Introduction

Materials and methods

Sampling methods

Description: The checklist was primarily based on four field surveys carried out in 2018 and 2019 at eight sites in the intertidal zone (Figs 1, 2), in the two protected areas, covering the four seasons. In addition to field surveys, previous records were obtained from databases: Jabot ("Jardim Botânico do Rio de Janeiro", JBRJ, http://www.jbrj.gov.br/jabot), Reflora ("Herbário Virtual Reflora", https://reflora.jbrj.gov.br/reflora/herbarioVirtual/) and speciesLink ("Centro de Referência em Informação Ambiental”, CRIA, https://specieslink.net/search/). Searches were based on the three municipalities "Aracruz", "Fundão" and "Serra" and only records that specified localities within protected areas' perimeters were selected. Species' names were updated following Guiry and Guiry (2023).

Figure 1.  

Shallow reef benthic assemblages adjacent to the coastline dominated by algae in the Costa das Algas EPA and Santa Cruz WR (2018-2019). A Zoanthid (Palythoa sp.) and algae; B Halimeda sp.; C Vidalia obtusilosa; D Tricleocarpa cylindrica; Е Maerls formed by living mono-specific CCA covering the sea bed associated with Dictyoperis delicatula; F Living rhodoliths surrounded by nodules covered by turf; G Living rhodoliths associated with Padina sp. and Sargassum sp.; H Collection of macroalgae in the field; Photos: (A-C) A. Bertoncini; Photos (D-H) F. Moraes.

Figure 2.  

Site location and views of the two studied MPAs. A Sampling sites in the multiple use Costa das Algas Environmental Protection Area (larger polygon) and in the no-take Santa Cruz Wildlife Reserve (smaller polygon); B Costa das Algas EPA; C Santa Cruz WR. Photos: F. Moraes.

Checklists of species with vouchers in the main national herbaria were published on the "Catálogo de Plantas das Unidades de Conservação do Brasil" (https://catalogo-ucs-brasil.jbrj.gov.br/) for both MPAs. Here, we report 30 additional species recorded in our field surveys, but not found in the herbaria. Their abundance was assessed according to the frequencies of occurrence in the eight studied sites and four different seasons in the field surveys (2018-2019), as follows: very common (VC = 28-32 occurrences); common (C = 21-27 occurrences); frequent (F = 3-10 occurrences) and rare (R = 1 or 2 occurrences). Coralline algae were often identified only at the genus level, since species level identification of these algae usually requires molecular analysis.

Quality control: Identifications were based on AlgaeBase (Guiry and Guiry 2023), identification guides, regional and local floristic studies and keys (Oliveira-Filho 1977, Amado-Filho and Yoneshigue-Valentin 1990, Nunes 1998, Nunes 2005, Guimarães 2006, Figueredo and Tâmega 2007, Pacheco 2011, Bahia 2014, Ximenes et al. 2017, Santos et al. 2020 , Coutinho et al. 2022, Wynne 2022) and validated by taxonomists.

Statistical analysis: Diversity of macroalgae of both MPAs was summarised at family and genus level, as well as endemism and status as native or non-native, based on Flora e Funga do Brasil (2023).

Data resources

Analysis

Taxonomy coverage

Two hundred and sixty-five macroalgal taxa were recorded in the protected areas, including four varieties, one subspecies and one marine angiosperm (Table 1, Suppl. material 1, Suppl. material 2). Costa das Algas EPA (250 taxa) was richer than the Santa Cruz WR (137 taxa) due to the combination of lower sampling effort (only two sampling sites) and smaller area of the latter (Fig. 3).

Figure 3.  

Number of macroalgal taxa of Rhodophyta, Chlorophyta and Ochrophyta in the Costa das Algas EPA and the Santa Cruz WR (ES).

