Accessibility / Report Error

Diversity of benthic fauna of rhodoliths and sediments deposited on sandstone reefs in Southeast Brazil

Abstract

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.

Descriptors:
Costa Das Algas environmental protection area; Faunal assemblage; Macrofauna; Meiofauna; Biodiversity

INTRODUCTION

Sandstones reefs play an important role in the coastal zone, providing habitats for a great variety of organisms such algae and benthic invertebrates sessile and motile (Martinez, Mendes and Leite, 2012MARTINEZ, 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.; Teodoro and Costa, 2018TEODORO, 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.). This environment features spatial heterogeneity, with high associated biodiversity and complex biological interactions (Soares et al., 2017SOARES, 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.; Queiroz et al., 2016QUEIROZ, 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.). Sandstone reefs differ from coral reefs by their sediment composition and typical rocky shore, mainly due to their gentle slope (Rabelo et al., 2015RABELO, 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.). Despite its ecological and socio-economic importance given that it shelters species of commercial interest, intertidal sandstone reefs are less studied than other hard bottom environments (Soares et al., 2017SOARES, 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.), with a resulting knowledge gap about reef biodiversity, mainly when we refer to mobile fauna.

In the state of Espírito Santo, southeastern Brazil, the north sector of the inner shelf is associated with abrasion terraces formed by lateritic concretions (Albino and Suguio, 2011ALBINO, 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.). The beaches of this region are characterized ferruginous sandstone reefs in the intertidal, and the sedimentary composition is predominantly bioclastic material, such fragments of carbonate organisms like bryozoans, coralline algae, benthic foraminifera, and mollusks (Albino, Neto and Oliveira, 2016ALBINO, J., NETO, N. C. & OLIVEIRA T. C. A. 2016. The beaches of Espírito Santo. Coastal Research Library, 17, 333-361.). Rhodolith nodules also contribute to local sedimentation, which are brought to the beach by storms or strong currents (Dias and Villaça, 2012DIAS, 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.; Andrades et al., 2014ANDRADES, 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.) brought in from adjacent rhodolith beds.

Rhodoliths are free-living nodules composed of coralline algae (Bosence, 1983BOSENCE, D. W. J. 1983. Description and classification of rhodoliths (rhodoids, rhodolites). In: PERYT, T. M. (ed.). Coated grains. Berlin: Springer-Verlag, pp. 217-224.) with three-dimensional structures and can be classified as ‘ecosystem engineers’ because they alter the physical features of the habitat (Bruno and Bartness, 2001BRUNO, J. F. & BERTNESS, M. D. 2001. Habitat modification and facilitation in benthic marine communities. Marine Community Ecology, 201-218.; Nelson, 2009NELSON, W. A. 2009. Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research, 60(8), 787-801.). The different growth forms and structures of the nodules form a microhabitat by providing a hard substrate for epibionts like other algae, sessile organisms, and small cryptic invertebrates that live inside the nodules, called cryptofauna (Steller et al., 2003STELLER, 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.; Amado-Filho and Pereira-Filho, 2012AMADO-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.; Gondim et al., 2014GONDIM, 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.). The cryptofauna of rhodoliths is generally composed of small annelids, crustaceans, mollusks, nematodes, and other groups that use the host substrate as shelter and food (Figueiredo et al., 2007FIGUEIREDO, 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.; Costa et al., 2019COSTA, 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., Sánchez-Latorre et al., 2020SÁNCHEZ-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., Otero-Ferrer et al., 2019OTERO-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., Neto, Bernardino & Netto, 2021NETO, 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., Stelzer et al., 2021STELZER, 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.). The cryptofauna associated with the rhodoliths is represented by two ecological compartments, macro- and meiofauna. A joint analysis of both components of the benthic fauna is necessary due to the lack of information on the role of rhodoliths as a shelter for smaller organisms and larval stages.

