of Sporolithon (Sporolithales, Rhodophyta) from the Brazilian continental shelf, with the description of Sporolithon elevatum sp. nov. Phytotaxa 190:320–330
Hernandez-Kantun JJ, Hall-Spencer JM, Grall J, Adey W, Rindi F, Maggs CA, Bárbara I, Peña V (2017) North Atlantic rhodolith beds. In: Riosmena-Rodríguez R, Nelson W, Aguirre J (eds) Rhodolith/maërl beds: a global perspective. Springer, Switzerland, pp 265–279
Holz VL, Bahia RG, Karez CS, Vieira FV, Moraes FC, Vale NF, Bastos AC (2020) Structure of rhodolith beds and surrounding habitats at the Doce River Shelf (Brazil). Diversity 12:75
Horta PA, Amancio E, Coimbra CS, Oliveira EC (2001) Considerações sobre a distribuição e origem da flora de macroalgas marinhas brasileiras. Hoehnea 28:243–265
Horta PA, Riul P, Amado Filho GM, Gurgel CFD, Berchez F, de Castro Nunes JM, Scherner F, Pereira S, Lotufo T, Peres L, Sissini M, de Oliveira Bastos E, Rosa J, Munoz P, Martins C, Gouvêa L, Carvalho V, Bergstrom E, Schubert N, Bahia RG, Rodrigues AC, Rörig L, Barufi JB, Figueiredo M (2016) Rhodoliths in Brazil: current knowledge and potential impacts of climate change. Braz J Oceanogr 64:117–136
Ichiki S, Mizuta H, Yamamoto H (2000) Effects of irradiance, water temperature and nutrients on the growth of sporelings of the crustose coralline alga Lithophyllum yessoense Foslie (Corallinales, Rhodophyceae). Phycol Res 48:115–120
Jesionek MB, Bahia RG, Hernandez-Kantun JJ, Adey WH, Yoneshigue-Valentin Y, Longo LL, Amado-Filho GM (2016) A taxonomic account of non-geniculate coralline algae (Corallinophycidae, rhodophyta) from shallow reefs of the Abrolhos bank, Brazil. Algae 31:317–340
Jesionek MB, Bahia RG, Lyra MB, Leão LAB, Oliveira MC, Amado-Filho GM (2020) Newly discovered coralline algae in Southeast Brazil: Tectolithon fluminense gen. et sp. nov. and Crustaphytum atlanticum sp. nov. (Hapalidiales, Rhodophyta). Phycologia 59:1–15
Kark S, Mukerji T, Safriel UN, Nissani R, Darvasi A (2002) Peak morphological diversity in an ecotone unveiled in the chukar partridge by a novel estimator in a dependent sample (EDS). J Anim Ecol 71:1015–1029
Kark S, Allnutt TF, Levin N, Manne LL, Williams PH (2007) The role of transitional areas as avian biodiversity centres. Glob Ecol Biogeogr 16:187–196
Keith SA, Kerswell AP, Connolly SR (2014) Global diversity of marine macroalgae: environmental conditions explain less variation in the tropics. Glob Ecol Biogeogr 23:517–529
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896
Leão ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 9–52
Leão ZMAN, Kikuchi RKP, Ferreira BP, Neves EG, Sovierzoski HH, Oliveira MDM, Maida M, Correia MD, Johnsson R (2016) Brazilian coral reefs in a period of global change: a synthesis. Braz J Oceanogr 64:97–116
Lim GS, Balke M, Meier R (2012) Determining species boundaries in a world full of rarity: singletons, species delimitation methods. Syst Biol 61:165–169
Lindner A, Cairns SD, Cunningham CW (2008) From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors. PLoS ONE 3:e2429
Littler MM, Arnold KE (1982) Primary productivity of marine macroalgal functional-form groups from south-western North America. J Phycol 18:307–311
Longo GO, Morais RA, Martins CDL, Mendes TC, Aued AW, Cândido DV, de Oliveira JC, Nunes LT, Fontoura L, Sissini MN, Teschima MM, Silva MB, Ramlov F, Gouvea LP, Ferreira CEL, Segal B, Horta PA, Floeter SR (2015) Between-habitat variation of benthic cover, reef fish assemblage and feeding pressure on the benthos at the only atoll in South Atlantic: Rocas atoll, NE Brazil. PLoS ONE 10:e0127176
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Ecology: biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808
