Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South-western Atlantic), reveal unique ichthyofauna and need for conservation

Although several studies on the ichthyofauna of the Fernando de Noronha Archipelago have been carried out, its mesophotic fish diversity has never been surveyed before. Here we used SCUBA and technical rebreather diving, baited remote underwater videos and remotely operated vehicle to record shallow (≤ 30 m depth) and mesophotic (31 to 150 m depth) fishes. Nineteen fish species belonging to 14 families are reported here as new records, representing an increase of 8.2% in marine fish richness for the region, which now has a total of 250 species and 77 families. These new records include four potential new species and highlight the importance of surveying mesophotic ecosystems, even in well studied sites. Our results also emphasize the need for protection and attention to the unique ichthyofauna found at mesophotic depths.

Keywords:
BRUVS; Marine Protected Area; Oceanic Island; Rebreather; Remotely Operated Vehicle

Authorship

Caio R. Pimentel

Programa de Pós-Graduação em Oceanografia Ambiental, Dep. de Oceanografia e Ecologia, Univ. Federal do Espírito Santo, Av. Fernando Ferrari, 514, Goiabeiras, 29075-910 Vitória, ES, Brazil. (CRP) caiopimentelr@gmail.com; (JCJ) jean.joyeux@ufes.br; (ASM) agnaldo.ufes@gmail.com; (JBT) jboceano@gmail.com; (JLG) gaspa.vix@gmail.com; (SDTD) dtdstephanie@gmail.com.Universidade Federal do Espírito SantoBrazilVitória, ES, Brazil Programa de Pós-Graduação em Oceanografia Ambiental, Dep. de Oceanografia e Ecologia, Univ. Federal do Espírito Santo, Av. Fernando Ferrari, 514, Goiabeiras, 29075-910 Vitória, ES, Brazil. (CRP) caiopimentelr@gmail.com; (JCJ) jean.joyeux@ufes.br; (ASM) agnaldo.ufes@gmail.com; (JBT) jboceano@gmail.com; (JLG) gaspa.vix@gmail.com; (SDTD) dtdstephanie@gmail.com.

California Academy of Sciences, 94118 San Francisco, CA, USA. (LAR) lrocha@calacademy.org; (BS) bshepherd@calacademy.org; San Francisco State University, 94132 San Francisco, CA, USA, (HTP) htpinheiro@gmail.com; (TP) tphelps@calacademy.org; (HTP) htpinheiro@gmail.com.California Academy of SciencesUSASan Francisco, CA, USA California Academy of Sciences, 94118 San Francisco, CA, USA. (LAR) lrocha@calacademy.org; (BS) bshepherd@calacademy.org; San Francisco State University, 94132 San Francisco, CA, USA, (HTP) htpinheiro@gmail.com; (TP) tphelps@calacademy.org; (HTP) htpinheiro@gmail.com.

http://orcid.org/0000-0003-4110-1249

Luiz A. Rocha

http://orcid.org/0000-0003-4011-569X

Bart Shepherd

http://orcid.org/0000-0002-8918-1551

Tyler A. Y. Phelps

http://orcid.org/0000-0001-7893-643X

Jean-Christophe Joyeux

http://orcid.org/0000-0002-1281-4154

Agnaldo S. Martins

http://orcid.org/0000-0003-2160-1326

Carlos Eduardo Stein

Associação Ambiental Voz da Natureza, Rua Coronel Shuwab Filho, 104, 29052-070 Vitória, ES, Brazil. (CES) stein.ce@gmail.com.Associação Ambiental Voz da NaturezaBrazilVitória, ES, BrazilAssociação Ambiental Voz da Natureza, Rua Coronel Shuwab Filho, 104, 29052-070 Vitória, ES, Brazil. (CES) stein.ce@gmail.com.

http://orcid.org/0000-0001-7304-4045

João B. Teixeira

http://orcid.org/0000-0002-7630-6474

João Luiz Gasparini

Programa de Pós-Graduação em Ciências Ambientais e Conservação, Instituto de Biodiversidade e Sustentabilidade, Univ. Federal do Rio de Janeiro, 29910-970 Macaé, RJ, Brazil.Universidade Federal do Rio de JaneiroBrazilMacaé, RJ, Brazil Programa de Pós-Graduação em Ciências Ambientais e Conservação, Instituto de Biodiversidade e Sustentabilidade, Univ. Federal do Rio de Janeiro, 29910-970 Macaé, RJ, Brazil.

http://orcid.org/0000-0001-8294-0618

José Amorim Reis-Filho

ICHTUS Soluções em Meio Ambiente, R. Dep. Herculano Menezes, 10, 41335-400 Salvador, BA, Brazil. (JARF) amorim@icthusambiental.com.br.ICHTUS Soluções em Meio AmbienteBrazilSalvador, BA, Brazil ICHTUS Soluções em Meio Ambiente, R. Dep. Herculano Menezes, 10, 41335-400 Salvador, BA, Brazil. (JARF) amorim@icthusambiental.com.br.