Operationally, benthic invertebrates are classified according to the mesh opening size used to retain them. The meiofauna comprises organisms retained in the 45-63 µm mesh size, while the macrofauna are organisms 500-5000 µm in size (Giere, 2009GIERE, O. 2009. Introduction to meiobenthology. In: GIERE, O. (ed.). Meiobenthology: the microscopic motile fauna of aquatic sediments. Hamburg: Springer, pp. 1-6.; Ruiz-Abierno and Armenteros, 2017RUIZ-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.). In addition to body size, the life history traits of the components are different (Gallucci et al., 2020GALLUCCI, 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.). Macrofauna is more mobile and has a planktonic larval stage, which enables greater dispersal. In contrast, meiofauna has direct benthic development and less mobility in the substrate (Schratzberger et al., 2008SCHRATZBERGER, 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.). Meio- and macrofauna contribute fundamentally to the ecosystem processes and functioning of marine environments (Neto, Bernardino and Netto, 2021NETO, 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., Lam-Gordillo, 2020LAM-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.). They act in nutrient cycling, decomposition of organic matter, energy transfer to higher trophic levels, bioturbation of sediments, and are commonly used as bioindicators due to their sensitivity to environmental disturbances (Schratzberger and Ingels, 2018SCHRATZBERGER, M. & INGELS, J. 2018. Meiofauna matters: the roles of meiofauna in benthic ecosystems. Journal of Experimental Marine Biology and Ecology, 502, 12-25.; Baldrighi and Manini, 2015BALDRIGHI, E. & MANINI, E. 2015. Deep-sea meiofauna and macrofauna diversity and functional diversity: are they related? Marine Biodiversity, 45(3), 469-488.).

In general, the presence of rhodoliths in the environment increases the biotic and structural complexity of the habitat, making more niches available (Figueiredo et al., 2007FIGUEIREDO, 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.; Berlandi, Figueiredo and Paiva, 2012BERLANDI, 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.) and significantly increasing local biodiversity (Riosmena-Rodríguez, 2017RIOSMENA-RODRÍGUEZ, R. 2017. Natural history of rhodolith/maërl beds: their role in near-shore biodiversity and management. Coastal Research Library, 15, 3-26.). Some studies indicate that rhodoliths have higher richness and associated diversity compared to those in the surrounding sandy bottom and/or under the beds (Steller et al., 2003STELLER, 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.; Foster et al., 2013FOSTER, 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., Gabara et al., 2018GABARA, 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.; Stelzer et al., 2021STELZER, 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.). However, these works focus on macrofauna, with studies involving meiofauna as an important promoter of biodiversity associated with rhodoliths being scarce (Neto, Bernardino & Netto, 2021NETO, 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.). Moreover, sampling is mostly carried out on beds, which are massive agglomerations of rhodoliths (Foster, 2001FOSTER, M. S. 2001. Rhodoliths, between rocks and soft places. Journal of Phycology, 37(5), 659-657.), constantly submerged, and at greater depths. Investigations of biodiversity associated with these algae in shallow intertidal or subtidal environments are neglected.

Therefore, the objective of the present study was to investigate the diversity of the benthic fauna (macro- and meiofauna) on different substrates (rhodoliths vs. unconsolidated sediment) in the sandstone reef. We expected that the fauna associated with the rhodoliths to be more diverse compared to unconsolidated sediment. We also investigated whether there are differences in benthic community structure between reef zones.

METHODS

Study area

The study was conducted on Gramuté Beach in the state of Espírito Santo, on the southeast coast of Brazil (19º58′21.48′′S, 40º08′14.32′′W) (Figure 1). The area is in the Environmental Protected Area (EPA) of Costa das Algas and is considered of high conservation importance. The site was created to protect biological diversity, mainly environments colonised by algae and associated benthic fauna, mangroves, coastal vegetation, and sedimentary formations (MMA/ICMBio, 2019ICMBIO (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/apacostadasalga...
).

Figure 1
Location map of the study area. Black circle indicates Gramuté Beach.

The region’s geomorphology is characterized by abrasion terraces of the Barreiras Formation (Martin et al., 1996MARTIN, 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.) that extend from the inner continental shelf to the coast. The intertidal and subtidal zones of Gramuté beach are mainly composed of ferruginous sandstone reefs. The reef structures, which are less than one meter in height, are exposed during low tide, and extensive tide pools form in the eroded reef spaces. In some places on the reefs, deposits of bioclastic sediment occurs, resulting from the intense fragmentation or encrustation of carbonate secreting organisms (Albino and Suguio, 2011ALBINO, 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.). This deposit forms a layer of unconsolidated sediment a few centimeters in thickness.

