Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-20T06:28:38.075Z Has data issue: false hasContentIssue false

When descriptive ecology meets physiology: a study in a South Atlantic rhodolith bed

Published online by Cambridge University Press:  24 April 2020

V. F. Carvalho*
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
J. Silva
CCMar – Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139Faro, Portugal
R. Kerr
Laboratório de Estudos dos Oceanos e Clima (LEOC), Instituto de Oceanografia, Universidade Federal do Rio Grande (FURG), 96203-900, Rio Grande, RS, Brazil
A. B. Anderson
Laboratory of Ichthyology – Departamento de Oceanografia e Ecologia, Universidade Federal do Espírito Santo, Av. Fernando Ferrari, 514, Goiabeiras, 29075-910, Vitória, ES, Brazil
E. O. Bastos
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
D. Cabral
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
L. P. Gouvêa
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
L. Peres
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
C. D. L. Martins
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
V. M. Silveira-Andrade
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
M. N. Sissini
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
P. H. Horta
Departamento de Botânica, CCB, Universidade Federal de Santa Catarina (UFSC), 88010-970 Florianópolis, SC, Brazil
Author for correspondence: V. F. Carvalho, E-mail:


This study presents two years of characterization of a warm temperate rhodolith bed in order to analyse how certain environmental changes influence the community ecology. The biomass of rhodoliths and associated species were analysed during this period and in situ experiments were conducted to evaluate the primary production, calcification and respiration of the dominant species of rhodoliths and epiphytes. The highest total biomass of rhodoliths occurred during austral winter. Lithothamnion crispatum was the most abundant rhodolith species in austral summer. Epiphytic macroalgae occurred only in January 2015, with Padina gymnospora being the most abundant. Considering associated fauna, the biomass of Mollusca increased from February 2015 to February 2016. Population densities of key reef fish species inside and around the rhodolith beds showed significant variations in time. The densities of grouper (carnivores/piscivores) increased in time, especially from 2015 to 2016. On the other hand, grunts (macroinvertebrate feeders) had a modest decrease over time (from 2014 to 2016). Other parameters such as primary production and calcification of L. crispatum were higher under enhanced irradiance, yet decreased in the presence of P. gymnospora. Community structure and physiological responses can be explained by the interaction of abiotic and biotic factors, which are driven by environmental changes over time. Biomass changes can indicate that herbivores play a role in limiting the growth of epiphytes, and this is beneficial to the rhodoliths because it decreases competition for environmental resources with fleshy algae.