Records of Rhodophyta consisted of 32 families, 75 genera and 143 species (60% of all taxa) in the Costa das Algas EPA and 29 families, 49 genera and 68 species (53% of all taxa) in the Santa Cruz WR. Chlorophyta consisted of 15 families, 21 genera and 57 species (24% of all taxa) in the Costa das Algas EPA and 10 families, 14 genera and 30 species (22% of all taxa) in the Santa Cruz WR. Ochrophyta was composed of seven families, 16 genera and 39 species (16% of all taxa) in the Costa das Algas EPA and five families, 14 genera and 33 species (24% of all taxa) in the Santa Cruz WR. The most species-rich families were Rhodomelaceae (37 taxa) and Corallinaceae (11 taxa) amongst Rhodophyta; Caulerpaceae (13) and Cladophoraceae (13) amongst Chlorophyta and Dictyotaceae (21) and Sargassaceae (12) amongst Ochrophyta in both MPAs.

Nine species are Brazilian endemic: Agissea inamoena, Alsidium oliveiranum, Calliblepharis jolyi, Cryptonemia delicatula, Hypnea brasiliensis, Laurencia longiramea, L. translucida (Rhodophyta); Laminaria abyssalis (Ochrophyta) and Halimeda jolyana (Chlorophyta) (Nunes 1998, Nunes 2005, Moura et al. 2015, Ximenes et al. 2017, Flora e Funga do Brasil 2023).

One hundred and four species (40% of all taxa), recorded before the 2015 themining disaster, were also presented in our 2018-2019 surveys. There were 86 new occurrences (34% of all taxa in the MPA) for the Costa das Algas EPA and 45 new ones (33% of all taxa in the MPA) for the Santa Cruz WR in the 2018-2019 surveys. On the other hand, 64 previously recorded taxa (45 Rhodophyta, 14 Chlorophyta and 5 Ochrophyta) were not found in our surveys.

Two hundred species were recorded during the four field surveys and eight sampling sites, however, 71 of which occurred only once or twice during sampling. These species were categorised as rare because they presented a very low frequency of occurrence in both MPAs. Conversely, only eight species (Codium intertextum, Anadyomene stellata, Dictyosphaeria versluysii, Lobophora variegata, Zonaria tournefortii, Hydrolithon farinosum, Ochtodes secundiramea and Dichotomaria marginata) were conspicuous and were found at all eight sampling sites in all seasons.

