Diversity of benthic fauna of rhodoliths and sediments deposited on sandstone reefs in Southeast Brazil
DOI:
https://doi.org/10.1590/2675-2824070.21029sbnKeywords:
Costa Das Algas environmental protection area, Faunal assemblage, Macrofauna, Meiofauna, BiodiversityAbstract
Sandstone reefs play an important role in sheltering a great diversity of organisms. In the north sector of the state of Espírito Santo, southeastern Brazil, the beaches are characterized by ferruginous sandstone reefs in the intertidal zones. These structures have unconsolidated sediment deposited over the reefs, mainly composed of bioclastic fragments of shells and seaweed, like the rhodolith. Rhodoliths are free-living calcareous algae with three-dimensional structures. By modifying the environment's physical characteristics, they create new microhabitats capable of being inhabited by several organisms, such as meio- and macrobenthonic invertebrates. This study sought to investigate the diversity of benthic fauna (macro- and meiofauna) on different substrates (rhodoliths vs. unconsolidated sediment) in the sandstone reef and investigate whether there are differences in benthic community structure between reef zones on Gramuté Beach in the Costa das Algas Environmental Protection Area in Aracruz, Espírito Santo, Brazil. Uni and multifactor analyses showed significant differences in the composition of the benthic fauna between the substrates (p < 0.05). Meiofauna and macrofauna had higher numbers of taxa and diversity associated with rhodoliths compared to with sediments. A multivariate analysis corroborates the results of the univariate, showing variations between substrates and beach zones. The presence of rhodoliths at Gramuté Beach contributes to the heterogeneity of the ecosystem and increases the richness and diversity of the benthos. The character of the benthic community and its dynamic aspects are discussed herein and are extremely important for conservation actions.
References
ALBINO, J., NETO, N. C. & OLIVEIRA T. C. A. 2016. The beaches of Espírito Santo. Coastal Research Library, 17, 333-361.
ALBINO, J. & SUGUIO, K. 2011. The influence of sediment grain size and composition on the morphodynamic state of mixed siliciclastic and bioclastic sand beaches in Espirito Santo State, Brazil. Revista Brasileira de Geomorfologia, 12(2), 81-92.
AMADO-FILHO, G. M., BAHIA, R. G, PEREIRA-FILHO, G. H & LONGO, L. L. 2017. South Atlantic rhodolith beds: latitudinal distribution, species composition, structure and ecosystem functions, threats and conservation status. In: RIOSMENA-RODRÍGUEZ, R., NELSON, W. & AGUIRRE, E. (eds.). Rhodolith/Maërl beds: a global perspective Cham: Springer International Publishing, pp. 299-317.
AMADO-FILHO, G. M., MANEVELDT, G. W., PEREIRA-FILHO, G. H., MANSO, R. C. C. & BAHIA, R. C. C. 2010. Seaweed diversity associated with a Brazilian tropical rhodolith bed. Ciências Marinas, 36, 371-391.
AMADO-FILHO, G. M. & PEREIRA-FILHO, G. H. 2012. Rhodolith beds in Brazil: a new potential habitat for marine bioprospection. Revista Brasileira de Farmacognosia, 22(4), 782-788.
ANDERSON, M. J., GORLEY, R. N. & CLARKE, K. R. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E.
ANDRADES, R., GOMES, M. P., PEREIRA-FILHO, G. H., SOUZA-FILHO, J. F., ALBUQUERQUE, C. Q. & MARTINS, A. S. 2014. The influence of allochthonous macroalgae on the fish communities of tropical sandy beaches. Estuarine, Coastal and Shelf Science, 144, 75-81.
ANTONIADOU, C. & CHINTIROGLOU, C. 2006. Trophic relationships of polychaetes associated with different algal growth forms. Helgoland Marine Research, 60, 39-49.
BALDRIGHI, E. & MANINI, E. 2015. Deep-sea meiofauna and macrofauna diversity and functional diversity: are they related? Marine Biodiversity, 45(3), 469-488.
BIANCHELLI, S., GAMBI, C., ZEPPILLI, D. & DANOVARO, R. 2010. Metazoan meiofauna in deep-sea canyons and adjacent open slopes: a large-scale comparison with focus on the rare taxa. Deep Sea Research Part I: Oceanographic Research Papers, 57(3), 420-433.
BERLANDI, R. M., FIGUEIREDO, M. A. O., M. A. & PAIVA, P. C. 2012. Rhodolith morphology and the diversity of polychaetes off the southeastern brazilian coast. Journal of Coastal Research, 28(1), 280-287.
