332 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

First use of baited remote underwater video stations

to assess fish diversity in the Metropolitan Region of Recife,

Northeastern Brazil

Natalia Priscila Alves Bezerra1,2; https://orcid.org/0000-0002-4203-8408

Ana Laura Tribst Corrêa1; https://orcid.org/0000-0002-6641-0585

Fabio Hissa Vieira Hazin†1

Ricardo Clapis Garla3,4*; https://orcid.org/0000-0002-0827-225X

1. Laboratório de Oceanografia Pesqueira, Departamento de Pesca e Aquicultura, Universidade Federal Rural de

Pernambuco, Rua Manuel de Medeiros, Dois Irmãos, 52171-011, Recife, Pernambuco, Brasil;

natalia_pab@hotmail.com, naliura@gmail.com (†In memoriam)

2. Departamento de Oceanografia e Ecologia, Universidade Federal do Espirito Santo, Av. Fernando Ferrari, 514,Campus

de Goiabeiras, 29075-910, Vitória, Epírito Santo, Brasil

3. Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Avenida Senador Salgado

Filho, 3000, Lagoa Nova, 59064-741, Natal, Rio Grande do Norte, Brasil; rgarla@hotmail.com (*Correspondence)

4. Curso de Ciências Biológicas, Centro Universitário barão de Mauá, Rua Ramos de Azevedo, 423, 14090-062,

Ribeirão Preto, São Paulo, Brasil.

Received 23-II-2021. Corrected 17-V-2022. Accepted 18-V-2022.

ABSTRACT

Introduction: Video techniques are used worldwide to study marine communities. As elsewhere, the use of

remote underwater videos has recently increased in Brazil and there is a need for information about their advan-

tages, disadvantages, and reliability in tropical habitats.

Objective: To evaluate the use of baited remote underwater video stations (BRUVS) in fish diversity research

in a tropical habitat.

Methods: We used baited video stations to record the fishes and their relationship with habitat type, underwater

visibility and depth, in 79 random sites in the Metropolitan Region of Recife, Northeastern Brazil (11 days in

November 2017).

Results: We recorded 3 286 individuals (65 taxa, 29 families) along a 25 km section of the shoreline, 10.2 to

28.6 m depth. The Clupeidae dominated numerically, followed by Haemulidae, Carangidae, and Lutjanidae;

by species, Haemulon aurolineatum, Opisthonema oglinum, Haemulon steindachneri, Lutjanus synagris and

Caranx crysos. The highest mean number of species was detected over sediment close to shipwrecks, but we

found no differences among the mean number of individuals between habitat types. More species and individuals

were observed at a depth of 20-25 m depth. The highest mean number of species was in 2-3 m of visibility, and

the highest number of individuals within 4-5 m.

Conclusions: Video recording seemed to be a valid method, and indicated that —besides being relatively

diverse— the local fish community is dominated by a few species of small and medium-sized mesopredators,

and a few top predators.

Key words: degraded reefs; fish abundance; ichthyofauna; marine biodiversity; BRUVS.

https://doi.org/10.15517/rev.biol.trop..v70i1.45915

AQUATIC VERTEBRATES

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In the last decades, new techniques have

been developed to study marine ecosystems

(Barnett et al., 2010) amidst growing threats,

such as habitat degradation, pollution, overfish-

ing and climate change (Brautigam et al., 2015;

Simpfendorfer et al., 2011). Particular empha-

sis has been put on non-lethal, non-extractive

methods that can detect temporal and spatial

fluctuations in populations associated with

natural and anthropogenic impacts (Barley et

al., 2017; Willis et al., 2000; Whitmarsh et al.,

2017). One such method is the Baited Remote

Underwater Video Stations (BRUVS). The use

of BRUVS has become increasingly popular

worldwide for assessing marine diversity and

estimating relative abundances (Whitmarsh et

al., 2017). This technique is less labour inten-

sive and produces less biased estimates of

species richness and relative abundance than

underwater visual censuses with SCUBA or

Diver Operated Video (Brooks et al., 2011;

Harvey et al., 2002; Watson et al., 2010). The

use of BRUVS, has also increased in recent

years in Brazil as a low-cost alternative to

study different ecosystems (Reis-Filho et al.,

2019; Rolim et al., 2019; Schimd et al., 2017).

The coastline of Pernambuco State, North-

eastern Brazil, includes relatively extensive

sandstone reefs, which occur parallel to the

coast and at different depths (Maida & Ferreira,

1997). These reefs have been suffering anthro-

pogenic impacts at an accelerated rate, includ-

ing discharge of sewage, dredging, effects of

coastal development, pollution, intense vessel

traffic, fishing, disordered tourism, ornamen-

tal fish market, and global climate changes

(Araújo et al., 2018).

Knowledge of the fish fauna along impact-

ed coastlines is important for management and

conservation decisions and efforts to protect

the local marine life. Surveys of fisheries land-

ings were conducted along the shoreline of

Pernambuco between 1995 and 2005 as part

of a regional effort to assess the fish fauna

of the Brazilian Economic Exclusive Zone

(REVIZEE Programme). Those studies record-

ed a total of 179 species and 54 families in this

region, including 159 species and 47 families

of teleosts, and 20 species and seven families

of elasmobranchs (Lessa et al., 2009). Previous

studies in the region of Recife, the state’s capi-

tal and a heavily urbanized area, have focused

on fish assemblages in shipwreck sites (Fisch-

er, 2009; Oliveira, 2012), and elasmobranch

ecology, due to the historic of human-shark

incidents in the region (Afonso et al., 2014;

Hazin et al., 2000; Hazin et al., 2008; Niella et

al., 2017). Knowledge of fish assemblages on

the sandy reefs offshore Recife, however, is rel-

atively scarce, hampering marine management

and conservation in the area. To improve this

lack of information, a series of single BRUVS

surveys was conducted. The goals were to

assess the diversity and relative abundance of

the ichthyofauna and investigate whether its

spatial distribution was influenced by depth,

underwater visibility, or habitat type.