Discussion

Acknowledgements

Author contributions

References

Amado-Filho GM, Yoneshigue-Valentin Y (1990)
Feofíceas novas e raras para o litoral brasileiro.
Rodriguésia
42/44
:
39
‑
46
. https://doi.org/10.1590/2175-7860199019924244687004
Amado-Filho GM, Barreto MB, Marins BV, Felix C, Reis RP (2003)
Estrutura das comunidades fitobentônicas do infralitoral da Baía de Sepetiba, RJ, Brasil.
Revista Brasileira de Botânica
26
:
329
‑
34
. https://doi.org/10.1590/s0100-84042003000300006
Amado-Filho GM, Maneveldt G, Pereira Filho G, Manso RC, Bahia R, Barreto MB, Guimarães SM (2010)
Seaweed diversity associated with a Brazilian tropical rhodolith bed.
Ciencias Marinas
36
:
371
‑
391
. https://doi.org/10.7773/cm.v36i4.1782
Bahia RG (2014)
Algas Coralináceas Formadoras de Rodolitos da Plataforma Continental Tropical e Ilhas Oceânicas do Brasil: Levantamento Florístico e Taxonomia. PhD Thesis.
Escola Nacional de Botânica Tropical
,
Rio de Janeiro
,
221
pp.
Barata D (2004)
Clorofíceas marinhas bentônicas do litoral do Espírito Santo.
Instituto de Botânica, Secretaria do Meio Ambiente
,
São Paulo
,
210
pp.
Bastos AC, Moscon DM, Carmo D, Baptista-Neto JA, Quaresma VS (2015)
Modern sedimentation processes in a wave-dominated coastal embayment: Espírito Santo Bay, southeast Brazil.
Geo-Marine Letters
35
:
23
‑
36
. https://doi.org/10.1007/s00367-014-0387
Bermejo R, Vergara JJ, Hernández I (2012)
Application and reassessment of the reduced species list index for macroalgae to assess the ecological status under the Water Framework Directive in the Atlantic coast of Southern Spain
.
Ecological Indicators
12
:
46
‑
57
. https://doi.org/10.1016/j.ecolind.2011.04.008
Carneiro IM, Paiva PC, Bertocci I, Lorini M., Széchy MT (2023)
Distribution of a canopy-forming alga along the Western Atlantic Ocean under global warming: The importance of depth range.
Marine Environmental Research
188
:
106013
. https://doi.org/10.1016/j.marenvres.2023.106013
Carvalho VF (2013)
Avaliação dos impactos da urbanização sobre as comunidades de macroalgas bentônicas no litoral do Espírito Santo, Brasil. Master Thesis.
Universidade Federal Rural de Pernambuco
,
Recife
,
66
pp.
Coppo GC, Gabriel FA, Mazzuco AC, Queiroz HM, Barcellos D, Ferreira TO, Bernardino AF (2023)
Long-term impacts on estuarine benthic assemblages (2015-2020) after a mine tailing spill in SE Brazil
.
Marine Pollution Bulletin
196
:
115616
. https://doi.org/10.1016/j.marpolbul.2023.115616
Costa ES, Cagnin RC, da Silva CA, Longhini CM, Sá F, Lima AT, Gomes LE, Bernardino AF, Rodriguez-Neto R (2021)
Iron ore tailings as a source of nutrients to the coastal zone.
Marine Pollution Bulletin
171
:
112725
. https://doi.org/10.1016/j.marpolbul.2021.112725
Coutinho L, Gomes F, Sissini M, Vieira-Pinto T, Henriques M, Henriques M, Horta P, Oliveira M (2022)
Cryptic diversity in non-geniculate coralline algae: A new genus Roseolithon (Hapalidiales, Rhodophyta) and seven new species from the Western Atlantic.
European Journal of Phycology
57
:
227
‑
250
. https://doi.org/10.1080/09670262.2021.1950839
Crispino LM (2000)
Feofíceas do litoral do Espírito Santo. Master Thesis.
Universidade Estadual Paulista
,
Rio Claro
,
193
pp.
De Paula JC, Lopes-Filho EA, Carvalho WF, Coração AC, Yoneshigue-Valentin Y (2020)
Long-term changes in macroalgae assemblages reveal a gradual biodiversity loss over the last 200 years in the hypereutrophic Guanabara Bay.
Marine Environmental Research
162
:
105153
. https://doi.org/10.1016/j.marenvres.2020.105153
Díaz-Pulido G, McCook LJ, Larkum AW, Lotze HK, Raven JA, Schaffelke B, Smith JE, Steneck RS (2007)
Vulnerability of macroalgae of the Great Barrier Reef to climate change
. In: Johnson JE, Marshall PA, Authority GBRMP (Eds)
Climate change and the Great Barrier Reef: a vulnerability assessment