Field and laboratory procedures

To investigate the diversity of the benthic fauna of the unconsolidated sediments and associated rhodoliths, we sampled at three-month intervals for one year (May, August, and December 2013 and February 2014) in three beach zones: shallow subtidal (<1m depth), intertidal, and tidal pool. We collected four replicates of each substrate per zone. Samples were always collected during low spring tides. This study was authorised by the Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio, under SISBIO (Biodiversity Information and Authorization System) license number 23658-2. Although sampling occurred over time, this work avoided a temporal analysis of the fauna.

To sample the unconsolidated sediment, we used 15cm x 15cm PVC squares randomly distributed in each zone to sample the macrofauna. We scraped the sediment from the delimited area with a spatula and immediately placed it in 0.5mm mesh bags to ensure organism retention. We fixed the contents in the field with 10% formaldehyde. Due to the irregularity of the sandstone reefs, the sampled sediment layers had different thicknesses, all greater than 5cm. Adjacent to the squares, we collected meiofauna with a plastic syringe (2 cm in diameter to a depth of 5 cm), added them to plastic jars, and fixed them immediately in 10% formalin. To analyze the meio- and macrofauna communities associated with the rhodoliths, we collected individual nodules with average sizes between 3.5 and 8.5. We placed each nodule in labeled plastic bags containing 7% magnesium chloride to anesthetize the associated fauna. After two hours, they were fixed with 10% formaldehyde.

Data analysis

To compare the contribution of each taxonomic group of macrofauna and meiofauna between substrates, the relative abundance of each was calculated. Univariate measures for both components of invertebrate fauna included number of taxa, Shannon-Wiener diversity (H’-Log2), and rarefaction (ES50). The rarefaction index was less dependent on sample size (Soetaert and Heip, 1995SOETAERT, 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.) and based on the Sanders rarefaction technique, as modified by Hurlbert (1971)HURLBERT, S. H. 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52(4), 577-586.. Using this index, the expected number of species (ES) for each sample was calculated for a given number of individuals. To compare univariate measures between different substrates (sediments and rhodoliths) and different zones, variance analysis using a generalised linear model (GLM) was conducted. After applying normality and homoscedasticity tests and residue analysis, we built models with the appropriate distribution in accordance with the data set, Gaussian for normal data, or Poisson for non-normal count data. The ecological descriptor data were analysed using ‘VEGAN’ (Oksanen et al., 2013OKSANEN, 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...
), and models were analysed using the GLM and ANOVA functions of the R package ‘CAR’ in the R program environment (R Development Core Team, 2013R 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].
https://www.r-project.org/...
).

Because of differences in sample size and units of density between the substrates (volumetric (ind./cm3) for rhodoliths and area (ind./cm2) for sediment), we used relative abundance data for multivariate analysis. We calculated the relative abundance of each taxon on the two substrates using the formula Ra (%) = (ni x 100)/N, where ni is the total abundance of the taxon i and N is the total abundance of the sample.

To examine variations in species composition between unconsolidated sediment and rhodoliths and in different zones, we applied nonmetric multidimensional scaling (nMDS). A similarity matrix was constructed using square root transformation and the Bray-Curtis coefficient. To assess differences in the composition of benthic fauna between substrates and zonation, a repeated-measure permutational analysis of variance (PERMANOVA) was used (Anderson, Gorley and Clarke, 2008ANDERSON, M. J., GORLEY, R. N. & CLARKE, K. R. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E.). When PERMANOVA showed significant differences (p<0.05), a pair-wise comparison (999 permutations) was conducted to explore differences among pairs of levels of the selected factor. Similarity percentage analysis SIMPER (Clarke, 1993CLARKE, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1), 117-143.) was used to identify invertebrate taxa contributing to differences in the main factors identified by PERMANOVA. All multivariate and diversity analyses were performed using PRIMER v.7 and its add-on package PERMANOVA+ (Clarke and Warwick, 2001CLARKE, K. R. & WARWICK, R. M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd ed. Plymouth: PRIMER-E.; Anderson, Gorley and Clarke, 2008ANDERSON, M. J., GORLEY, R. N. & CLARKE, K. R. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E.).