Magris RA, Costa MDP, Ferreira CEL, Vilar CC, Joyeux J-C, Cred JC, Copertino MS, Horta PA, Sumida PYG, Francini-Filho RB, Floeter SR (2020) A blueprint for securing Brazil’s marine biodiversity and supporting the achievement of global conservation goals. Divers Distrib 27:198–215
Martins LR, Coutinho PN (1981) The Brazilian continental margin. Earth Sci Rev 17:87–107
Mazzuco ACA, Stelzer OS, Bernardino AF (2020) Substrate rugosity and temperature matters: patterns of benthic diversity at tropical intertidal reefs in the SW Atlantic. PeerJ 8:e8289
Mellin C, Mouillot D, Kulbicki M, McClanahan TR, Vigliola L, Bradshaw CJA, Brainard RE, Chabanet P, Edgar GJ, Fordham DA, Friedlander AM, Parravicini V, Sequeira AMM, Stuart-Smith RD, Wantiez L, Caley MJ (2016) Humans and seasonal climate variability threaten large-bodied coral reef fish with small ranges. Nat Commun 7:1–9
Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM, Bastos AC, Almeida MG, Silva JM, Araujo BF, Brito FP, Rangel TP, Oliveira BCV, Bahia RG, Paranhos RP, Dias RJS, Siegle E, Figueiredo AG, Pereira RC, Leal CV, Hajdu E, Asp NE, Gregoracci GB, Neumann-Leitão S, Yager PL, Francini-Filho RB, Fróes A, Campeão M, Silva BS, Moreira APB, Oliveira L, Soares AC, Araujo L, Oliveira NL, Teixeira JB, Valle RAB, Thompson CC, Rezende CE, Thompson FL (2016) An extensive reef system at the Amazon River mouth. Sci Adv 2:1–12
Moura RL, Abieri ML, Castro GM, Carlos-Júnior LA, Chiroque-Solano PM, Fernandes NC, Bastos AC (2021) Tropical rhodolith beds are a major and belittled reef fish habitat. Sci Rep 11:794
Mumby PJ (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28:761–773
Nauer F, Deluqui Gurgel CF, Ayres-Ostrock LM, Plastino EM, Oliveira MC (2019) Phylogeography of the Hypnea musciformis species complex (Gigartinales, Rhodophyta) with the recognition of cryptic species in the western Atlantic Ocean. J Phycol 55:676–687
Olson B, Richards J (1988) Spatial arrangement of tiller replacement in Agropyro desertorum following grazing. Oecologia 76:7–10
Paoli C, Morten A, Bianchi CN, Morri C, Fabiano M, Vassallo P (2016) Capturing ecological complexity: OCI, a novel combination of ecological indices as applied to benthic marine habitats. Ecol Indic 66:86–102
Pascelli C, Riul P, Riosmena-Rodríguez R, Scherner F, Nunes M, Hall-Spencer JM, de Oliveira EC, Horta P (2013) Seasonal and depth-driven changes in rhodolith bed structure and associated macroalgae off Arvoredo island (southeastern Brazil). Aquat Bot 111:62–65
Peña V, Vieira C, Braga JC, Aguirre J, Rösler A, Baele G, De Clerck O, Le Gall L (2020) Radiation of the coralline red algae (Corallinophycidae, Rhodophyta) crown group as inferred from a multilocus time-calibrated phylogeny. Mol Phylogenet Evol 150:106845
Pimenta FM, Campos EJD, Miller JL, Piola AR (2005) A numerical study of the Plata River plume along the southeastern South American continental shelf. Braz J Oceanogr 53:129–146
Pinheiro HT, Joyeux JC, Moura RL (2014) Reef oases in a seamount chain in the southwestern Atlantic. Coral Reefs 33:1113
Pinheiro HT, Rocha LA, Macieira RM, Carvalho-Filho A, Anderson AB, Bender MG, di Dario F, Ferreira CEL, Figueiredo-Filho J, Francini-Filho R, Gasparini JL, Joyeux JC, Luiz OJ, Mincarone MM, Moura RL, de Anchieta C C Nunes J, Quimbayo JP, Rosa RS, Sampaio CLS, Sazima I, Simon T, Vila-Nova DA, Floeter SR (2018) South-western Atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Divers Distrib 24:951–965
Pinheiro HT, Teixeira JB, Francini-Filho RB, Soares-Gomes A, Ferreira CEL, Rocha LA (2019) Hope and doubt for the world’s marine ecosystems. Perspect Ecol Conserv 17:19–25
Piola AR, Palma ED, Bianchi AA, Castro BM, Dottori M, Guerrero RA, Marrari M, Matano RP, Möller OO, Saraceno M (2018) Physical oceanography of the SW Atlantic shelf: a review. In: Hoffmeyer M, Sabatini M, Brandini F, Calliari D, Santinelli N (eds) Plankton ecology of the Southwestern Atlantic. Springer, Cham