.
The Great Barrier Reef Marine Park Authority
,
154-192
pp. URL: http://hdl.handle.net/11017/540
Duffy J, Benedetti-Cecchi L, Trinanes J, Muller-Karger F, Ambo-Rappe R, Bostr&ouml m, Buschmann A, Byrnes J, Coles R, et al. (2019)
Toward a Coordinated Global Observing System for Seagrasses and Marine Macroalgae
.
Frontiers in Marine Science
6
https://doi.org/10.3389/fmars.2019.00317
Figueredo M, Tâmega F (2007)
Macroalgas marinhas Biodiversidade marinha da Baía da Ilha Grande
.
Ministério do Meio Ambiente
,
Brasilia
. https://doi.org/10.13140/RG.2.1.4571.4088
Flora e Funga do Brasil (2023)
Jardim Botânico do Rio de Janeiro
. http://floradobrasil.jbrj.gov.br/. Accessed on: 2023-9-21.
González-Nieto D, Oliveira M, Resendiz M, Dreckmann K, Mateo-Cid L, Senties A (2020)
Molecular assessment of the genus Sargassum (Fucales, Phaeophyceae) from the Mexican coasts of the Gulf of Mexico and Caribbean, with the description of S. xochitlae sp. nov.
Phytoxa
461
:
254
‑
274
.
Guimarães S (2003)
Uma análise da diversidade da flora marinha do estado do Espírito Santo, Brasil
.
Hoehnea
30
:
11
‑
19
.
Guimarães S (2006)
A revised checklist of benthic marine Rhodophyta from the State of Espírito Santo, Brazil.
Boletim do Instituto de Botânica
17
:
143
‑
194
.
Guiry M, Guiry G (Eds) (2023)
AlgaeBase. World-wide electronic publication, National University of Ireland, Galway.
https://www.algaebase.org. Accessed on: 2023-1-21.
Hanley ME, Firth LB, Foggo A (2024)
Victim of changes? Marine macroalgae in a changing world
.
Annals of Botany
133
(
1
):
1
‑
16
. https://doi.org/10.1093/aob/mcad185
Holz V, Bahia R, Karez C, Vieira F, Moraes F, Vale N, Sudatti D, Salgado L, Moura R, Amado-Filho G, Bastos A (2020)
Structure of rhodolith beds and surrounding habitats at the Doce River Shelf (Brazil)
.
Diversity
12
(
2
):
75
. https://doi.org/10.3390/d12020075
Horta P, Amâncio E, Coimbra C, Oliveira E (2001)
Considerações sobre distribuição e a origem da flora de macroalgas marinhas brasileiras
.
Hoehnea
28
:
243
‑
265
.
IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) (2006)
Relatório Final da Proposta de Criação das Unidades de Conservação “Área de Proteção Ambiental Costa das Algas” e “Refúgio de Vida Silvestre de Santa Cruz” na Faixa Costeira dos Municípios da Serra, Fundão e Aracruz e Região Marinha Confrontante, Estado do Espírito Santo. Vitória-ES.
MMA/Gerência Executiva do IBAMA no Estado do Espírito Santo
.
ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (2023a)
Área de Proteção Ambiental Costa das Algas e Refúgio de Vida Silvestre de Santa Cruz
. https://www.icmbio.gov.br/apacostadasalgas.. Accessed on: 2023-1-14.
ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (2023b)
Plano de manejo [livro eletrônico] : Refúgio de Vida Silvestre de Santa : área de proteção ambiental Costa das Algas.
ICMBio
,
Brasilia
. URL: https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/marinho/lista-de-ucs/apa-costa-das-algas/arquivos/plano_de_manejo___versao___livro_digital_compactado.pdf [ISBN
978-65-5693-075-6
]
Instituto Estadual de Meio Ambiente e Recursos Hídricos (2014)
Plano de Manejo da APA da Conceição da Barra
.
Governo do Estado do Espírito Santo
. URL: https://iema.es.gov.br/Media/iema/Downloads/GRN/20150508_VOLUME_II_Indice_Volume.pdf
Mazzucco AC, Stelzer PS, Bernardino AF (2020)
Substrate rugosity and temperature matters: patterns of benthic diversity at tropical intertidal reefs in the SW Atlantic
.
PeerJ,
8
:
e8289
. https://doi.org/10.7717/peerj.8289
Moura CW, Alves AM, Santos AA, Almeida WR, Moniz-Brito K, Oliveira IS, Freitas NS, Oliveira IB, Ramos GJ (2015)
Checklist of phytobenthos from Boipeba Island, Bahia, Brazil, emphasizing the morphological features of Nitophyllum punctatum (Rhodophyta, Ceramiales).