MATERIALS AND METHODS

Study area: The study was carried out in

the coastal area of the Metropolitan Region of

Recife (MRR), which is influenced by clearly

defined wet (March-August) and dry (Septem-

ber-February) seasons (Mendonça & Danni-

Oliveira, 2007). Southeastern trade winds are

more frequent in the austral winter (Northeast

wet season), so the surface current at this time

flows predominantly northwards. Northeastern

trade winds become stronger in the austral

summer (Northeast dry season), when the cur-

rents occasionally may flow southwards (Lira

et al., 2010; Rollnic & Medeiros, 2013). The

continental shelf is narrow and relatively flat,

extending for 35 km, and typically with the

slope at 60 m depth. There is an underwater

sandstone reef approximately 1 km from the

shore and a 6.5 m deep channel parallel to the

beach (Hazin et al., 2008; Lessa et al., 2009).

The internal continental shelf (0 to 20 m) is

characterized mainly by quartz sand and the

medium continental shelf (20 to 40 m) with

predominance of sand and calcium carbonate

gravel (Coutinho, 1976; Cunha, 2004). Many

old vessels were purposely sunk in this area to

334 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

create a shipwreck park and act as diving points

and artificial reefs (Fischer, 2009).

The tidal regime is semidiurnal and mean

water temperatures range from 24 to 30 ˚C,

during the austral winter and austral summer,

respectively. Two main estuaries are included

in the study area, the Capibaribe River in its

Northern part and the Jaboatão River in the

Southern part (Fig. 1). Both are shallow low-

land estuaries with a predominance of muddy

substrates and scattered sandy deposits in some

sections. Both rivers are regarded as heavily

polluted due to the inflow of effluents from

domestic and industrial sewage, nautical and

port activities (Hazin et al., 2008).

Sampling collection and analysis: An

approximately 25 km stretch of MRR’s shore-

line was sampled as part of the Global FinPrint

initiative (http://www.globalfinprint.org). For

this reason, samples were concentrated around

the two regions where most of the shark-human

incidents has been recorded since 1992: Boa

Viagem and Piedade (Hazin et al., 2008).

Seventy-nine sites were sampled with single

BRUVS (one camera) deployed at random sites

in 11 days of effort between November 15th

and 27th 2017 (Fig. 1). BRUVS were deployed

between 8:00 h and 17:00 h, and were left at

least 80 min in depths ranging from 10.0 to

28.6 m and at distances from shore ranging

from one to nine km. Each BRUVS consisted

of a GoPro Hero 3 + camera inside an under-

water housing mounted on a stainless-steel

frame with a bait cage with a pre-weighted 1

kg of crushed sardine (Sardinella brasilien-

sis) mounted on a pole in front of the camera.

BRUVS were tied by a rope to a buoy and were

deployed at least 1 km apart of each other to

avoid overlapping bait plumes.

Fig. 1. Geographical position of Pernambuco State in Northeast Brazil and the Metropolitan Region of Recife (MRR)

(inset). ∆ and + represent Capibaribe and Jaboatão rivers, respectively, and the white dots represent the locations of BRUVS

deployments in November 2017.

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Latitude, longitude, date, time and depth

were collected before each deployment. The

number of species and individuals attracted to

the bait, the maximum number of individuals of

each species in the camera field of view at the

same time (MaxN) and the sum of MaxN (Sum

MaxN) (Cappo et al., 2003) were calculated

using the recorded videos. The underwater vis-

ibility was visually estimated through video

analyses, using the BRUVS’ one-meter pole as

a reference. The habitat type was characterised

by the predominantly substrate recorded on

a frame, which could be Sediment, Sediment

with phytobenthos and Sediment in shipwreck

area (Fig. 2).

Video files were analysed with QuickTime

(Apple Inc., 2010). Species were identified

to their lowest possible taxonomic level. Tro-

phic categories of each species were deter-

mined according to Fish Base (Froese & Pauly,

2019) and the international conservation status

through IUCN’s website (IUCN, 2018). Spe-

cies richness for each dataset was determined

using the species accumulation curve in the

vegan package in R (Jari Oksansen, 2022).

Confidence intervals were calculated from

standard deviations (P < 0.05).