BOSENCE, D. W. J. 1983. Description and classification of rhodoliths (rhodoids, rhodolites). In: PERYT, T. M. (ed.). Coated grains Berlin: Springer-Verlag, pp. 217-224.
BRUNO, J. F. & BERTNESS, M. D. 2001. Habitat modification and facilitation in benthic marine communities. Marine Community Ecology, 201-218.
BUENO, M., DENA-SILVA, S. A., FLORES, A. A. V. & LEITE, F. P. P. 2016. Effects of wave exposure on the abundance and composition of amphipod and tanaidacean assemblages inhabiting intertidal coralline algae. Journal of the Marine Biological Association of the United Kingdom, 96(3), 761-767.
CARVALHO, L. R. S. & BARROS, F. 2017. Physical habitat structure in marine ecosystems: the meaning of complexity and heterogeneity. Hydrobiologia, 797(2), 1-9.
CELENTANO, E., LERCARI, D., MANEIRO, P., RODRÍGUEZ, P., GIANELLI, I., ORTEGA, L., ORLANDO, L. & DEFEO, O. 2019. The forgotten dimension in sandy beach ecology: Vertical distribution of the macrofauna and its environment. Estuarine, Coastal and Shelf Science, 217, 165-172.
CLARKE, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1), 117-143.
CLARKE, K. R. & WARWICK, R. M. 2001. Change in marine communities: an approach to statistical analysis and interpretation 2nd ed. Plymouth: PRIMER-E.
CORREIA, J. R. M., OLIVEIRA, W. D., PEREIRA, P. S., CAMARGO, J. M. R. & ARAÚJO, M. E. 2018. Substrate zonation as a function of reef morphology: a case study in Carneiros Beach, Pernambuco, Brazil. Journal of Coastal Research, 81(spe1), 1-9.
COSTA, D. D. A., DOLBETH, M., PRATA, J., SILVA, F. D. A., SILVA, G. M. B., FREITAS, P. R. S., CHRISTOFFERSEN, M. L., LIMA, S. F. B., MASSEI, K. & LUCENA, R. F. P. 2021. Marine invertebrates associated with rhodoliths/maërl beds from northeast Brazil (State of Paraíba). Biodiversity Data Journal, 9.
COSTA, D. D. A., LUCENA, R. F. P., SILVA, F. D. A., SILVA, G. M. B., MASSEI, K., CHRISTOFFERSEN, M. L. & DOLBETH, M. 2021. Importance of rhodoliths as habitats for benthic communities in impacted environments. Regional Studies in Marine Science, 48, 102055.
COSTA, D. D. A., SILVA, F. D. A., SILVA, J. M., PEREIRA, A. R., DOLBETH, M., CHRISTOFFERSEN, M. L. & LUCENA, R. F. P. 2019. Is tourism affecting polychaete assemblages associated with rhodolith beds in Northeastern Brazil. Revista de Biología Tropical, 67(Suppl 5), S1-S15.
COSTA, K. G. & NETTO, S. A. 2014. Effects of small-scale trawling on benthic communities of estuarine vegetated and non-vegetated habitats. Biodiversity and Conservation, 23(4), 1041-1055.
DIAS, G. T. M. & VILLAÇA, R. C. 2012. Coralline algae depositional environments on the Brazilian central-south-eastern shelf. Journal of Coastal Research, 28(1), 270-279.
FIGUEIREDO, M. A., MENEZES, K. S., COSTA-PAIVA, E. M., PAIVA, P. C. & VENTURA, C. R. R. 2007. Experimental evaluation of rhodoliths as living substrata for infauna at the Abrolhos Bank, Brazil. Ciencias Marinas, 33(4), 427-440.
FIGUEIREDO, M. D. O., MENEZES, K. S., COSTA-PAIVA, E. M., PAIVA, P. C. & VENTURA, C. R. R. 2007. Experimental evaluation of rhodoliths as living substrata for infauna at the Abrolhos Bank, Brazil. Ciencias Marinas, 33(4), 427-440.
FOSTER, M. S. 2001. Rhodoliths, between rocks and soft places. Journal of Phycology, 37(5), 659-657.
FOSTER, M. S., AMADO-FILHO, G. M., KAMENOS, N. A., RIOSMENA-RODRÍGUEZ, R. & STELLER, D. L. 2013. Rhodoliths and rhodolith beds. In: LANG, M. A., MARINELLI, R. L., ROBERTS, S. J. & TAYLOR, P. R. (eds.). Research and discoveries: the revolution of science through SCUBA, 39, 143-155.