http://orcid.org/0000-0001-6942-1290

Ricardo C. Garla

Departamento de Botânica e Zoologia, Univ. Federal do Rio Grande do Norte, 59078-970 Natal, RN, Brazil. (RCG) rgarla@hotmail.com.Universidade Federal do Rio Grande do NorteBrazilNatal, RN, Brazil Departamento de Botânica e Zoologia, Univ. Federal do Rio Grande do Norte, 59078-970 Natal, RN, Brazil. (RCG) rgarla@hotmail.com.

http://orcid.org/0000-0002-0827-225X

Ronaldo B. Francini-Filho

Centro de Biologia Marinha, Univ. de São Paulo, 11612-109 São Sebastião, SP, Brazil. (RBFF) francinifilho@usp.br.Univ. de São PauloBrazilSão Sebastião, SP, Brazil Centro de Biologia Marinha, Univ. de São Paulo, 11612-109 São Sebastião, SP, Brazil. (RBFF) francinifilho@usp.br.

http://orcid.org/0000-0002-7678-6797

Stephanie D. T. Delfino

http://orcid.org/0000-0002-2006-0292

Thayná J. Mello

Programa de Pós-Graduação em Ecologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, 59072-970 Natal, RN, Brazil. (TJM) thaynajm@gmail.com.Universidade Federal do Rio Grande do NorteBrazilNatal, RN, Brazil Programa de Pós-Graduação em Ecologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, 59072-970 Natal, RN, Brazil. (TJM) thaynajm@gmail.com.

http://orcid.org/0000-0002-9123-5643

Tommaso Giarrizzo

Núcleo de Ecologia Aquática e Pesca da Amazônia, Univ. Federal do Pará, Av. Perimetral, 2651, Terra Firme, 66040-170 Belém, PA, Brazil. (TG) tgiarrizzo@gmail.com.Univ. Federal do ParáBrazilBelém, PA, Brazil Núcleo de Ecologia Aquática e Pesca da Amazônia, Univ. Federal do Pará, Av. Perimetral, 2651, Terra Firme, 66040-170 Belém, PA, Brazil. (TG) tgiarrizzo@gmail.com.

http://orcid.org/0000-0002-5116-5206

Hudson T. Pinheiro

http://orcid.org/0000-0002-3143-1474

Edited by

Fernando Gibran

Correspondence

Caio R. Pimentel caiopimentelr@gmail.com

Author's Contriburion

Caio R. Pimentel: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Luiz A. Rocha: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Bart Shepherd: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Tyler A. Y. Phelps: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Jean-Christophe Joyeux: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Agnaldo S. Martins: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Carlos Eduardo Stein: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

João B. Teixeira: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

João Luiz Gasparini: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

José Amorim Reis-Filho: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Ricardo C. Garla: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Ronaldo B. Francini-Filho: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Stephanie D. T. Delfino: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Thayná J. Mello: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Tommaso Giarrizzo: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Hudson T. Pinheiro: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Competing Interests

The authors declare no competing interests.

Ethical Statement

The Brazilian Environmental Agency (ICMBio, license #64991-3).

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (7)
Tables (1)

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FIGURE 1 |
Location of the Fernando de Noronha Archipelago, Brazil (South-western Atlantic). Blue line indicates the area of the Marine National Park of Fernando de Noronha (no-take MPA). Dashed lines indicate the 30, 60, 90 and 150 m isobaths. Black triangles, red stars, golden squares and green dots indicate the position of stereo-BRUVS deployments, rebreather dives, SCUBA dives and ROV footages, respectively.

Thumbnail

FIGURE 2 |
Middle mesophotic (61 to 90 m depth) mosaic of habitats sampled with stereo-BRUVS around the Fernando de Noronha Archipelago. A. Patch reefs; B. Sand bottoms; and C. Rhodoliths beds.

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FIGURE 3 |
Lower mesophotic (below 90 m depth) ecosystems explored through technical rebreather diving around the Fernando de Noronha Archipelago. A.The insular shelf edge; and B. The steep wall.

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FIGURE 4 |
New records of fishes at the mesophotic ecosystems. A. Chromis enchrysura(~ 10 cm total length); B. Balistes capriscus(~ 30 cm total length); C. Chromis scotti (~ 7.5 cm total length); D. Prognathodes guyanensis (~ 15 cm total length); E. Synodus sp. (~ 15 cm total length); F. Scorpaena sp. (~ 7.5 cm total length); G. Psilotris sp. (~ 5 cm total length); and H. Cosmocampus profundus(white arrow; ~ 15 cm total; I. Lutjanus buccanella (~ 50 cm total length). Photos by L. A. Rocha (A, C-G) and stereo-BRUVS (B, Hand I). Tosanoidessp. is under description and its picture is not shown.