Relative abundance was calculated as

MaxN h-1 (maximum number of individuals

of each species in the camera field of view

at the same time per hour) (Cappo et al.,

2003) and compared with habitat type (sedi-

ment, sediment with phytobenthos, sediment

in shipwreck area), depth (10-15 m, 15.1-20

m, 20.1-25 m, 25.1-30 m), and underwater vis-

ibility (≤ 1 m, 2-3 m, 4-5 m, ≥ 6 m). Univariate

analyses were conducted on MaxN h-1 data for

each factor (habitat type, depth and underwater

visibility), to investigate differences in mean

individuals/species number recorded, both tele-

osts and elasmobranchs. One way ANOVA was

used for normal distributed data and Kruskal-

Wallis tests for nonparametric data. Significant

level adopted was P < 0.05 and variables were

transformed using (x + 1) or log (x + 1) to

achieve normal distribution. To avoid bias due

to the passage of schools of fishes, records with

more than a hundred individuals were excluded

from the abundance related statistical analysis

(Fitzpatrick et al., 2012). Diversity Indices

were calculated: 1) Shannon-Wiener H’, this

value is measured by the community’s specific

richness and the distribution of the individuals

amidst species and 2) Pielou’s evenness J’, the

value (ranging from 0 to 1) follows the abun-

dance distribution among species of the com-

munity, where higher values (approximately

1) reflect species abundance lower than the

Fig. 2. A. Representative images of the ecosystems within

the Sediment with phytobenthos B. Sediment C. Sediment

in shipwreck area.

336 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

others (Krebs, 1999). All data analysis were

performed in R (R Core Team, 2016).

RESULTS

The 79 sites sampling effort was sufficient

to explain the overall fish species diversity in

MRR (Fig. 3). The total recording time was 7

254 min (120.9 h) with a minimum of 71 min

and a maximum of 153 min per deployment

(mean time = 93 ± 15 Standard Deviation, SD).

The underwater visibility ranged from 0.5 m to

≥ 6 m, with an average of 3.26 m (± 2.52 SD).

The highest visibility (≥ 6 m) occurred in 12.7

% of the samples and the lowest (≤ 1 m) in 26.6

%. Depths ranged from 10.0 to 28.6 m, with an

average of 19.41 m (± 4.36 m SD). The number

of samples per each habitat type was unbal-

anced, due to the random choice of sampling

locations (Sediment: 60, Sediment with phy-

tobentos: 16, Sediment in shipwreck area: 3).

A total of 3 286 individuals (MaxN h-1 =

27.29 h-1) distributed in 65 taxa and 29 families

was recorded. Of the 65 taxa, 60 were teleosts

and five were elasmobranchs (Table 1). Fifty-

three taxa (83 % of the total) were identified at

species level. Eleven taxa (17 % of the total, N

= 128 specimens) were identified as genus, due

to inadequate visibility and distance from the

camera. Flounders were not identified to family

or species levels given their mimetic coloration

and difficulties of detecting diagnostic charac-

ters of their flat-shaped body always in contact

with the bottom.

The Clupeidae family was dominant in

number of individuals, representing 39.6 % of

all organisms recorded (10.81 h-1). Haemuli-

dae represented 32.8 % (8.94 h-1), Carangidae

7.7 % (2.11 h-1), Lutjanidae 4.6 % (1.26 h-1),

and the remaining families 15.3 % (Fig. 4,

Table 1). Haemulidae was the most diverse

Fig. 3. Species accumulation curve based on fish

assemblages observed in BRUV surveys in the Metropolitan

Region of Recife.

Fig. 4. Mean relative abundance of individuals per hour of sampling (MaxN h-1) of the most representative families recorded

in BRUVS surveys in the Metropolitan Region of Recife.

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TABLE 1

Classes, families and species of the fishes observed in BRUVS surveys in the Metropolitan Region of Recife in November 2017

Class Family Species Sum MaxN MaxN h-1 Mean MaxN± SD

(Min-Max) TP Habitat IUCN

Osteichthyes

Acanthuridae Acanthurus chirurgus (Bloch 1787) 1 0.008 0.01 ± 0.11 (1) H SW LC

Acanthurus bahianus (Castelnau 1855) 2 0.017 0.03 ± 0.23 (1-2) H SP LC

Acanthurus coeruleus (Bloch & Schneider 1801) 1 0.008 0.01 ± 0.11 (1) H S LC

Balistidae Balistes capriscus (Gmelin 1788) 28 0.232 0.35 ± 0.82 (1-5) CSP, S VU

Balistes vetula (Linnaeus 1758) 3 0.025 0.04 ± 0.25 (1-2) C SP NT

Carangidae Chloroscombrus chrysurus (Linnaeus 1766)** 67 0.554 0.85 ± 3.47 (1-23) Om SP. S LC

Caranx crysos (Mitchill 1815) 110 0.910 1.39 ± 3.99 (1-30) CSW, SP, S LC

Caranx ruber (Bloch 1793)** 31 0.256 0.39 ± 1.53 (1-9) CSW, SP, S LC

Caranx sp. 11 0.091 0.14 ± 0.86 (1-7) CSW, SP, S -

Carangoides bartholomaei (Cuvier 1833) 1 0.008 0.01 ± 0.11 (1) C S LC

Decapterus sp. 34 0.281 0.43 ± 3.71 (1-33) C SP -

Seriola rivoliana (Cuvier 1833)** 1 0.008 0;01 ± 0.11 (1) C SW LC

Chaetodontidae Chaetodon striatus (Linnaeus 1758) 5 0.041 0.06 ± 0.33 (1-2) HSW, SP LC

Clupeidae Opisthonema oglinum (Lesueur 1818) 507 4.194 6.42 ± 56.25 (7-500) Om SW, S LC

Echeneidae Echeneis naucrates (Linnaeus 1758) 22 0.182 0.28 ± 0.6 (1-3) CSW, SP, S LC

Epinephelidae Epinephelus adscensionis (Osbeck 1765) 1 0.008 0.01 ± 0.11 (1) C SP LC

Ephippidae Chaetodipterus faber (Broussonet 1782) 2 0.017 0.03 ± 0.23 (1-2) C SP LC