Research Article
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Almada, VC and Faria, C (2004) Temporal variation of rocky intertidal resident fish assemblages – patterns and possible mechanisms with a note on sampling protocols. Reviews in Fish Biology and Fisheries 14, 239250.CrossRefGoogle Scholar
Amado-Filho, GM, Maneveldt, G, Manso, RCC, Rosa Marins, BV, Pacheco, MR and Guimarães, SMPB (2007) Estructura de los mantos de rodolitos de 4 a 55 metros de profundidad en la costa sur del estado de Espírito Santo, Brasil. Ciencias Marinas 33, 399410.CrossRefGoogle Scholar
Amado-Filho, GM, Moura, RL, Bastos, AC, Salgado, LT, Sumida, PY, Guth, AZ, Francini-Filho, RB, Pereira-Filho, GH, Abrantes, DP, Brasileiro, PS, Bahia, RG, Leal, RN, Kaufman, L, Kleypas, JA, Farina, M and Thompson, FL (2012 a) Rhodolith beds are major CaCO3 bio-factories in the tropical South West Atlantic. PLoS ONE 7, e35171.CrossRefGoogle ScholarPubMed
Amado-Filho, GM, Pereira-Filho Guilherme, H, Bahia, RG, Abrantes, P, Veras, PC and Matheus, Z (2012 b) Occurrence and distribution of rhodolith beds on the Fernando de Noronha Archipelago of Brazil. Aquatic Botany 101, 4145.CrossRefGoogle Scholar
Amado-Filho, GM, Bahia, RG, Pereira-Filho, GH and Longo, LL (2017) South Atlantic rhodolith beds: latitudinal distribution, species composition, structure and ecosystem functions, threats and conservation status. In Riosmena-Rodríguez, R, Nelson, W and Aguirre, J (eds), Rhodolith/Maërl Beds: A Global Perspective. Cham: Springer International Publishing Switzerland, pp. 299317.CrossRefGoogle Scholar
AmslerCD, Ed. CD, Ed. (2008) Algal Chemical Ecology. Berlin: Springer.CrossRefGoogle Scholar
Anderson, AB (2017) Peixes tropicais no seu limite de distribuição: dinâmica temporal da ictiofauna recifal no Sul do Brasil (PhD thesis). Federal University of Santa Catarina, Florianópolis, Brazil.Google Scholar
Anderson, AB, Bonaldo, RM, Barneche, DR, Hackradt, CW, Félix-Hackradt, FC, García-Charton, JA and Floeter, SR (2014) Recovery of grouper assemblages indicates effectiveness of a marine protected area in Southern Brazil. Marine Ecology Progress Series 514, 207215.CrossRefGoogle Scholar
Anderson, AB, Carvalho-Filho, A, Morais, RA, Nunes, LT, Quimbayo, JP and Floeter, SR (2015) Brazilian tropical fishes in their southern limit of distribution: checklist of Santa Catarina's rocky reef ichthyofauna, remarks and new records. Check List (Luis Felipe Toledo) 11, 1688.CrossRefGoogle Scholar
Andradi-Brown, DA, Vermeij, MJ, Slattery, M, Lesser, M, Bejarano, I, Appeldoorn, R, Goodbody-Gringley, G, Chequer, AD, Pitt, JM and Eddy, C (2017) Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management. Biological Invasions 19, 939954.CrossRefGoogle Scholar
Andrews, S, Bennett, S and Wernberg, T (2014) Reproductive seasonality and early life temperature sensitivity reflect vulnerability of a seaweed undergoing range reduction. Marine Ecology Progress Series 495, 119129.CrossRefGoogle Scholar
Bahia, RG, Abrantes, DP, Brasileiro, PS, Pereira-Filho, GH and Amado-Filho, GM (2010) Rhodolith bed structure along a depth gradient on the northern coast of Bahia State, Brazil. Brazilian Journal of Oceanography 58, 323337.CrossRefGoogle Scholar
Basso, D (2012) Carbonate production by calcareous red algae and global change. Geodiversitas 34, 1333.CrossRefGoogle Scholar
Baum, JK and Worm, B (2009) Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78, 699714.CrossRefGoogle ScholarPubMed
Begon, M, Townsend, CRH, John, L, Colin, RT and John, LH (2006) Ecology: From Individuals to Ecosystems. Malden, MA: Blackwell.Google Scholar
Bellwood, DR, Goatley, CH and Bellwood, O (2017) The evolution of fishes and corals on reefs: form, function and interdependence. Biological Reviews 92, 878901.CrossRefGoogle ScholarPubMed
Blake, C and Maggs, CA (2003) Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from Northern Europe. Phycologia 42, 606612.CrossRefGoogle Scholar