Quimbayo JP, Dias MS, Kulbicki M, Mendes TC, Lamb RW, Johnson AF, Aburto-Oropeza O, Alvarado JJ, Bocos AA, Ferreira CEL, Garcia E, Luiz OJ, Mascareñas-Osorio I, Pinheiro HT, Rodriguez-Zaragoza F, Salas E, Zapata FA, Floeter SR (2019) Determinants of reef fish assemblages in tropical oceanic islands. Ecography 42:77–87
Riding R (2002) Structure and composition of organic reefs and carbonate mud mounds: concepts and categories. Earth Sci Rev 58:163–231
Rindi F, Braga JC, Martin S, Peña V, le Gall L, Caragnano A, Aguirre J (2019) Coralline algae in a changing mediterranean sea: how can we predict their future, if we do not know their present? Front Mar Sci 6:723
Riul P, Targino CH, Farias JDN, Visscher PT, Horta PA (2008) Decrease in Lithothamnion sp. (Rhodophyta) primary production due to the deposition of a thin sediment layer. J Mar Biol Assoc U K 88:17–19
Santos CSG, Lino JB, de Cerqueira VP, Amado-Filho GM, Francini-Filho RB, Motta FS, Pereira-Filho GH (2016) Environmental licensing on rhodolith beds: insights from a worm. Nat Conserv 14:137–141
Schubert N, Salazar VW, Rich WA, Vivanco Bercovich M, Almeida Saá AC, Fadigas SD, Silva J, Horta PA (2019) Rhodolith primary and carbonate production in a changing ocean: the interplay of warming and nutrients. Sci Total Environ 676:455–468
Simon T, Pinheiro HT, Moura RL, Carvalho-Filho A, Rocha LA, Martins AS, Mazzei E, Francini-Filho RB, Amado-Filho GM, Joyeux JC (2016) Mesophotic fishes of the Abrolhos Shelf, the largest reef ecosystem in the South Atlantic. J Fish Biol 89:990–1001
Sissini MN, Oliveira MC, Gabrielson PW, Robinson NM, Okolodkov YB, Rodríguez RR, Horta PA (2014) Mesophyllum erubescens (Corallinales, Rhodophyta)—so many species in one epithet. Phytotaxa 190:299–319
Sissini MN, Berchez F, Hall-Spencer J, Ghilardi-Lopes N, Carvalho VF, Schubert N, Koerich G, Diaz-Pulido G, Silva J, Serrão E, Assis J, Santos R, Floeter SR, Rörig L, Barufi JB, Bernardino AF, Francini-Filho R, Turra A, Hofmann LC, Aguirre J, le Gall L, Peña V, Nash MC, Rossi S, Soares M, Pereira-Filho G, Tâmega F, Horta PA (2020) Brazil oil spill response: protect rhodolith beds. Science 367:156
Smale DA, Burrows MT, Evans AJ, King N, Sayer MD, Yunnie AL, Moore PJ (2016) Linking environmental variables with regional-scale variability in ecological structure and standing stock of carbon within UK kelp forests. Mar Ecol Prog Ser 542:79–95
Smith TB, Wayne RK, Girman DJ, Bruford MW (1997) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857
Smith TB, Kark S, Schneider CJ, Wayne RK, Moritz C (2001) Biodiversity hotspots and beyond: the need for preserving environmental transitions. Trends Ecol Evol 16:431
Soares MO, Teixeira C, Bezerra LE, Paiva SV, Tavavres TCL, Garcia TM, Campos CC, Ferreira SMC, Matthews-Cascon H, Frota A, Mont'Alverne TCF, Silva ST, Rabelo EF, Barroso CX, Freitas JEP, Júnior MMM, Campelo RPS, Santana CS, Carneiro P, Meirelles AJ, Santos BA, Oliveira AHB, Horta P, Cavalcante RM (2020) Oil spill in South Atlantic (Brazil): environmental and governmental disaster. Mar Policy 115:103879
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583
Spotorno-Oliveira P, Figueiredo MAO, Tâmega FTS (2015) Coralline algae enhance the settlement of the vermetid gastropod Dendropoma irregulare (d’Orbigny, 1842) in the southwestern Atlantic. J Exp Mar Biol Ecol 471:137–145
Stramma L, England M (1999) On the water masses and mean circulation of the South Atlantic Ocean. J Geophys Res Oceans 104:20863–20883
Torrano-Silva BN, Vieira BR, Riosmena-Rodríguez R, Oliveira MC (2018) Guidelines for DNA barcoding of coralline algae, focusing on Lithophylloideae (Corallinales) from Brazil. Bot Mar 61:127–140