FUKUDA, M. V. 2017. Aspectos reprodutivos de Syllidae (Annelida,“Polychaeta”). Revista Brasileira de Zoociências, 17, 51-54.
GABARA, S. S., HAMILTON, S. L., EDWARDS, M. S. & STELLER, D. L. 2018. Rhodolith structural loss decreases abundance, diversity, and stability of benthic communities at Santa Catalina Island, CA. Marine Ecology Progress Series, 595, 71-88.
GALLUCCI, F. A., CHRISTOFOLETTI, R., FONSECA, G. & DIAS, G. M. 2020. The effects of habitat heterogeneity at distinct spatial scales on hard-bottom-associated communities. Diversity, 12(1), 39.
GIERE, O. 2009. Introduction to meiobenthology. In: GIERE, O. (ed.). Meiobenthology: the microscopic motile fauna of aquatic sediments Hamburg: Springer, pp. 1-6.
GONDIM, A. I., DIAS, T. L. P., DUARTE, R. C. S., RIUL, P., LACOUTH, P. & CHRISTOFFERSEN, M. L. 2014. Filling a knowledge gap on the biodiversity of rhodolith-associated Echinodermata from northeastern Brazil. Tropical Conservation Science, 7(1), 87-99.
GUERRA-GARCÍA, J. M., FIGUEROA, J. T., NAVARRO-BARRANCO, C., ROS, M., SÁNCHEZ-MOYANO, J. E. & MOREIRA, J. 2014. Dietary analysis of the marine Amphipoda (Crustacea: Peracarida) from the Iberian Peninsula. Journal of Sea Research, 85, 508-517.
GRAVE, S. 1999. The influence of sedimentary heterogeneity on within maerl bed differences in infaunal crustacean community. Estuarine, Coastal and Shelf Science, 49(1), 153-163.
HICKS, G. R. F. 1985. Meiofauna associated with rocky shore algae. In: MOORE, P. G. & SEED, R. (eds.). The ecology of rocky coasts London: Hodder and Stoughton, pp. 36-64.
HIEBERT, T. C. 2015. Leptochelia sp. In: HIEBERT, T. C., BUTLER, B. A. & SHANKS, A. L. (eds.). Oregon estuarine invertebrates: Rudys’ illustrated guide to common species. 3rd ed. Charleston: University of Oregon Libraries and Oregon Institute of Marine Biology.
HIGGINS, R. P. & THIEL, H. 1988. Introduction to the study of meiofauna Washington: Smithsonian Institution Press.
HURLBERT, S. H. 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52(4), 577-586.
ICMBIO (Instituto Chico Mendes de Conservação da Biodiversidade). MMA (Ministério do Meio Ambiente). 2019. Costa das algas [online]. Brasília: ICMBIO-MMA. Available at: http://www.icmbio.gov.br/apacostadasalgas/ [Accessed: 17 Jul 2019].
» http://www.icmbio.gov.br/apacostadasalgas/
KIONTKE, K. & FITCH, D. H. A. 2013. Nematodes. Current Biology, 23(19), R862-R864.
LAM-GORDILLO, O., BARING, R. & DITTMANN, S. 2020. Ecosystem functioning and functional approaches on marine macrobenthic fauna: a research synthesis towards a global consensus. Ecological Indicators, 115, 106379.
LARSEN, K., GUŢU, M. & SIEG, J. 2015. Order Tanaidacea Dana, 1849. In: KLEIN, C. V. P. (ed.). Treatise on zoology - anatomy, taxonomy, biology. The crustacean 5th ed. Place: Brill, pp. 249-329.
LU, Y., YUAN, J., LU, X., SU, C., ZHANG, Y., WANG, C., CAO, X., LI, Q., SU, J., ITTEKKOT, V., GARBUTT, R. A., BUSH, S. R., FLETCHER, S., WAGEY, T., KACHUR, A. & SWEIJD, N. 2018. Major threats of pollution and climate change to global coastal ecosystems and enhanced management for sustainability. Environmental Pollution, 239, 670-680.
MARTIN, L., SUGIO, K., FLEXOR, J. M. & ARCANJO, J. D. 1996. Coastal quaternary formations of the southern part of the State of Espírito Santo (Brazil). Academia Brasileira de Ciências, 68(3), 389-404.