Borowitzka, MA and Larkum, AWD (1987) Calcification in algae: mechanisms and the role of metabolism. Critical Reviews in Plant Sciences 6, 145.CrossRefGoogle Scholar
Burdett, HL, Keddie, V, MacArthur, N, McDowall, L, McLeich, J, Spielvogel, E, Hatton, AD and Kamenos, NA (2014) Dynamic photoinhibition exhibited by red coralline algae in the red sea. BMC Plant Biology 14, 139.CrossRefGoogle ScholarPubMed
Caragnano, A, Basso, D and Rodondi, G (2016) Growth rates and ecology of coralline rhodoliths from the Ras Ghamila back reef lagoon, Red Sea. Marine Ecology 37, 713726.CrossRefGoogle Scholar
Cavalcanti, GS, Gregoracci, GB, Dos Santos, EO, Silveira, CB, Meirelles, PM, Longo, L, Gotoh, K, Nakamura, S, Iida, T, Sawabe, T, Rezende, CE, Francini-Filho, RB, Moura, RL, Amado-Filho, GM and Thompson, FL (2014) Physiologic and metagenomic attributes of the rhodoliths forming the largest CaCO3 bed in the South Atlantic Ocean. ISME Journal 8, 5262.CrossRefGoogle ScholarPubMed
Chatfield, C (1989) Non-linear and non-stationary time series analysis: M.B. Priestley, (Academic Press, London, 1988), £25.00, pp. 237. International Journal of Forecasting 5, 428429.CrossRefGoogle Scholar
Comeau, S, Carpenter, RC and Edmunds, PJ (2014) Effects of irradiance on the response of the coral Acropora pulchra and the calcifying alga Hydrolithon reinboldii to temperature elevation and ocean acidification. Journal of Experimental Marine Biology and Ecology 453, 2835.CrossRefGoogle Scholar
Cornwall, CE, Comeau, S and McCulloch, MT (2017) Coralline algae elevate pH at the site of calcification under ocean acidification. Global Change Biology 23, 42454256.CrossRefGoogle ScholarPubMed
Côté, IM, Darling, ES, Malpica-Cruz, L, Smith, NS, Green, SJ, Curtis-Quick, J and Layman, C (2014) What doesn't kill you makes you wary? Effect of repeated culling on the behaviour of an invasive predator. PLoS ONE 9, e94248.CrossRefGoogle ScholarPubMed
de Mendiburu, F (2013) Statistical Procedures for Agricultural Research. Package “Agricolae” Version 1.4–4. Comprehensive R Archive Network. Vienna: Institute for Statistics and Mathematics. Scholar
Dickson, AG, Afghan, JD and Anderson, GC (2003) Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity. Marine Chemistry 80, 185197.CrossRefGoogle Scholar
Dickson, AG, Sabine, CL and Christian, JR (2007) Guide to Best Practices for Ocean CO2 Measurements. Sidney, BC: North Pacific Marine Science Organization.Google Scholar
Dodds, WK (1991) Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologia 85, 572580.CrossRefGoogle ScholarPubMed
Drake, LA, Dobbs, FC and Zimmerman, RC (2003) Effects of epiphyte load on optical properties and photosynthetic potential of the seagrasses Thalassia testudinum Banks ex König and Zostera marina. Limnology and Oceanography 48, 456463.CrossRefGoogle Scholar
Dring, MJ (1981) Chromatic adaptation of photosynthesis in benthic marine algae: an examination of its ecological significance using a theoretical model. Limnology and Oceanography 26, 271284.CrossRefGoogle Scholar
Dunne, JA, Williams, RJ and Martinez, ND (2004) Network structure and robustness of marine food webs. Marine Ecology Progress Series 273, 291302.CrossRefGoogle Scholar
Eichler, PPB, Sen Gupta, BK, Eichler, BB, Braga, ES and Campos, EJ (2008) Benthic foraminiferal assemblages of south Brazil: relationship to water masses and nutrient distributions. Continental Shelf Research 28, 16741686.CrossRefGoogle Scholar
Figueiredo, MAO, Kain, JM and Norton, TA (2000) Responses of crustose corallines to epiphyte and canopy cover. Journal of Phycology 36, 1724.CrossRefGoogle Scholar
Floeter, SR, Krohling, W, Gasparini, JL, Ferreira, CE and Zalmon, IR (2007) Reef fish community structure on coastal islands of southeastern Brazil: the influence of exposure and benthic cover. Environmental Biology of Fishes 78, 147160.CrossRefGoogle Scholar
Fong, P and Zedler, JB (1993) Temperature and light effects on the seasonal succession of algal communities in shallow coastal lagoons. Journal of Experimental Marine Biology and Ecology 171, 259272.CrossRefGoogle Scholar