RESULTS

Meiofauna

For meiofauna, 3,061 organisms and 12 taxa were recorded in the sediment, and 21,933 organisms and 16 taxa were associated with rhodoliths, totaling 24,994 individual organisms registered in the present study. The mean density found in sediment and rhodoliths was 203 ind./100 cm3 and 1790 ind./100 cm3, respectively. Copepoda dominated the meiofauna, with 54.3% in sediment and 56.4% in rhodoliths). Numerically, nematodes ranked second among taxons with 14.8% in sediment and 25.1% in rhodoliths (Figure 2). The list of taxonomic groups associated with the unconsolidated sediment and rhodoliths on the sandstone reef at Gramuté Beach can be seen in Supplementary Table S1.

Figure 2
Taxonomic groups found in the present study and relative contribution of the main groups of meiofauna associated with rhodoliths and unconsolidated sediment.

The number of meiofauna taxonomic groups was significantly higher in rhodoliths (16.145 ± 6.115) than in sediments (9.45 ± 4.71; Pr(>Chi) = <0.001). Equitability (J′) was also higher in rhodoliths (J’ = 0.723 ± 0.133), demonstrating greater uniformity in the distribution of taxa compared to unconsolidated sediment (J’ = 0.5604 ± 0,087; F = 52.013, p <0.001) (Figure 3). Equitability was also significantly different in sediment vs. zonation interaction (F = 3.190, p <0.04). Though diversity and ES50 were also higher in the rhodoliths, the difference was not statistically significant. The exploratory analysis nMDS (Figure 4) and PERMANOVA multifactorial found significant differences in the meiofaunal community structure between substrates (Table 2). A-posteriori pairwise comparisons indicate clear distinctions between meiofauna of unconsolidated sediment and rhodoliths (t = 5.570; p =0.001). However, zonation did not show well-defined groupings; there was no significant difference. SIMPER showed an average dissimilarity of 45.6% in meiofauna composition between substrates, mainly due to differences in abundance of Nematoda and Copepoda (Table 1).

Table 1
Percentage similarity (SIMPER) of meiofauna associated with rhodoliths and unconsolidated sediment.
Table 2
Results from the multivariate repeated measure PERMANOVA to test effects of substrate (sediment/rhodoliths) and zonation (subtidal/intertidal/tidal pool) on faunal descriptors and pair-wise comparisons for meio- and macrofauna; macrofauna as presence/absence data only. Significant P-values are in bold.

Figure 3
Number of taxa and equitability (J') of meiofauna in sediment (white) and rhodolith (grey) in subtidal (ST), intertidal (IT) and tidal pool (TP) zones.

Figure 4
nMDS ordination for meiofauna density in rhodoliths (black circles) and sediments (grey triangles).

Macrofauna

A total of 128 macrobenthic taxa were recorded in this study, 74 in sediment (22 exclusive) and 104 in rhodoliths (52 exclusive). In total, 8,252 macrofauna individuals were found in both substrates, with 5,374 organisms occurring as infauna in the unconsolidated sediment and 2878 organisms associated with rhodoliths. The taxonomic list of macrofauna organisms can be seen in Supplementary Table S2.

Polychaeta and Crustacea were the most abundant group in both substrates. In total, 31 families of polychaetes were identified, of which Syllidae and Spionidae were the most abundant (80.1 and 4.9%, respectively). In both substrates, Syllidae polychaetes were present in all samples.

Among crustaceans, Tanaidacea and Amphipoda were dominant in both substrates. Amphipoda, with 11 identified families, was the most abundant order associated with rhodoliths, mainly represented by Globosolembos sp. Tanaidacea was the most abundant taxon in unconsolidated sediments, represented by 4 families, with the genus Leptochelia sp. being the most abundant.

GLMs showed that both substrates and zonation had a significant effect on the macrofauna community structure. The number of taxa (F= 36.653, p<0.0001) ES50 (F= 67.048, p<0.0001) and diversity (Pr(>Chi) = 0.0002) were significantly higher in rhodoliths (S = 16.145 ± 6.115; ES50 = 13.771 ± 4.396; H’= 3.109 ± 0.597) than in sediments (S = 9.479 ± 4.766; ES50 = 8.406 ± 3.965; H’=1.941 ± 0.915) (Figure 5). According to nMDS ordination, there was a clear distinction in macrofauna structure between substrate. As such, PERMANOVA detected significant results between substrates and zonation (Table 2, Figure 6).