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FIGURE 5 |
New records of fishes from the mesophotic ecosystems collected and photographed in aquarium. A. Aulotrachichthys argyrophanus(~ 6.5 cm total length; CIUFES 3909); B. Corniger spinosus(~ 15 cm total length; CIUFES 3922); C. Decodon puellaris (~ 7.5 cm total length; CIUFES 3914); and D. Pronotogrammus martinicensis(~ 20 cm total length; CIUFES 3939 / 3960). Photos by J. L. Gasparini.

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FIGURE 6 |
New records of fishes from the euphotic ecosystems. A. Kyphosus bigibbus(~ 25 cm total length); B. Kyphosus cinerascens (~ 25 cm total length); C. Kyphosus vaigiensis(~ 25 cm total length; CIUFES 4050); and D. Pseudogramma gregoryi(~ 6.5 cm total length; CIUFES 4029). Photos A, B and C by J. L. Gasparini and photo D by R. M. Macieira. Apogon pseudomaculatus(CIUFES 3957) is not shown.

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FIGURE 7 |
Evidence of human impacts (arrows) by fishing debris, plastics and other trash found in the ecosystems explored around the Fernando de Noronha Archipelago. A.and B.Mesophotic (> 30 m deep); C. Intertidal; and D. Shallow ecosystems (≤ 30 m deep). Photos Aand B by L. A. Rocha and photos Cand D by J. L. Gasparini.

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TABLE 1 |
New records of fishes from Fernando de Noronha Archipelago, north-eastern Brazil. Families are presented in phylogenetic order according to Nelson et al. (2016)Nelson JS, Grande TC, Wilson MVH. Fishes of the world. Hoboken, New Jersey: Wiley & Sons; 2016.. Information about depth zone, habitat, record type and voucher of the new records, as well as distribution and conservation status of the species are presented. Depth zone of the record: euphotic (≤ 30 m deep) and mesophotic (31 to 150 m deep). Geographic range: amphi-Atlantic (AA), Caribbean Sea (CS), Circumtropical (CT), Mediterranean (M), Northern Brazil (NB), South-western Atlantic (SW) and Western Atlantic (WA). International Union for Conservation of Nature and Natural Resources (IUCN) conservation status: data deficient (DD), least concern (LC), and vulnerable (VU); N/A: not applicable.

FIGURE 1 | Location of the Fernando de Noronha Archipelago, Brazil (South-western Atlantic). Blue line indicates the area of the Marine National Park of Fernando de Noronha (no-take MPA). Dashed lines indicate the 30, 60, 90 and 150 m isobaths. Black triangles, red stars, golden squares and green dots indicate the position of stereo-BRUVS deployments, rebreather dives, SCUBA dives and ROV footages, respectively.

FIGURE 2 | Middle mesophotic (61 to 90 m depth) mosaic of habitats sampled with stereo-BRUVS around the Fernando de Noronha Archipelago. A. Patch reefs; B. Sand bottoms; and C. Rhodoliths beds.

FIGURE 3 | Lower mesophotic (below 90 m depth) ecosystems explored through technical rebreather diving around the Fernando de Noronha Archipelago. A.The insular shelf edge; and B. The steep wall.

FIGURE 4 | New records of fishes at the mesophotic ecosystems. A. Chromis enchrysura(~ 10 cm total length); B. Balistes capriscus(~ 30 cm total length); C. Chromis scotti (~ 7.5 cm total length); D. Prognathodes guyanensis (~ 15 cm total length); E. Synodus sp. (~ 15 cm total length); F. Scorpaena sp. (~ 7.5 cm total length); G. Psilotris sp. (~ 5 cm total length); and H. Cosmocampus profundus(white arrow; ~ 15 cm total; I. Lutjanus buccanella (~ 50 cm total length). Photos by L. A. Rocha (A, C-G) and stereo-BRUVS (B, Hand I). Tosanoidessp. is under description and its picture is not shown.

FIGURE 5 | New records of fishes from the mesophotic ecosystems collected and photographed in aquarium. A. Aulotrachichthys argyrophanus(~ 6.5 cm total length; CIUFES 3909); B. Corniger spinosus(~ 15 cm total length; CIUFES 3922); C. Decodon puellaris (~ 7.5 cm total length; CIUFES 3914); and D. Pronotogrammus martinicensis(~ 20 cm total length; CIUFES 3939 / 3960). Photos by J. L. Gasparini.

FIGURE 6 | New records of fishes from the euphotic ecosystems. A. Kyphosus bigibbus(~ 25 cm total length); B. Kyphosus cinerascens (~ 25 cm total length); C. Kyphosus vaigiensis(~ 25 cm total length; CIUFES 4050); and D. Pseudogramma gregoryi(~ 6.5 cm total length; CIUFES 4029). Photos A, B and C by J. L. Gasparini and photo D by R. M. Macieira. Apogon pseudomaculatus(CIUFES 3957) is not shown.