Foster, MS (2001) Rhodoliths: between rocks and soft places. Journal of Phycology 37, 659667.CrossRefGoogle Scholar
Foster, MS, Amado-Filho, GM, Kamenos, NA, Riosmena-Rodriguez, R and Steller, DL (2013) Rhodoliths and rhodolith beds. Smithsonian Contributions to the Marine Sciences 39, 143155.Google Scholar
Francini-Filho, RB, Coni, EO, Meirelles, PM, Amado-Filho, GM, Thompson, FL, Pereira-Filho, GH, Bastos, AC, Abrantes, DP, Ferreira, CM, Gibran, FZ, Güth, AZ, Sumida, PYG, Oliveira, NL, Kaufman, L, Minte-Vera, CV and Moura, RL (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS ONE 8, e54260.CrossRefGoogle ScholarPubMed
Fredericq, S, Krayesky-Self, S, Sauvage, T, Richards, J, Kittle, R, ArakakiN, Hickerson E N, Hickerson E and Schmidt, WE (2018) 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. Frontiers in Marine Science, 5, 502.CrossRefGoogle Scholar
Freire, AS, Varela, ARD, Fonseca, ALO, Menezes, BS, Fest, CB, Obata, CS, Gorri, C, Franco, D, Machado, EC, Barros, G, Molessari, LS, Madureira, LAS, Coelho, MP, Carvalho, M and Pereira, TL (2017) O ambiente oceanográfico. In Segal, B, Freire, AS, Lindner, A, Krajewski, JP and Soldateli, M (eds), Maare: Monitoramento Ambiental da Reserva Marinha do Arvoredo e Entorno. Florianópolis: UFSC/Maare, pp 159198.Google Scholar
Friedlander, AM and DeMartini, EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Marine Ecology Progress Series 230, 253264.CrossRefGoogle Scholar
Frith, CA, Leis, JM and Goldman, B (1986) Currents in the Lizard Island region of the Great Barrier Reef Lagoon and their relevance to potential movements of larvae. Coral Reefs 5, 8192.CrossRefGoogle Scholar
Froese, R and Pauly, D (2016) Fishbase (www database). World Wide Web Electronic Publications. Accessed online September 2016.Google Scholar
Gherardi, DF (2004) Community structure and carbonate production of a temperate rhodolith bank from Arvoredo Island, southern Brazil. Brazilian Journal of Oceanography 52, 207224.CrossRefGoogle Scholar
Grall, J, Le Loc'h, F, Guyonnet, B and Riera, P (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. Journal of Experimental Marine Biology and Ecology 338, 115.CrossRefGoogle Scholar
Gross, EM (2003) Allelopathy of aquatic autotrophs. Critical Reviews in Plant Science 22, 313339.CrossRefGoogle Scholar
Guillou, M, Grall, J and Connan, S (2002) Can low sea urchin densities control macro-epiphytic biomass in a north-east Atlantic maerl bed ecosystem (Bay of Brest, Brittany, France)? Journal of the Marine Biological Association of the United Kingdom 82, 867876.CrossRefGoogle Scholar
Hay, ME, Renaud, PE and Fenical, W (1988) Large mobile vs small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia 75, 246252.CrossRefGoogle Scholar
Heithaus, MR, Frid, A, Wirsing, AJ and Worm, B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology and Evolution 23, 202210.CrossRefGoogle ScholarPubMed
Herbing, I (2002) Effects of temperature on larval fish swimming performance: the importance of physics to physiology. Journal of Fish Biology 61, 865876.CrossRefGoogle Scholar
Heupel, MR, Knip, DM, Simpfendorfer, CA and Dulvy, NK (2014) Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series 495, 291298.CrossRefGoogle Scholar
Hily, C, Potin, P and Floc'h, JY (1992) Structure of subtidal algal assemblages on soft-bottom sediments: fauna/flora interactions and role of disturbances in the Bay of Brest, France. Marine Ecology Progress Series 85, 115130.CrossRefGoogle Scholar
Hinojosa-Arango, G, Maggs, CA and Johnson, MP (2009) Like a rolling stone: the mobility of maerl (Corallinaceae) and the neutrality of the associated assemblages. Ecology 90, 517528.CrossRefGoogle Scholar
Ho, M and Carpenter, RC (2017) Differential growth responses to water flow and reduced pH in tropical marine macroalgae. Journal of Experimental Marine Biology and Ecology 491, 5865.CrossRefGoogle Scholar