MARTINEZ, A. S., MENDES, L. F. & LEITE, T. S. 2012. Spatial distribution of epibenthic molluscs on a sandstone reef in the Northeast of Brazil. Brazilian Journal of Biology, 72(2), 287-298.
MARTINS, R., MAGALHÃ ES, L., PETER, A., SAN MARTÍN, G., RODRIGUES, A. M. & QUINTINO, V. 2013. Diversity, distribution and ecology of the family Syllidae (Annelida) in the Portuguese coast (Western Iberian Peninsula). Helgoland Marine Research, 67, 775-188.
MAZZUCO, A. C. A., STELZER, P. S., DONADIA, G., BERNARDINO, J. V., JOYEUX, J. C. & BERNARDINO A. F. 2019. Lower diversity of recruits in coastal reef assemblages are associated with higher sea temperatures in the tropical South Atlantic. Marine Environmental Research, 148, 87-98.
NEILL, K. F., NELSON, W. A., D’ARCHINO, R., LEDUC, D. & FARR, T. J. 2015. Northern New Zealand rhodoliths: assessing faunal and floral diversity in physically contrasting beds. Marine Biodiversity, 45(1), 63-75.
NELSON, W. A. 2009. Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research, 60(8), 787-801.
NETO, J. M., BERNARDINO, A. F. & NETTO, S. A. 2021. Rhodolith density influences sedimentary organic matter quantity and biochemical composition, and nematode diversity. Marine Environmental Research, 171, 105470.
NETTO, S. A., ATTRILL, M. J. & WARWICK, R. M. 1999. Sublittoral meiofauna and macrofauna of Rocas Atoll (NE Brazil): indirect evidence of a topographically controlled front. Marine Ecology Progress Series, 179, 175-186.
OKSANEN, J., BLANCHET, F. G., KINDT, R., LEGENDRE, P., MINCHIN, P. R., O’HARA, R. B. & OKSANEN, M. J. 2013. Package ‘vegan’. Community Ecology Package, Version [online], 2(9), 1-295. Available at: http://CRAN.R-project.org/package=vegan [Accessed: 15 Dec 2020].
» http://CRAN.R-project.org/package=vegan
OTERO-FERRER, F., MANNARÀ, E., COSME, M., FALACE, A., MONTIEL-NELSON, J. A., ESPINO, F. & TUYA, F. 2019. Early-faunal colonization patterns of discrete habitat units: a case study with rhodolith-associated vagile macrofauna. Estuarine, Coastal and Shelf Science, 218, 9-22.
PIMENTEL, C. R., VILAR, C., ROLIM, F. A., ABIERI, M. L. & JOYEUX, J. C. 2019. New records of the snow bass Serranus chionaraia (Perciformes: Serranidae) confirm an established population in the Brazilian Province. Journal of Fish Biology, 95(5), 1346-1349.
PEREIRA, N. S., MARINS, Y. O., SILVA, A. M. C., OLIVEIRA, P. G. V. & SILVA, M. B. 2008. Influência do ambiente sedimentar na distribuição dos organismos meiobentônicos do Atol das Rocas. Estudos Geológicos, 18(2), 67-80.
PRATA, J., COSTA, D. A., MANSO, C. L. D. C., CRISPIM, M. C. & CHRISTOFFERSEN, M. L. 2017. Echinodermata associated to rhodoliths from Seixas Beach, State of Paraíba, Northeast Brazil. Biota Neotropica, 17(3), e20170363
QUEIROZ, E. V., ARAÚJO, P. V. N., HAMMILL, E. & AMARAL, R. F. 2016. Morphological characteristics of rhodolith and correlations with associated sediment in a sandstone reef: Northeast Brazil. Regional Studies in Marine Science, 8(Pt 1), 133-140.
R DEVELOPMENT CORE TEAM. 2013. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing. Available at: https://www.r-project.org/ [Accessed: 15 Dec 2020].
RABELO, E. F., SOARES, M. D. O., BEZERRA, L. E. A. & MATTHEWS-CASCON, H. 2015. Distribution pattern of zoanthids (Cnidaria: Zoantharia) on a tropical reef. Marine Biology Research, 11(6), 584-592.
RIOSMENA-RODRÍGUEZ, R. 2017. Natural history of rhodolith/maërl beds: their role in near-shore biodiversity and management. Coastal Research Library, 15, 3-26.
RIUL, P., LACOUTH, P., PAGLIOSA, P. R., CHRISTOFFERSEN, M. L. & HORTA, P. A. 2009. Rhodolith beds at the easternmost extreme of South America: community structure of an endangered environment. Aquatic Botany, 90(4), 315-320.