FIGURE 7 | Evidence of human impacts (arrows) by fishing debris, plastics and other trash found in the ecosystems explored around the Fernando de Noronha Archipelago. A.and B.Mesophotic (> 30 m deep); C. Intertidal; and D. Shallow ecosystems (≤ 30 m deep). Photos Aand B by L. A. Rocha and photos Cand D by J. L. Gasparini.

TABLE 1 | New records of fishes from Fernando de Noronha Archipelago, north-eastern Brazil. Families are presented in phylogenetic order according to Nelson et al. (2016)Nelson JS, Grande TC, Wilson MVH. Fishes of the world. Hoboken, New Jersey: Wiley & Sons; 2016.. Information about depth zone, habitat, record type and voucher of the new records, as well as distribution and conservation status of the species are presented. Depth zone of the record: euphotic (≤ 30 m deep) and mesophotic (31 to 150 m deep). Geographic range: amphi-Atlantic (AA), Caribbean Sea (CS), Circumtropical (CT), Mediterranean (M), Northern Brazil (NB), South-western Atlantic (SW) and Western Atlantic (WA). International Union for Conservation of Nature and Natural Resources (IUCN) conservation status: data deficient (DD), least concern (LC), and vulnerable (VU); N/A: not applicable.

Family	Species	Depth zone	Habitat	Record type	Voucher	Geographic range	Conservation status
Synodontidae	Synodus sp.	Mesophotic	Reef	Photo	Fig. 4	Unknown	N/A
Holocentridae	Corniger spinosus Agassiz, 1831	Mesophotic	Reef	Collected / Photo	CIUFES 3922 / Fig. 5	AA	LC
Trachichthyidae	Aulotrachichthys argyrophanus (Woods, 1961)	Mesophotic	Reef	Collected / Photo	CIUFES 3909 / Fig. 5	SW	DD
Apogonidae	Apogon pseudomaculatus Longley, 1932	Euphotic	Reef	Collected	CIUFES 3957	WA	LC
Gobiidae	Psilotris sp.	Mesophotic	Reef	Photo	Fig. 4	Unknown	N/A
Pomacentridae	Chromis enchrysura Jordan & Gilbert, 1882	Mesophotic	Reef	Collected / Photo	CIUFES 3902 / Fig. 4	AA	LC
Pomacentridae	Chromis scotti Emery, 1968	Mesophotic	Reef	Photo	Fig. 4	CS / NB	LC
Syngnathidae	Cosmocampus profundus (Herald, 1965)	Mesophotic	Rhodolith	Stereo-BRUVS	Fig. 4	WA	DD
Labridae	Decodon puellaris (Poey, 1860)	Mesophotic	Reef	Collected	CIUFES 3914 / Fig. 5	WA	LC
Kyphosidae	Kyphosus bigibbus Lacepède, 1801	Euphotic	Reef	Photo	Fig. 6	CT	LC
Kyphosidae	Kyphosus cinerascens (Forsskål, 1775)	Euphotic	Reef	Photo	Fig. 6	CT	LC
Kyphosidae	Kyphosus vaigiensis (Quoy & Gaimard, 1825)	Euphotic	Reef	Collected / Photo	CIUFES 4050 / Fig. 6	CT	LC
Serranidae	Pronotogrammus martinicensis (Guichenot, 1868)	Mesophotic	Reef	Collected / Photo	CIUFES 3939 / 3960 / Fig. 5	WA	LC
Serranidae	Pseudogramma gregoryi (Breder, 1927)	Euphotic	Rhodolith	Collected / Photo	CIUFES 4029 / Fig. 6	WA	LC
Serranidae	Tosanoides sp.	Mesophotic	Reef	Collected	CIUFES 3892 / 3893 / 3894 / 3912 / 3913 / 3952	Unknown	N/A
Chaetodontidae	Prognathodes guyanensis (Durand, 1960)	Mesophotic	Reef	Collected / Photo / ROV	CIUFES 3959 / Fig. 4	WA	LC
Lutjanidae	Lutjanus buccanella (Cuvier, 1828)	Mesophotic	Rhodolith	Stereo-BRUVS	Fig. 4	WA	DD
Scorpaenidae	Scorpaena sp.	Mesophotic	Reef	Photo	Fig. 4	Unknown	N/A
Balistidae	Balistes capriscus Gmelin, 1789	Mesophotic	Rhodolith	Stereo-BRUVS	Fig. 3	AA / M	VU

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Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br

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Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South-western Atlantic), reveal unique ichthyofauna and need for conservation

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[1] Edited by

Fernando Gibran