Hoegh-Guldberg, O (1988) A method for determining the surface area of corals. Coral Reefs 7, 113116.CrossRefGoogle Scholar
Hofmann, LC, Koch, M and de Beer, D (2016) Biotic control of surface pH and evidence of light-induced H+ pumping and Ca2+−H+ exchange in a tropical crustose coralline alga. PLoS ONE 11, e0159057.CrossRefGoogle Scholar
Horta, PA, Salles, JP, Bouzon, JL, Scherner, F, Cabral, DQ and Bouzon, ZL (2008) Composição e estrutura do fitobentos do infralitoral da Reserva Biológica Marinha do Arvoredo, Santa Catarina, Brasil – Implicações para conservação. Oecologia Brasiliensis 12, 243257.Google Scholar
Horta, PA, Riul, P, Amado Filho, GM, Gurgel, CFD, Berchez, F, Nunes, JMC, Scherner, F, Pereira, S, Lotufo, T, Peres, L, Sissini, M, Bastos, EO, Rosa, J, Munoz, P, Martins, C, Gouvêa, L, Carvalho, V, Bergstrom, E, Schubert, N, Bahia, RG, Rodrigues, AC, Rörig, L, Barufi, JB and Figueiredo, M (2016) Rhodoliths in Brazil: current knowledge and potential impacts of climate change. Brazilian Journal of Oceanography 64, 117136.CrossRefGoogle Scholar
Hurd, CL (2000) Water motion, marine macroalgal physiology, and production. Journal of Phycology 36, 453472.CrossRefGoogle Scholar
Johansen, HW (1981) Coralline Algae: A First Synthesis. Worcester: CRC Press.Google Scholar
Kamenos, NA and Law, A (2010) Temperature controls on coralline algal skeletal growth. Journal of Phycology 46, 331335.CrossRefGoogle Scholar
Kim, J, Choi, JS, Kang, SE, Cho, JY, Jin, HJ, Chun, BS and Hong, YK (2004) Multiple allelopathic activity of the crustose coralline alga Lithophyllum yessoense against settlement and germination of seaweed spores. Journal of Applied Phycology 16, 175179.CrossRefGoogle Scholar
Kordas, RL, Harley, CD and O'Connor, MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. Journal of Experimental Marine Biology and Ecology 400, 218226.CrossRefGoogle Scholar
Krayesky-Self, S, Schmidt, WE, Phung, D, Henry, C, Sauvage, T, Camacho, O and Fredericq, S (2017) Eukaryotic life inhabits rhodolith-forming coralline algae (Hapalidiales, Rhodophyta), remarkable marine benthic microhabitats. Scientific Reports 7, 45850.CrossRefGoogle Scholar
Labasque, T, Chaumery, C, Aminot, A and Kergoat, G (2004) Spectrophotometric Winkler determination of dissolved oxygen: re-examination of critical factors and reliability. Marine Chemistry 88, 5360.CrossRefGoogle Scholar
Legrand, E, Riera, P, Lutier, M, Coudret, J, Grall, J and Martin, S (2017) Species interactions can shift the response of a maerl bed community to ocean acidification and warming. Biogeosciences Discussions 14, 53595376.CrossRefGoogle Scholar
Levin, LA and Creed, EL (1986) Effect of temperature and food availability on reproductive responses of Streblospio benedicti (Polychaeta: Spionidae) with planktotrophic or lecithotrophic development. Marine Biology 92, 103113.CrossRefGoogle Scholar
Littler, DM and Littler, MM (2000) Caribbean Reef Plants: An Identification Guide to the Reef Plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. Washington, DC: Offshore Graphics Inc.Google Scholar
Littler, MM, Littler, DS, Blair, SM and Norris, JN (1986) Deep-water plant communities from an uncharted seamount off San Salvador Island, Bahamas: distribution, abundance, and primary productivity. Deep-Sea Research Part I: Oceanographic Research Papers 33, 881892.CrossRefGoogle Scholar
Littler, MM, Littler, DS and Taylor, PR (1995) Selective herbivore increases biomass of its prey: a chiton-coralline reef-building association. Ecology 76, 16661681.CrossRefGoogle Scholar
Lubchenco, J (1983) Littorina and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology 64, 11161123.CrossRefGoogle Scholar
Martin, S, Castets, MD and Clavier, J (2006) Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquatic Botany 85, 121128.CrossRefGoogle Scholar
Martin, S, Clavier, J, Chauvaud, L and Thouzeau, G (2007) Community metabolism in temperate maerl beds, I. Carbon and carbonate fluxes. Marine Ecology Progress Series 335, 1929.CrossRefGoogle Scholar