Figure 5
Number of taxa, ES50 and diversity (H') of macrofaunal at sediment (white) and rhodolith (grey). Zones: ST = subtidal, IT = intertidal, TP = tidal pool

Figure 6
nMDS ordination for macrofauna relative abundance data in Gramuté Beach and for zones (tidal pool, intertidal and subtidal). Representation of rhodoliths (dark circles) and sediments (grey triangles).

SIMPER analyses of relative abundance data showed a considerable dissimilarity (74.71%) in average species composition between substrates. The amphipod Globosolembos sp., the polychaete Nematonereis sp., and the echinoderms of the Ophiuroidea class had higher relative abundance in the rhodolith samples, while polychaetes of the family Syllidae and Nematoda were more frequent in unconsolidated sediment. These five taxa were mainly responsible for the dissimilarity between the substrates (Table 3).

Table 3
Percentage similarity (SIMPER) of macrofauna associated with rhodoliths and unconsolidated sediment.

DISCUSSION

Structurally more complex environments favour the presence of a diverse benthic fauna (Yanovski et al., 2017YANOVSKI, 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.; Otero-Ferrer et al., 2019OTERO-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.). In rhodoliths, the properties that provide complexity to microhabitats are shape, volume, porosity, size of the nodules, amount of sediment trapped in the holes, and epiphytic algae adhered to surfaces (Amado-Filho et al., 2010AMADO-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.; Veras et al., 2020VERAS, 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.). Thus, the presence of free nodules on the abrasion terrace on Gramuté Beach increases the possibility of shelter and protection for various organisms and corroborates the hypothesis that benthic fauna richness and diversity (meiofauna and macrofauna) in sandstones reefs is higher in rhodolith beds than in the sediment deposited in the surroundings.

Steller et al. (2003)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. and Robinson (2015)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. also demonstrated that greater species richness and diversity are typically associated with live rhodoliths rather than unconsolidated gravelly sediments and algae fragments. More recently, Stelzer et al. (2021)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. investigated the fauna associated with rhodolith beds on the continental shelf adjacent to Gramuté Beach at the isobath of approximately 50m and compared it to the sediment under the beds. As expected, the authors found higher numbers of species in the algae and higher functional diversity. Our results demonstrate that, in the same way as on a rhodolith bank on the continental shelf, rhodoliths of shallow intertidal or subtidal environments also increase the richness and diversity of the benthos.

The present study is the first to include meiofauna in a comparison between rhodolith nodules and adjacent sediment in a beach environment with intertidal sandstone reefs. Although knowledge about rhodolith beds has developed over the past few decades in various aspects, such as geological, taxonomic, and ecological (Amado-Filho et al, 2017AMADO-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.; Costa et al., 2021aCOSTA, 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.; Otero-Ferrer, et al., 2019OTERO-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.; Riul et al., 2009RIUL, 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.; Rocha et al., 2020ROCHA, 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.), the interaction patterns and processes with the benthic cryptofaunal communities, especially the meiofauna, remain poorly studied.

Shratzberger and Ingels (2017) highlighted the importance of knowledge about the role of meiofauna in benthic ecosystems. In the coastal region, where the environment is constantly subject to anthropogenic stressors (Lu et al., 2018LU, 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.), meiofaunal communities are less vulnerable to disturbance than macrofauna. Due to their continuous reproduction strategy, recolonization of disturbed sediments by meiofauna is facilitated (Costa and Netto, 2014COSTA, 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.) in contrast to the slower recolonization of macrofauna. Therefore, meiofauna activities may increase the resilience of ecosystem processes, such as energy transfer and nutrient regeneration (Baldrighi and Manini, 2015BALDRIGHI, E. & MANINI, E. 2015. Deep-sea meiofauna and macrofauna diversity and functional diversity: are they related? Marine Biodiversity, 45(3), 469-488.).