Traut BH (2005) The role of coastal ecotones: a case study of the salt marsh/upland transition zone in California. J Ecol 93:279–290
Twist BA, Neill KF, Bilewitch J, Jeong SY, Sutherland JE, Nelson WA (2019) High diversity of coralline algae in New Zealand revealed: knowledge gaps and implications for future research. PLoS ONE 14:e0225645
Tyberghein L, Verbruggen H, Pauly K, Troupin C, Mineur F, de Clerck O (2012) Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr 21:272–281
van den Hoek C (1987) The possible significance of long-range dispersal for the biogeography of seaweeds. Helgol Mar Res 41:261–272
Vermeij MJA, van Moorselaar I, Engelhard S, Hörnlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS ONE 5:1–8
Vieira-Pinto T, Oliveira MC, Bouzon J, Sissini M, Richards JL, Riosmena-Rodríguez R, Horta PA (2014) Lithophyllum species from Brazilian coast: range extension of Lithophyllum margaritae and description of Lithophyllum atlanticum sp. nov. (Corallinales, Corallinophycidae, Rhodophyta). Phytotaxa 190:355–369
Weiss A, Martindale RC (2017) Crustose coralline algae increased framework and diversity on ancient coral reefs. PLoS ONE 12:e0181637
Wilson S, Blake C, Berges JA, Maggs CA (2004) Environmental tolerances of free-living coralline algae (maerl): implications for European marine conservation. Biol Conserv 120:279–289
Zeebe RE, Zachos JC, Caldeira K, Tyrrell T (2008) Carbon emissions and acidification. Science 321:52–52
Žuljević A, Kaleb S, Peña V, Despalatović M, Cvitković I, De Clerck O, Le Gall L, Falace A, Vita F, Braga JC, Antolić B (2016) First freshwater coralline alga and the role of local features in a major biome transition. Sci Rep 6:19642
Acknowledgements
R. Morais, H. Guabiroba, L. Cabral, M. Lucena, M. Cavichioli, D. Cabral, and E. Bastos are thanked for assistance with sampling. We thank the Laboratório Multiusuário de Estudos em Biologia (LAMEB) of the Universidade Federal de Santa Catarina (UFSC) for the availability of equipment. We also thank R. Morais for comments. This work is dedicated to the memory of our great friend and colleague Thiony E. Simon. This work was financed in part by Conselho Nacional de Desenvolvimento Científico e Tecnologico (CNPq), Prospecção Sustentável e Ilhas Oceânicas: Biodiversidade, Química, Ecologia e Biotecnologia (PROSPECMAR 458548/2013-8), Rede Nacional de Pesquisa em Biodiversidade Marinha (SISBIOTAMar), Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (FAPESC), Fundação Grupo Boticário de Proteção à Natureza, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001. M.N.S. received a Ph.D. scholarship from CAPES and a Grant from the International Association for Plant Taxonomy (IAPT). Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP) provided scholarship for B.N.T.S. and T.V.P. (2010/19234-3, 2012/05076-2) and research funding to M.C.O, (Biota 2013/11833-3). M.C.O. also thanks the CNPq (305687/2018-2 and Br BOL 564945-2010-2). J.M.C.N is grateful to his personal grant provided by CNPq (308542/2018-5). M.B.B.B. thanks the grant Biota–FAPERJ (E–26/110.019/2011) provided by Fundação de Apoio à Pesquisa do Estado do Rio de Janeiro (FAPERJ). PH also thanks fellowship and additional financial support of CNPq, CAPES, CAPES-PRInt, FAPESC, and Fundação Boticário.
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Sissini, M.N., Koerich, G., de Barros-Barreto, M.B. et al. Diversity, distribution, and environmental drivers of coralline red algae: the major reef builders in the Southwestern Atlantic. Coral Reefs 41, 711–725 (2022). https://doi.org/10.1007/s00338-021-02171-1
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DOI: https://doi.org/10.1007/s00338-021-02171-1