Matano, RP, Palma, ED and Piola, AR (2010) The influence of the Brazil and Malvinas currents on the southwestern Atlantic shelf circulation. Ocean Science 7, 135.Google Scholar
Maughan, BC and Barnes, DKA (2000) Epilithic boulder communities of Lough Hyne, Ireland: the influence of water movement and sediment. Journal of the Marine Biological Association of the United Kingdom 80, 767776.CrossRefGoogle Scholar
McConnico, LA, Carmona, GH, Morales, JSM and Rodríguez, RR (2017) Temporal variation in seaweed and invertebrate assemblages in shallow rhodolith beds of Baja California Sur, México. Aquatic Botany 139, 3747.CrossRefGoogle Scholar
McNicholl, C, Koch, MS and Hofmann, LC (2019) Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: a proposed mechanism to sustain calcification under ocean acidification. Journal of Experimental Marine Biology and Ecology 521, 151208.CrossRefGoogle Scholar
McQuaid, CD and Froneman, PW (1993) Mutualism between the territorial intertidal limpet Patella longicosta and the crustose alga Ralfsia verrucosa. Oecologia 96, 128133.CrossRefGoogle ScholarPubMed
Möller, OO Jr, Piola, AR, Freitas, AC and Campos, EJD (2008) The effects of river discharge and seasonal winds on the shelf off Southeastern South America. Continental Shelf Research 28, 16071624.CrossRefGoogle Scholar
National Institute of Meteorology – INMET. Historical Data. Accessed online in August 2017.Google Scholar
Neill, KF, Nelson, WA, D'Archino, R, Leduc, D and Farr, TJ (2015) Northern New Zealand rhodoliths: assessing faunal and floral diversity in physically contrasting beds. Marine Biodiversity 45, 6375.CrossRefGoogle Scholar
Neushul, M, Benson, J, Harger, BWW and Charters, AC (1992) Macroalgal farming in the sea: water motion and nitrate uptake. Journal of Applied Phycology 4, 255265.CrossRefGoogle Scholar
Noisette, F, Duong, G, Six, C, Davoult, D and Martin, D (2013) Effects of elevated pCO2 on the metabolism of a temperate rhodolith Lithothamnion corallioides grown under different temperatures. Journal of Phycology 49, 746757.CrossRefGoogle Scholar
Orselli, IB, Kerr, R, Ito, RG, Tavano, VM, Mendes, CRB and Garcia, CA (2018) How fast is the Patagonian shelf-break acidifying? Journal of Marine Systems 178, 114.CrossRefGoogle Scholar
Ottersen, G, Nils, CS and Hurrell, JW (2014) Climatic fluctuations and marine systems: a general introduction to the ecological effects. In Stenseth, N, Ottersen, G, Hurrell, JW and Belgrano, A (eds), Marine Ecosystems and Climate Variation. Oxford: Oxford University Press, pp. 314.Google Scholar
Paquette, ML, Bonetti, C, Bitencourt, V and Bonetti, J (2016) Spatial patterns of benthic foraminifera as a support to the oceanographic characterisation of Arvoredo biological marine reserve (South Atlantic, Brazil). Marine Environmental Research 114, 4050.CrossRefGoogle Scholar
Pascelli, C (2009) Variação sazonal e estrutura da comunidade fitobêntica do banco de nódulos calcários da Reserva Biológica Marinha do Arvoredo-Um oásis submerso (Graduation thesis). Federal University of Santa Catarina, Florianópolis, Brazil.Google Scholar
Pascelli, C, Riul, P, Riosmena-Rodríguez, R, Scherner, F, Nunes, M, Hall-Spencer, JM, Oliveira, EC and Horta, P (2013) Seasonal and depth-driven changes in rhodolith bed structure and associated macroalgae off Arvoredo island (southeastern Brazil). Aquatic Botany 111, 6265.CrossRefGoogle Scholar
Peña, V, Bárbara, I, Grall, J, Maggs, CA and Hall-Spencer, JM (2014). The diversity of seaweeds on maerl in the NE Atlantic. Marine Biodiversity 44, 533551.CrossRefGoogle Scholar
Pörtner, HO, Berdal, B, Blust, R, Brix, O, Colosimo, A, De Wachter, B, Giuliani, A, Johansen, T, Fischer, T, Knust, R, Lannig, G, Naevdal, G, Nedenes, A, Nyhammer, G, Sartoris, FJ, Serendero, I, Sirabella, P, Thorkildsen, S and Zakhartsev, M (2001) Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus). Continental Shelf Research 21, 19751997.CrossRefGoogle Scholar