ROBINSON, K. M. 2015. Motile cryptofaunal invertebrate assemblages in Catalina Island’s rhodolith beds in relation to physical structure and live rhodoliths. MSc. California: California State University.
ROCHA, G. A., BASTOS, A. C., AMADO-FILHO, G. M., BONI, G. C., MOURA, R. L. & OLIVEIRA, N. 2020. Heterogeneity of rhodolith beds expressed in backscatter data. Marine Geology, 423(spe2), 106136.
RUIZ-ABIERNO, A. & ARMENTEROS, M. 2017. Coral reef habitats strongly influence the diversity of macro-and meiobenthos in the Caribbean. Marine Biodiversity, 47(1), 101-111.
SÁNCHEZ-LATORRE, C., TRIAY-PORTELLA, R., COSME, M., TUYA, F. & OTERO-FERRER, F. 2020. Brachyuran crabs (Decapoda) associated with rhodolith beds: spatio-temporal variability at Gran Canaria Island. Diversity, 12(6), 223.
SARMENTO, V. C., BARRETO, A. F. S & SANTOS, P. J. P. 2011. The response of meiofauna to human trampling on coral reefs. Scientia Marina, 75(3), 559-570.
SARMENTO, V. C. & SANTOS, P. J. P. 2012. Species of Harpacticoida (Crustacea, Copepoda) from the phytal of Porto de Galinhas coral reefs, northeastern Brazil. Check List, 8(5), 936-939.
SCHRATZBERGER, M. & INGELS, J. 2018. Meiofauna matters: the roles of meiofauna in benthic ecosystems. Journal of Experimental Marine Biology and Ecology, 502, 12-25.
SCHRATZBERGER, M., MAXWELL, T. A. D., WARR, K., ELLIS, J. R. & ROGERS, S. I. 2008. Spatial variability of infaunal nematode and polychaete assemblages in two muddy subtidal habitats. Marine Biology, 153(4), 621-642.
SCIBERRAS, M., RIZZO, M., MIFSUD, J. R., CAMILLERI, K., BORG, J. A., LANFRANCO, E. & SCHEMBRI, P. J. 2009. Habitat structure and biological characteristics of a maerl bed off the northeastern coast of the Maltese Islands (central Mediterranean). Marine Biodiversity, 39(4), 251-264.
SOARES, M. D. O., ROSSI, S., MARTINS, F. A. S. & CARNEIRO, P. B. D. M. 2017. The forgotten reefs: benthic assemblage coverage on a sandstone reef (Tropical South-western Atlantic). Journal of the Marine Biological Association of the United Kingdom, 97(8), 1585-1592.
SOETAERT, K. & HEIP, C. 1995. Nematode assemblages of deep-sea and shelf break sites in the North Atlantic and Mediterranean Sea. Marine Ecology Progress Series, 125, 171-183.
STELLER, D. L., RIOSMENA‐RODRÍGUEZ, R., FOSTER, M. S. & ROBERTS, C. A. 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(Suppl 1), S5-S20.
STELZER, P. S., MAZZUCO, A. C. A., GOMES, L. E., MARTINS, J., NETTO, S. & BERNARDINO, A. F. 2021. Taxonomic and functional diversity of benthic macrofauna associated with rhodolith beds in SE Brazil. PeerJ, 9, e11903.
TEODORO, N. M. S. & COSTA, K. G. 2018. Checklist of polychaetes (Annelida: Polychaeta) from a sandstone reef of Southeastern Brazil. Revista Brasileira de Gestão Ambiental e Sustentabilidade, 5(10), 779-787.
VENEKEY, V. & SANTOS, T. M. 2017. Free-living nematodes of Brazilian oceanic islands: revealing the richness in the most isolated marine habitats of Brazil. Nematoda, 4, e122016.
VERAS, P. C., PIEROZZI JUNIOR, I., LINO, J. B., AMADO-FILHO, G. M., SENNA, A. R., SANTOS, C. S. G. & PEREIRA-FILHO, G. H. 2020. Drivers of biodiversity associated with rhodolith beds from euphotic and mesophotic zones: insights for management and conservation. Perspectives in Ecology and Conservation, 18, 37-43.
YANOVSKI, R., NELSON, P. A. & ABELSON, A. 2017. Structural complexity in coral reefs: examination of a novel evaluation tool on different spatial scales. Frontiers in Ecology and Evolution, 5, 27.