Fistulariidae Fistularia sp. 7 0.058 0.09 ± 0.4 (1-3) SP, S -

Gerreidae Eucinostomus sp.** 42 0.347 0.53 ± 1.23 (1-7) SP, S -

Haemulidae Anisotremus virginicus (Linnaeus 1758) 4 0.033 0.05 ± 0.27 (1-2) CSW, S LC

Anisotremus surinamensis (Bloch 1791)** 2 0.017 0.03 ± 0.23 (1-2) C SW DD

Anisotremus moricandi (Ranzini 1842)** 1 0.008 0.01 ± 0.11 (1) Om SP LC

Conodon sp. 1 0.008 0.01 ± 0.11 (1) SP -

Haemulon squamipinna (Rocha & Rosa 1999) 59 0.488 0.75 ± 4.94 (1-43) CSW, SP, S LC

Haemulon parra (Desmarest 1823) 2 0.017 0.03 ± 0.23 (1-2) C S LC

Haemulon aurolineatum (Cuvier 1830) 679 5.616 8.59 ± 21.55 (1-130) CSW, SP, S LC

Haemulon plumierii (Lacepéde 1801) 10 0.083 0.13 ± 0.43 (1-2) CSP, S LC

Haemulon steindachneri (Jordan & Gilbert 1882) 267 2.208 3.38 ± 9.26 (1-60) CSW, SP, S LC

338 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

TABLE 1 (Continued)

Class Family Species Sum MaxN MaxN h-1 Mean MaxN± SD

(Min-Max) TP Habitat IUCN

Orthopristis ruber (Cuvier 1830)** 55 0.455 0.7 ± 2.16 (1-15) CSP, S LC

Holocentridae Holocentrus adscensionis (Osbeck 1765) 3 0.025 0.04 ± 0.25 (1-2) CSW, SP LC

Labridae Bodianus rufus (Linnaeus 1758) 3 0.025 0.04 ± 0.25 (1-2) CSW, SP LC

Lutjanidae Lutjanus synagris (Linnaeus 1758) 137 1.133 1.73 ± 1.95 (1-11) CSW, SP, S NT

Lutjanus analis (Cuvier 1828) 6 0.050 0.08 ± 0.42 (1-3) C SW NT

Lutjanus cyanopterus (Cuvier 1828) 1 0.008 0.01 ± 0.11 (1) C SW VU

Lutjanus griseus (Linnaeus 1758) 1 0.008 0.01 ± 0.11 (1) C SW LC

Ocyurus chrysurus (Bloch 1791) 7 0.058 0.09 ± 0.79 (1-7) C SW DD

Monacanthidae Aluterus monoceros (Linnaeus 1758) 38 0.314 0.48 ± 1.69 (1-12) CSP, S LC

Aluterus scriptus (Osbeck 1765) 4 0.033 0.05 ± 0.27 (1-2) Om SP LC

Aluterus schoepfii (Walbaum 1792)** 2 0.017 0.03 ± 0.16 (1) Om S LC

Cantherhines sp. 1 0.008 0.01 ± 0.11 (1) S -

Mullidae Mulloidichthys martinicus (Cuvier 1829) 2 0.017 0.03 ± 0.23 (1-2) C SW LC

Pseudupeneus maculatus (Bloch 1793) 11 0.091 0.14 ± 0.52 (1-3) CSW, S LC

Muraenidae Gymnothorax funebris (Ranzani 1840) 2 0.017 0.03 ± 0.16 (1) C S LC

Gymnothorax vicinus (Castelnau 1856) 1 0.008 0.01 ± 0.11 (1) C SP LC

Ostraciidae Lactophrys trigonus (Linnaeus 1758)** 12 0.099 0.15 ± 0.36 (1) Om S LC

Acanthostracion sp. 1 0.008 0.01 ± 0.11 (1) SW -

Pempheridae Pempheris sp. 13 0.108 0.16 ± 1.46 (1-13) SW -

Pomacanthidae Holacanthus tricolor (Bloch 1795) 1 0.008 0.01 ± 0.11 (1) Om SW LC

Pomacanthus paru (Bloch 1787) 1 0.008 0.01 ± 0.11 (1) H SP LC

Pomacentridae Abudefduf saxatilis (Linnaeus 1758) 17 0.14 0.22 ± 1.52 (4-13) Om SW, SP LC

Chromis multilineata (Guichenot 1853) 7 0.058 0.09 ± 0.79 (1-7) Om SW LC

Scombridae Scomberomorus brasiliensis (Collete,

Russo & Zavala-Carmin 1978) 3 0.025 0.04 ± 0.19 (1) CSP, S LC

Serranidae Cephalopholis fulva (Linnaeus 1758) 14 0.116 0.18 ± 0.96 (3-7) CSW, SP LC

Diplectrum formosum (Linnaeus 1766) 45 0.372 0.57 ± 0.94 (1-3) CSP, S LC

Sparidae Calamus pennatula (Guichenot 1868) 5 0.041 0.06 ± 0.37 (1-3) CSW, SP LC

Sphyraenidae Sphyraena barracuda (Walbaum 1792) 8 0.066 0.10 ± 0.3 (1) CSW, SP, S LC

Sphyraena picudilla (Poey 1860) 90 0.744 1.14 ± 9.06 (10-80) C S LC

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family (10 species), followed by Carangidae

(6), Lutjanidae (5), Monacanthidae (4) and

Acanthuridae (3) (Table 1).