Randall, CJ and Szmant, AM (2009) Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28, 537545.CrossRefGoogle Scholar
Reiskind, JB, Beer, S and Bowes, G (1989) Photosynthesis, photorespiration and ecophysiological interactions in marine macroalgae. Aquatic Botany 34, 131152.CrossRefGoogle Scholar
Riul, P, Targino, CH, Farias, JDN, Visscher, PT and Horta, PA (2008) Decrease in Lithothamnion sp. (Rhodophyta) primary production due to the deposition of a thin sediment layer. Journal of the Marine Biological Association of the United Kingdom 88, 1719.CrossRefGoogle Scholar
Riul, P, Lacouth, P, Pagliosa, PR, Christoffersen, ML and Horta, PA (2009) Rhodolith beds at the easternmost extreme of South America: community structure of an endangered environment. Aquatic Botany 90, 315320.CrossRefGoogle Scholar
Rocha, RM, Metri, R and Omuro, JY (2006) Spatial distribution and abundance of ascidians in a bank of coralline algae at Porto Norte, Arvoredo Island, Santa Catarina. Journal of Coastal Research 39, 16761679.Google Scholar
Rohde, S, Hiebenthal, C, Wahl, M, Karez, R and Bischof, K (2008) Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: effects of light deficiency and epibionts on growth and photosynthesis. European Journal of Phycology 43, 143150.CrossRefGoogle Scholar
Sand-Jensen, K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquatic Botany 3, 5563.CrossRefGoogle Scholar
Sañé, E, Chiocci, FL, Basso, D and Martorelli, E (2016) Environmental factors controlling the distribution of rhodoliths: an integrated study based on seafloor sampling, ROV and side scan sonar data, offshore the W-Pontine Archipelago. Continental Shelf Research 129, 1022.CrossRefGoogle Scholar
Scherner, F, Riul, P, Bastos, E, Bouzon, ZL, Pagliosa, PR, Blankensteyn, A, Oliveira, EC and Horta, PA (2010) Herbivory in a rhodolith bed: a structuring factor. Pan-American Journal of Aquatic Sciences 5, 358366.Google Scholar
Scherner, F, Pereira, CM, Duarte, G, Horta, PA, Castro, CB, Barufi, JB and Pereira, SMB (2016) Effects of ocean acidification and temperature increases on the photosynthesis of tropical reef calcified macroalgae. PLoS ONE 11, e0154844.CrossRefGoogle ScholarPubMed
Semesi, IS, Beer, S and Björk, M (2009) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Marine Ecology Progress Series 382, 4147.CrossRefGoogle Scholar
Short, JA, Pedersen, O and Kendrick, GA (2015) Turf algal epiphytes metabolically induce local pH increase, with implications for underlying coralline algae under ocean acidification. Estuarine, Coastal and Shelf Science 164, 463470.CrossRefGoogle Scholar
Sissini, MN, Oliveira, MC, Gabrielson, PW, Robinson, NM, Okolodkov, YB, Riosmena-Rodríguez, R and Horta, PA (2014) Mesophyllum erubescens (Corallinales, Rhodophyta) – so many species in one epithet. Phytotaxa 190, 299319.CrossRefGoogle Scholar
Smale, DA, Wernberg, T and Vanderklift, MA (2017) Regional-scale variability in the response of benthic macroinvertebrate assemblages to a marine heatwave. Marine Ecology Progress Series 568, 1730.CrossRefGoogle Scholar
Smith, SV and Key, GS (1975) Carbon dioxide and metabolism in marine environments. Limnology and Oceanography 20, 493495.CrossRefGoogle Scholar
Snedecor, GW and Cochran, WG (1989) Statistical Methods, 8th Edn. Ames, IA: Iowa State University Press.Google Scholar
Stachowicz, JJ and Hay, ME (1996) Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105, 377387.CrossRefGoogle Scholar
Stachowicz, JJ and Whitlatch, RB (2005) Multiple mutualists provide complementary benefits to their seaweed host. Ecology 86, 24182427.CrossRefGoogle Scholar
Steller, DS and Foster, MS (1995) Environmental factors influencing distribution and morphology of rhodoliths in Bahia Concepcion, B.C.S., Mexico. Journal of Experimental Marine Biology and Ecology 194, 201212.CrossRefGoogle Scholar
Steller, DL, Riosmena-Rodríguez, R, Foster, MS and Roberts, CA (2003) Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S5S20.CrossRefGoogle Scholar