Check List
11
(
4
):
1704
. https://doi.org/10.15560/11.4.1704
Nunes JM (1998)
Catálogo de algas marinhas bentônicas do Estado da Bahia, Brasil. Acta Botanica Malacitana
.
Acta Botanica Malacitana
23
:
5
‑
21
. https://doi.org/10.24310/abm.v23i0.8547
Nunes JMDC (2005)
Rodofíceas marinhas bentônicas do estado da Bahia, Brasil. PhD Thesis
.
Universidade de São Paulo
,
São Paulo
,
410
pp.
Oliveira EC, Qi Y (2003)
Decadal changes in a polluted bay as seen from its seaweed flora: the case of Santos Bay in Brazil
.
AMBIO
32
:
403
‑
405
. https://doi.org/10.1579/0044-7447-32.6.403
Oliveira-Filho EC (1969)
Algas marinhas do sul do estado do Espírito Santo (Brasil) I. Ceramiales
.
Boletim da Faculdade de Ciências e Letras da Universidade de São Paulo
26
:
1
‑
277
. https://doi.org/10.11606/issn.2318-5988.v26i1p7-277
Oliveira-Filho EC (1976)
Deep water marine algae from Espírito Santo State (Brazil)
.
Boletim de Botânica da Universidade de São Paulo
4
:
73
‑
80
. https://doi.org/10.11606/issn.2316-9052.v4i0p73-79
Oliveira-Filho EC (1977)
Algas marinhas bentônicas do Brasil. Habilitation Thesis
.
Universidade de São Paulo
.
Oliveira N, Bastos AC, Quaresma VS, Vieira FV (2020)
The use of Benthic Terrain Modeler (BTM) in the characterization of continental shelf habitats.
Geo-Marine Letters
40
:
1087
‑
1097
. https://doi.org/10.1007/s00367-020-00642-y
Oliveira ND, Lavagnino AC, Rocha GA, Moura R, Bastos AC (2023)
Geomorphological significance of shelf-incised valleys as mesophotic habitats
.
Frontiers in Remote Sensing
4
:
1111825
. https://doi.org/10.3389/frsen.2023.1111825
Pacheco MR (2011)
Macroalgas marinhas associadas a bancos de rodolitos do infralitoral do Espírito Santo, Brasil. PhD Thesis
.
Universidade de São Paulo
,
São Paulo
,
371
pp.
Quaresma VD, Catabriga G, Bourguignon SN, Godinho E, Bastos AC (2015)
Modern sedimentary processes along the Doce river adjacent continental shelf.
Brazilian Journal of Geology
45
:
635
‑
644
. https://doi.org/10.1590/2317-488920150030274
Quaresma VS, Aguiar VM, Bastos AC, Oliveira KS, Vieira FV, S&aacute F, Baptista Neto JA (2021)
The impact of trace metals in marine sediments after a tailing dam failure: the Fundão dam case (Brazil)
.
Environmental Earth Sciences
80
:
1
‑
16
. https://doi.org/10.1007/s12665-021-09817-x
Santos GN, Pestana EM, Santos CC, Cassano V, Nunes JM (2020)
Diversity of Galaxauraceae (Nemaliales, Rhodophyta) in northeastern Brazil: new record and two new species, Dichotomaria viridis sp. nov. and Tricleocarpa laxa sp. nov.
Phytotaxa
2020
:
73
‑
103
. https://doi.org/10.11646/phytotaxa.454.2.1
Scherner F, Horta PA, Oliveira EC, Simonassi JC, Hall-Spencer JM, Chow F, Nunes JM, Pereira SM (2013)
Coastal urbanization leads to remarkable seaweeds species loss and community shifts along the SW Atlantic
.
Marine Pollution Bulletin
7
:
106
‑
115
. https://doi.org/10.1016/j.marpolbul.2013.09.019
WFD-UKTAG (Water Framework Directive - United Kingdom Technical Advisory Group) (2009)
United Kingdom Technical Advisory Group “UKTAG” coastal water assessment methods macroalgae: Macroalgae – rocky shore reduced species list
.
Water Framework Directive - United Kingdom Technical Advisory Group (WFD-UKTAG)
. URL: https://webarchive.nationalarchives.gov.uk/ukgwa/20110908153222/http://www.wfduk.org/bio_assessment/
Wynne MJ (2022)
Checklist of benthic marine algae of tropical and subtropical Western Atlantic
.
5th Revision
.
Nova Hedwiga
,
Beiheft
,
153
pp.
Ximenes CF, Cassano V, Oliveira-Carvalho MD, Bandeira-Pedrosa ME, Gurgel CF, Verbruggen H, Pereira SM (2017)
Systematics of the genus Halimeda (Bryopsidales, Chlorophyta) in Brazil including the description of Halimeda jolyana sp. nov.
Phycologia
56
(
4
):
369
‑
381
. https://doi.org/10.2216/16-77.1.

Supplementary materials