Teleosts represented the majority of speci-

mens observed (3 256 individuals). Haemulon

aurolineatum was the predominant species in

numbers (679 individuals, 5.62 h-1), followed

by Opisthonema oglinum (507, 4.19 h-1), Hae-

mulon steindachneri (267, 2.21 h-1), Lutjanus

synagris (137, 1.13 h-1) and Caranx crysos

(110, 0.91 h-1) (Fig. 5, Table 1). The most com-

mon species was L. synagris, recorded in 56

samples, followed by H. steindachneri (N =

34), C. crysos (N = 32) and H. aurolineatum (N

= 30). Ten species (Table 1) were not observed

in previous local ichthyofaunal surveys: Chlo-

roscombrus chrysurus, Caranx ruber, Seriola

rivoliana, Eucinostomus sp., Anisotremus suri-

namensis, Anisotremus moricandi, Orthopristis

ruber, Aluterus schoepfii, Lactophrys trigonus

and Lagocephalus laevigatus (Table 1). Most

species recorded (65 %, N = 42) were carni-

vore, 14 % (N = 9), followed by omnivore and

21 % (N = 5) herbivore (Table 1).

Thirty elasmobranch specimens (0.8 %

of the total number), including two sharks

and 28 rays, were recorded in 29 (36.7 %)

of the deployments. Sharks were recorded in

two samples (2.5 %) and rays in 27 (34.2 %).

Two different species of sharks were recorded:

Ginglymostoma cirratum and a shark of the

genus Carcharhinus that could not be identi-

fied at species level due to poor water visibility.

Two species of rays were identified: Hypanus

berthalutzae (N = 17) and Hypanus marianae

(N = 1). The remaining 10 specimens of rays

observed belonged to the genus Hypanus,

but could not be identified at species level

(Table 1).

The highest mean number of species was

observed over Sediment in shipwreck area (Sed

+ wreck), which was significantly higher than

that observed in Sediment (Sed) (F = 17.83, P

= 0.00008), but not than Sediment with phyto-

benthos (Sed + phytob) (F = 4.196, P = 0.0562)

(Table 2, Fig. 6). The mean number of spe-

cies observed between the habitat types Sedi-

ment and Sediment with phytobentos was not

TABLE 1 (Continued)

Class Family Species Sum MaxN MaxN h-1 Mean MaxN± SD

(Min-Max) TP Habitat IUCN

Tetraodontidae Lagocephalus laevigatus (Linnaeus 1766)** 10 0.083 0.13 ± 0.33 (1) CSP, S LC

Sphoeroides sp. 7 0.058 0.09 ± 0.33 (1-2) SP -

Unidentified Unidentified species of flounders 39 0.323 0.49 ± 0.75 (1-3) SP, S -

Chondrichthyes

Carcharhinidae Carcharhinus sp. 1 0.008 0.01 ± 0.11 (1) C S -

Dasyatidae Hypanus berthalutzae (Petean, Naylor & Lima, 2020) 17 0.141 0.22 ± 0.41 (1) CSW, SP, S DD

Hypanus marianae (Gomes, Rosa & Gadig 2000) 1 0.008 0.01 ± 0.11 (1) C S DD

Hypanus sp. 10 0.083 0.13 ± 0.33 (1) CSW, SP, S -

Ginglymostomatidae Ginglymostoma cirratum (Bonnaterre 1788) 1 0.008 0.01 ± 0.11 (1) C S DD

Sum MaxN: sum of maximum number of individuals in the camera field of view at the same time. MaxN h-1: relative abundance calculated by the maximum number of individuals

of each species in the camera field of view at the same time per hour of sampling. Mean MaxN ± SD: mean of MaxN ± standard error (number in parenthesis indicate minimum and

maximum numbers of individuals recorded). TP: trophic position (C= Carnivore; H= Herbivore; Om= Omnivore), Habitat type (S: sediment; SW: sediment in shipwreck area; SP:

sediment with phytobenthos) and IUCN status (VU= Vulnerable; NT= Near Threatened; LC= Least Concern; DD= Data Deficient). ** indicates species not observed in previous studies.

340 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

statistically different (F = 2.998, P = 0.0875).

Although the mean number of individuals was

higher in Sediment, the differences between

habitat types were not statistically significant

(Table 2). Values of Pielou’s evenness (J’) and

Shannon-Wiener diversity (H’) are presented

in Table 2.

Among teleosts, 1 942 were recorded

over sediment (Sed), 695 over sediment with

phytobenthos (Sed+phytob), and 632 over sedi-

ment in shipwreck area (Sed + wreck) (Table

2). Despite the large difference in the total

number of teleosts by habitat type, the mean

teleosts MaxN h-1 was not different between

habitat types (X2 = 4.965, P = 0.0835). Eigh-

teen elasmobranchs were recorded over sedi-

ment, 10 over sediment with phytobenthos, and

two over sediment in shipwreck area (Table 2).

Fig. 5. Mean relative abundance of individuals per hour of sampling (MaxN h-1) of the more common species recorded in

BRUVS surveys in the Metropolitan Region of Recife in November 2017.

Fig. 6. Mean relative abundance of individuals per hour of sampling (± SE) (MaxN h-1) observed in BRUVS surveys in

different habitat types (Sediment with phytobenthos, Sediment, and Sediment in shipwreck area) of the Metropolitan Region

of Recife in November 2017.