Steller, DL, Hernandez-Ayon, JM, Riosmena-Rodriguez, R and Cabello-Pasini, A (2007) Effect of temperature on photosynthesis, growth and calcification rates of the free-living coralline alga Lithophyllum margaritae. Ciencias Marinas 33, 441456.CrossRefGoogle Scholar
Steneck, RS and Dethier, MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69, 476498.CrossRefGoogle Scholar
Steneck, RS, Hacker, SD and Dethier, MN (1991) Mechanisms of competitive dominance between crustose coralline algae: an herbivore-mediated competitive reversal. Ecology 72, 938950.CrossRefGoogle Scholar
Strub, PT, James, C, Combes, V, Matano, RP, Piola, AR, Palma, ED, Saraceno, M, Guerrero, RA, Fenco, H and Ruiz-Etcheverry, LA (2015) Altimeter derived seasonal circulation on the Southwest Atlantic Shelf: 27°–43°S. Journal of Geophysical Research: Oceans 120, 33913418.Google ScholarPubMed
Suzuki, Y, Takabayashi, T, Kawaguchi, T and Matsunaga, K (1998) Isolation of an allelopathic substance from the crustose coralline algae, Lithophyllum spp., and its effect on the brown alga, Laminaria religiosa Miyabe (Phaeophyta). Journal of Experimental Marine Biology and Ecology 225, 6977.CrossRefGoogle Scholar
Teichert, S and Freiwald, A (2014) Polar coralline algal CaCO3-production rates correspond to intensity and duration of the solar radiation. Biogeosciences (Online) 11, 833842.CrossRefGoogle Scholar
Treml, EA, Halpin, PN, Urban, DL and Pratson, LF (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecology 23, 1936.CrossRefGoogle Scholar
Underwood, A (1981) Techniques of analysis of variance in experimental marine biology and ecology. Annual Reviews of Oceanography and Marine Biology 19, 513605.Google Scholar
Underwood, GJC, Thomas, JD and Baker, JH (1992) An experimental investigation of interactions in snail-macrophyte-epiphyte systems. Oecologia 91, 587595.CrossRefGoogle ScholarPubMed
Vermeij, MJA, Dailer, ML and Smith, CM (2011) Crustose coralline algae can suppress macroalgal growth and recruitment on Hawaiian coral reefs. Marine Ecology Progress Series 422, 17.CrossRefGoogle Scholar
Vinagre, C, Mendonça, V, Cereja, R, Abreu-Afonso, F, Dias, M, Mizrahi, D and Flores, AA (2018) Ecological traps in shallow coastal waters – potential effect of heat-waves in tropical and temperate organisms. PLoS ONE 13, e0192700.CrossRefGoogle ScholarPubMed
Wahl, M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24, 427438.CrossRefGoogle ScholarPubMed
Wilson, S, Blake, C, Berges, JA and Maggs, CA (2004) Environmental tolerances of free-living coralline algae (maerl): implications for European marine conservation. Biological Conservation 120, 279289.CrossRefGoogle Scholar
Woelkerling, WJ (1988) The Coralline Red Algae: An Analysis of the Genera and Subfamilies of Nongeniculate Corallinaceae. Oxford: Oxford University Press.Google Scholar
Wolf-Gladrow, DA, Zeebe, RE, Klaas, C, Kortzinger, A and Dickson, AG (2007) Total alkalinity: the explicit conservative expression and its application to biogeochemical processes. Marine Chemistry 106, 287300.CrossRefGoogle Scholar
Worm, B and Myers, RA (2003) Meta-analysis of cod–shrimp interactions reveals top-down control in oceanic food webs. Ecology 84, 162173.CrossRefGoogle Scholar
Zar, JH (1999) Biostatistical Analysis, 5th Edn. Harlow: Pearson Education.Google Scholar
Supplementary material: File

Carvalho et al. supplementary material

Figure S1

Download Carvalho et al. supplementary material(File)
File 661 KB
Supplementary material: File

Carvalho et al. supplementary material

Figure S2

Download Carvalho et al. supplementary material(File)
File 88.9 KB
Supplementary material: File

Carvalho et al. supplementary material

Table S1

Download Carvalho et al. supplementary material(File)
File 11.4 KB
Supplementary material: File

Carvalho et al. supplementary material

Table S2

Download Carvalho et al. supplementary material(File)
File 10.8 KB