Multivariate analyses (nMDS, PERMANOVA and SIMPER) showed variations in macrofauna and meiofauna community structure between substrates, as well as spatial differences between the subtidal, intertidal, and tidal pools for the macrofauna. Stelzer et al. (2021)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. also observed differences in macrofauna composition between sediments under beds and rhodoliths. The authors attribute these changes to a high turnover of taxa between substrates and to the fact that macrofauna of the unconsolidated sediment is not a subgroup of species inhabiting the nodules (and vice versa). Differences in faunal composition and community descriptors between zonations were expected. Because it is an intertidal environment alternating between emersed and submerged periods, the zones have different hydrodynamics, daily variations in salinity and temperature, and availability of food (Correia et al., 2018CORREIA, 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.). Therefore, the taxonomic composition of the community may be different among the beach zones due to the distinct responses and adaptations of the taxa to environmental variations (Celentano et al., 2019CELENTANO, 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.).

Regarding the meiofauna taxonomic groups composition, we highlight that the higher richness in the rhodoliths is due to the exclusive presence of juveniles of the groups Priapulida, Sipuncula, Cladocera, Cumacea, and Tanaidacea, which are components of the temporary meiofauna (Bianchelli et al., 2010BIANCHELLI, 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.). Thus, when they achieve the adult stage, with a larger body size, these can become components of the macrofauna.

The taxonomic groups that contributed the most to meiofauna density were the same for both substrates studied. High densities of Copepoda and Nematoda, such as those recorded in the present study, were also found in studies of carbonate sediments deposited on the coral reefs of Atol das Rocas (Netto, Attrill and Warwick, 1999NETTO, 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.; Pereira et al., 2008PEREIRA, 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.), which has granulometric characteristics similar to Gramuté Beach. Sarmento, Barreto and Santos (2011)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., investigating the meiofauna associated with sediments adjacent to sandstone reefs in Porto de Galinhas (northeast of Brazil), also verified the dominance of these two groups. In sediments characterized by the predominance of coarse sand, copepods are generally the dominant group because they are well adapted to high energy environments due to their brief life cycle and preference for oxygen-rich environments (Hicks, 1985HICKS, 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.; Higgins and Thiel, 1988HIGGINS, R. P. & THIEL, H. 1988. Introduction to the study of meiofauna. Washington: Smithsonian Institution Press.). The meiofauna associated with algae is also dominated by copepods, mostly of the order Harpacticoida (Sarmento and Santos, 2012SARMENTO, 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.).

Nematoda, the second most abundant group of meiofauna, also occurred as macrofauna in the unconsolidated sediment as the third taxonomic group in total number of individuals. Diversity in mouth parts and the small and elongated body of Nematoda allow them to occupy interstitial spaces in several ecosystems with unique characteristics (Kiontke and Fitch, 2013KIONTKE, K. & FITCH, D. H. A. 2013. Nematodes. Current Biology, 23(19), R862-R864.; Venekey and Santos, 2017VENEKEY, 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.).

In both substrates, polychaetes contributed most to the abundance of macrofauna, corroborating several studies investigating the community of associated invertebrates (Figueiredo et al., 2007FIGUEIREDO, 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.; Costa et al., 2021bCOSTA, 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.; Stelzer et al., 2021STELZER, 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.). In this study, the Syllidae family was predominant among polychaetes. This family is one of the most diverse and widely distributed in the world and can be found in high densities on various substrates, including calcareous algae and corals reefs (Antoniadou and Chintiroglou 2006ANTONIADOU, C. & CHINTIROGLOU, C. 2006. Trophic relationships of polychaetes associated with different algal growth forms. Helgoland Marine Research, 60, 39-49.), mainly in shallow water. General feeding and reproduction strategies, active and mobile lifestyles, and the ability to move in interstitial spaces are factors that may contribute to the success of this family in various environments (Martins et al., 2013MARTINS, 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.; Fukuda, 2017FUKUDA, M. V. 2017. Aspectos reprodutivos de Syllidae (Annelida,“Polychaeta”). Revista Brasileira de Zoociências, 17, 51-54.).