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TABLE 2

Total number of samples and species in each habitat type, depth and underwater visibility ranges recorded in BRUVS surveys

in the Metropolitan Region of Recife in November 2017

Factors (NS; ST) NSP Sp

MaxN h-1 ± SD NI Ind

MaxN h-1 ± SD NT Teleosts

MaxN h-1 ± SD NE Elasmo

MaxN h-1 ± SD J’ H’

Habitat type

Sediment with phytobenthos

(16, 1 428)

45 4.68 ± 2.95 705*475 29.50 ± 25.94*19.71 ± 16.02 695*465 19.09 ± 15.58 10 0.42 ± 0.41 0.55 2.10

Sediment (60, 5 549) 44 3.60 ± 1.99 1 960*1 160 22.08 ± 73.50*13.09 ± 16.98 1 942*1 142 12.89 ± 16.96 18 0.20 ± 0.31 0.58 2.19

Sediment in a shipwreck

area (3, 277)

34 9.55 ± 7.47 634*134 143.53 ± 228.21*29.90 ± 31.41 632*132 29.45 ± 31.18 20.44 ± 0.39 0.33 1.17

Depth

10-15 m (9, 933) 33 3.04 ± 3.60 182 12.36 ± 17.87 179 3.80 ± 17.87 30.19 ± 0.31 0.69 2.38

15.1-20 (37, 3 483) 38 3.10 ± 1.65 777*677 14.01 ± 21.21*12.15 ± 19.11 765*665 5.93 ± 18.88 12 0.21 ± 0.35 0.69 2.53

20.1-25 m (23, 2 047) 59 6.11 ± 3.05 2 167*737 63.91 ± 137.07*21.83 ± 15.40 2 154*724 19.57 ± 15.58 13 0.38 ± 0.35 0.52 2.11

25.1-30 m (9, 791) 20 3.78 ± 1.77 172 12.81 ± 13.01 170 5.07 ± 12.79 20.15 ± 0.30 0.72 2.14

Underwater visibility

< 1 m (21, 2 057) 62 1.58 ± 1.22 303*203 9.74 ± 17.07*6.46 ± 10.23 298*198 2.14 ± 10.14 50.15 ± 0.29 0.94 2.84

2-3 m (29, 2 586) 168 3.95 ± 2.32 668*538 15.47 ± 17.97*12.45 ± 12.70 659*529 6.66 ± 12.50 90.21 ± 0.36 0.96 3.23

4-5 m (19, 1 712) 165 5.85 ± 3.39 1 232*732 44.03 ± 91.12*26.09 ± 25.87 1 221*721 18.91 ± 25.90 11 0.39 ± 0.34 0.95 2.82

> 6 m (10, 899) 83 5.56 ± 1.43 1 096*296 73.74 ± 163.64*19.81 ± 11.24 1 091*291 16.31 ± 11.22 50.34 ± 0.36 0.98 2.27

NS: total number of samples. ST: total soak time in minutes. NSP: total number of species. Sp MaxN h-1: maximum number of species per hour of sampling ± standard error.

NI: total number of individuals. Ind MaxN h-1: maximum number of individuals per hour of sampling, including schools of fishes. NT: total number of teleosts. Teleosts MaxN

h-1: maximum number of teleosts per hour of sampling ± standard error. NE: total number of elasmobranchs. Elasmo MaxN h-1: maximum number of elasmobranchs per hour of

sampling ± standard error. J’: Pielou’s evenness index. H’: Shannon-Wiener diversity index. *Represent the number used in the calculations, excluding fishes in schools.

342 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

Despite the large difference in the total number

of elasmobranchs by habitat type, mean elas-

mobranch MaxN h-1 was not different between

habitat types (X2 = 3.072, P = 0.1262).

The highest number of species and indi-

viduals were observed between 20.1 and 25

m, which was significantly higher than those

observed in other ranges: 10-15 m (F = 9.27, P

= 0.0047), 15.1-20 m (F = 12.94, P = 0.0006)

and 25.1-30 m (F = 5.196, P = 0.0299) (Fig. 7).

The mean number of species per sample was

also significantly higher in that depth range:

10-15 m (F = 16.77, P = 0.0002), 15.1-20 m

(F = 29.76, P = 0.000001) and 25.1-30 m (F

= 7.635, P = 0.0096). Values of Pielou’s even-

ness (J’) and Shannon-Wiener diversity (H’)

for depth range are given in Table 2. Forty-one

samples (55 %) contained up to 5 different spe-

cies, whereas 26 samples (35 %) contained 6 to

10 species, 5 (7 %) had 11 to 15 species, and

only three samples (4 %) had more than 16 spe-

cies (two of them located in shipwreck sites).

Teleosts and elasmobranchs sightings per depth

range are shown in Table 2. The mean number

of teleosts per hour (MaxN h-1) was higher

between 20.1 and 25 m compared to 10-15m

depth strata (F = 5.475, P = 0.0378) and 15.1-

20 m depth strata (F = 12.88, P = 0.0007). No

differences were observed between other depth

ranges: 10-15 m and 15.1-20 m (X2 = 0.6193,

P = 0.4313), 10-15 m and 25.1-30 m (X2 =

0.6667, P = 0.4142), 15.1-20 m and 25.1-30 m

(X2 = 0.0089, P = 0.9246), 20.1-25 m and 25.1-

30 m (X2 = 2.455, P = 0.1172). There were no

differences in the mean elasmobranch MaxN

h-1 per depth strata (X2 = 3.948, P = 0.1513).

The highest mean number of species was

observed in the visibility of 2-3 m, with no

significant differences between the 4-5 m (F =

0.478, P = 0.499) and with significant differ-

ences to the visibilities < 1 m (F = 6.326, P =

0.0189) and > 6 m (F = 8.428, P = 0.0175). On

the other hand, the highest number of individu-

als was recorded in the 4-5 m visibility, with

significant differences in the 2-3 m visibility

(F = 8.095, P = 0.0112) and no significant dif-

ferences to the < 1 m (F = 1.725, P = 0.207)

and > 6 m categories (F = 0.391, P = 0.549)

(Fig. 8, Table 2). Values of Pielou’s evenness

(J’) and Shannon-Wiener diversity (H’) for vis-

ibility classes are given in Table 2. The highest

mean number of teleosts per hour (MaxN h-1)

were observed in the visibility of 4-5 m, with

significant differences in the visibilities < 1

m (F = 26.95, P = 7.356x10-6) and 2-3 m (F

= 7.825, P = 0.008), and no differences in the

> 6 m visibility. The other combinations were

significant different: < 1 m and 2-3 m (F =

9.346, P = 0.004), < 1 m and > 6 m (F = 26.71,

P = 1.783x10-5), 2-3 m and > 6 m (F = 7.24,

Fig. 7. Mean relative abundance of individuals per hour of sampling (± SE) (MaxN h-1) observed in BRUVS surveys

in different depth ranges (10-15 m, 15.1-20 m, 20.1-25 m, and 25.1-30 m) of the Metropolitan Region of Recife in

November 2017.

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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

P = 0.0129). There were no significant differ-

ences (X2 = 15.022, P = 0.001798) for the mean

elasmobranch MaxN h-1 per visibility class.

DISCUSSION

Most of the previous reef fishes studies

in the Metropolitan Region of Recife (MRR)

have focused on shipwrecks, due to the large

number of ships intentionally sunk to create

artificial reefs and the high abundance of spe-

cies associated with this environment (Coxey,

2008; Fischer, 2009; Oliveira, 2012). The num-

ber of fish species reported by investigations

employing visual censuses ranged from 65 to

97, with sampling efforts ranging from 180 to 1

800 min (Coxey, 2008; Fischer, 2009; Oliveira,

2012). The present study recorded 65 taxa in

11 days, with a much larger sampling effort

of 7 254 min, and the detection of ten species

not observed in those previous investigations.

Our calculated ecological indices were simi-

lar to those calculated by Fischer (2009) and

Oliveira (2012), and the BRUVS were effective

to not only record carnivores and omnivores,

but also a few herbivores species, as reported

elsewhere (Harvey et al., 2007; Gomelyuk,

2009; Schmid et al., 2017). Thus, results fur-

ther demonstrate the efficacy of this technique

to assess fish assemblages, employing short

temporal sampling periods and higher effort,

and covering larger areas than underwater

visual census techniques.

The high relative abundance of Haemuli-

dae found in the present study, with the fami-

lies Haemulidae, Carangidae and Lutjanidae

being the most representative (70 % of the

total) also corroborate the results of previous

studies in MRR (Coxey, 2008; Fischer, 2009;

Oliveira, 2012). Lower-level carnivores, rep-

resented here by Haemulon aurolineatum, H.

steindachneri, Lutjanus synagris and Caranx

crysos are the dominant components of temper-

ate and tropical reefs, both in species richness

and biomass (Ferreira et al., 2004; Jones et

al., 1991; Morais et al., 2017; Wainwright &

Bellwood, 2002). H. aurolineatum is dominant

from Northeastern to Southern Brazil, H. stein-

dachneri is mainly restricted to high latitudes

and coastal habitats, and Caranx has been

regarded as the main representative genus of

Carangidae along the Brazilian coast (Ferreira

et al., 2004; Reis-Filho et al., 2019). Lutjani-

dae are distributed on tropical and subtropical

reefs up to 450 m depth (Allen, 1985) and are

highly fished off Northeastern Brazil (Fer-

reira & Frédou, 2005; Reis-Filho et al., 2019;

Santos, 2001). Additional efforts are needed

to investigate whether the absence of large

specimens of many species and the scarcity

Fig. 8. Mean relative abundance of individuals per hour of sampling (± SE) (MaxN h-1) observed in BRUVS deployed in

different visibility classes of the Metropolitan Region of Recife (MRR) in November 2017.

344 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

of top predators such as sharks, large groupers

and large Lutjanidae species are an indicative

of the impoverished state of MRR’s fish fauna.

This fact has been reported by Reis-Filho et al.

(2019) in a large coastal bay in Northeastern

Brazil and seems to be common in sites close

to heavily urbanised areas.

Previous investigations using fisheries

techniques in MRR have demonstrated the

occurrence of 11 species of sharks and six spe-

cies of rays (Afonso et al., 2014; Afonso et al.,

2017; Hazin et al., 2000). Only two species

of sharks and two species of rays previously

recorded in MRR were observed in the present

study. Earlier fisheries independent surveys

also corroborate the low shark density recorded

by BRUVS in MRR (Afonso et al., 2017;

Hazin et al., 2000; Niella et al., 2017). Niella

et al. (2017) have shown a peak of abundance

of sharks from May to August in MMR and

additional surveys focusing elasmobranchs are

needed to investigate their seasonal abundance.