The subphylum Crustacea was the second most abundant macrofauna in both substrates. Peracarid crustaceans are commonly associated with algae and carbonaceous sediments (Bueno et al., 2016BUENO, 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.) due to a wide variety of life modes, such as free-living or tube-building, and various feeding modes, suggesting that organisms in this group can exploit a range of resources (Guerra-Garcia et al., 2014GUERRA-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.). The great abundance of amphipods associated with rhodoliths was also described by other authors, who pointed out that amphipods and polychaetes were the most dominant cryptofauna (De Grave, 1999GRAVE, 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.; Figueiredo et al., 2007FIGUEIREDO, 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.; Neill et al., 2015NEILL, 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.; Robinson, 2015ROBINSON, 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.). In unconsolidated sediment, there was a greater representation of Tanaidacea, most of which belonging to the genus Leptochelia sp., considered the best adapted and most abundant genus found in shallow waters worldwide (Hiebert, 2015HIEBERT, 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.; Larsen, Gutu and Sieg, 2015LARSEN, 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.).

The echinoderms of the Ophiuroidea class were also represented in the fauna associated with rhodoliths. Gondim et al. (2014)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. had already observed that echinoderms have a preference for rhodoliths. On a rhodolith bank in Paraíba, Brazil, these authors recorded greater richness and diversity of echinoderms than in other marine environments within the same geographical region. More data on species assemblages of echinoderms and other phyla are needed to understand lifestyles and life cycles. Do they complete the entire life cycle inside the nodule or just part of early development? Can they migrate to other environments (Prata et al., 2017PRATA, 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)? These are but two of the many questions to be addressed in future studies of this unique environment and its ecology.

In studies with rhodoliths, care should be taken when comparing results because estimates of ecological indices depend on sample design (Sciberras et al., 2009SCIBERRAS, 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.). Research investigating crypofauna associated with rhodoliths use different methodological approaches. For example, Steller et al. (2003)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. and Trejo et al. (2020) sampled random rhodoliths arranged in different transects on different beds in California and New Zealand. The sampling unit for the density of associated organisms was ind/cm3, and they already used the size measurements of each nodule. However, Neto, Bernardino & Netto (2021)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., and Stelzer et al. (2021)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. delimited squares on beds in southeastern Brazil and collected all individuals. The sampling unit for density of organisms was per unit area (m2). In this study, we randomly collected individual rhodoliths in different zonations of a sandstone reef between seas and the unconsolidated sediment per square. The difference in units of measurement between substrates (cm3 for rhodolith nodules vs. cm2 for sediment of squares) used to analyze macrofauna in the present study did not allow for a more detailed comparison between abundance and density of the associated fauna. When comparing distinct substrates (such as unconsolidated sediment and rhodolith beds), we suggest that a sampling strategy be devised to measure parameters in a common unit of measurement, preferably volume to quantify both substrates (i.e., cm3).

In terms of significance, this study was the first to verify the composition of benthic macrofauna and meiofauna in rhodolith in intertidal environments. The scarcity of information on the subject makes it difficult to discuss the interaction between fauna associated with rhodoliths and unconsolidated sediments and the processes involved, such as turnover and species and interspecies interactions. Gramuté Beach is an environment composed of a mosaic of habitats, with structural elements such as hard-bottom, sandy beach, tide pools, and a great diversity of algal fronds in the infralittoral. Carvalho and Barros (2017)CARVALHO, L. R. S. & BARROS, F. 2017. Physical habitat structure in marine ecosystems: the meaning of complexity and heterogeneity. Hydrobiologia, 797(2), 1-9. state that habitats with a wide variety of elements support greater richness and abundance of organisms. As a conservation unit with scant information on local biodiversity, still without a management plan, and with scarce studies on the faunal composition (Mazzuco et al., 2019MAZZUCO, 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.; Pimentel et al., 2019PIMENTEL, 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.), there is a need for more information to consolidate conservation status.

ACKNOWLEDGMENTS

We would like to thank Professor Mauricio Hostim for his availability and orientation, NUBEM for support in the analyses, specialists Jesser Fidelis and Franklin Santos for assistance in species identification, and Guilherme Pereira Filho and Luiz Fernando Duboc for valuable contributions.

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].
    » https://www.r-project.org/
  • 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.

Edited by

Associate Editor: Karen Diele

Publication Dates

  • Publication in this collection
    22 Apr 2022
  • Date of issue
    2022

History

  • Received
    06 Apr 2021
  • Accepted
    27 Jan 2022
Instituto Oceanográfico da Universidade de São Paulo Praça do Oceanográfico 191, CEP: 05508-120, São Paulo, SP - Brasil, Tel.: (11) 3091-6501 - São Paulo - SP - Brazil
E-mail: diretoria.io@usp.br