Structural complexity is a strong predic-

tor of reef fish abundance and species richness

(Darling et al., 2017; Gratwicke & Speight,

2005), and this explains the highest mean

number of species observed close to the more

complex structures of shipwrecks in MRR.

However, no differences were found in the

mean number of individuals between habitat

types. Reef fish communities are strongly

influenced by depth with effects on abundance

and species richness, among other attributes

(Asher et al., 2017; Mac Donald et al., 2016;

Pereira et al., 2018). Deep reefs are currently

considered to be less susceptible to local dis-

turbances, such as overfishing and pollution,

when compared to shallower ones (Lesser et

al., 2009; Lindfield et al., 2014). We observed

the highest number of species, specimens, and

the mean number of species per sample in

the 20.1-25 m depth range. Although further

studies are needed to evaluate depth effects

in MRR, this higher abundance might reflect

lower disturbance levels caused by depth and

distance from the shoreline.

Since the MRR is located between two

estuaries, water turbidity is commonly high

and most of the BRUVS deployments (64 %)

had less than 3 m of underwater visibility. Not-

withstanding, studies of nektonic assemblages

using BRUVS have been efficiently carried

out in regions with low visibility (Cappo

et al., 2003; Gomelyuk, 2009; Whitmarsh et

al., 2014), as corroborated here. Although the

poor visibility has not compromised the per-

formance of the present study, it has hindered

identification of species in sites closer to the

shoreline, even at the time of the year when

visibility is supposed to be at its best. Thus,

visibility should be taken into account when

planning future surveys closer to the shoreline,

as it may potentially preclude or reduce species

identification, especially during the heavy rains

of the austral winter.

Overall, this first use of BRUVS in MMR

provided a baseline on the local the species

richness and relative abundance. We recom-

mend future research and monitoring programs

to evaluate the influence of seasonal distribu-

tion of the local fish fauna using a combina-

tion of BRUVS and techniques such as visual

censuses and fisheries dependent and indepen-

dent surveys. Results also attest the relatively

degraded condition of MRR reef environments

except for the shipwrecks that showed a greater

diversity of species, even though usually rep-

resented by solitary individuals. Top predators

are rare, and few species were detected in most

sites, with the predominance of one medium

(Caranx crysos) and three small-sized (genera

Lutjanus and Haemulon) mesopredators. The

low species abundance and absence of top

predators call the attention for actions aimed

at the local coastal management, including the

recovery and conservation of the reef ecosys-

tems and its fish fauna.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is

no conflict of interest of any kind; and that

we followed all pertinent ethical and legal

procedures and re-quirements. All financial

sources are fully and clearly stated in the

345

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 70: 332-347, January-December 2022 (Published May 25, 2022)

acknowledge-ments section. A signed docu-

ment has been filed in the journal archives.

ACKNOWLEDGMENTS

Paul G. Allen Philanthropies/Global Fin-

Print provided equipment and resources for the

fieldwork. This paper represents part of ALTC

Master thesis, who thanks Conselho Nacional

de Desenvolvimento Científico e Tecnológi-

co (CNPq) for financial support. We thank

FACEPE Foundation for scholarship (NPAB).

We are grateful to José Alexandre Carvalho and

Rafael “Brutus” Muniz for logistical support

and friendship, to the captain Gleicinho and the

deckhands Paulinho and Zé of RV Sinuelo for

invaluable assistance onboard. Drausio P. Veras

and Yuri Marins helped in species identifica-

tion. We thank Daniel Nyqvist for comments

on the manuscript.

RESUMEN

Primer uso de Sistemas de Videos Remotos

Submarinos Cebados para evaluar la diversidad

de peces en la Región Metropolitana de Recife,

noreste de Brasil

Introducción: Las técnicas de video se utilizan en todo

el mundo para estudiar las comunidades marinas. Como

en otros lugares, el uso de videos submarinos remotos ha

aumentado recientemente en Brasil y existe la necesidad de

información sobre sus ventajas, desventajas y confiabilidad

en los hábitats tropicales.

Objetivo: Evaluar el uso de estaciones de video subacuáti-

cas remotas cebadas en la investigación de la diversidad de

peces en un hábitat tropical.

Métodos: Utilizamos estaciones de video cebadas para

registrar los peces y su relación con el tipo de hábitat, la

visibilidad submarina y la profundidad, en 79 sitios alea-

torios en la Región Metropolitana de Recife, noreste de

Brasil (11 días en noviembre de 2017).

Resultados: Registramos 3 286 individuos (65 taxones, 29

familias) a lo largo de una sección de 25 km de la costa,

de 10.2 a 28.6 m de profundidad. Los Clupeidae domi-

naron numéricamente, seguidos de Haemulidae, Carangi-

dae y Lutjanidae; por especies, Haemulon aurolineatum,

Opisthonema oglinum, Haemulon steindachneri, Lutjanus

synagris y Caranx crysos. El mayor número medio de

especies se detectó sobre sedimentos cerca de naufragios,

pero no encontramos diferencias entre el número medio

de individuos entre tipos de hábitat. Se observaron más

especies e individuos a una profundidad de 20-25 m. El

mayor número medio de especies se registró en 2-3 m de

visibilidad, y el mayor número de individuos en 4-5 m.

Conclusiones: La grabación en video pareció ser un méto-

do válido e indicó que, además de ser relativamente diver-

sa, la comunidad local de peces está dominada por unas

pocas especies de mesodepredadores de tamaño pequeño y

mediano, y pocos depredadores superiores.

Palabras clave: arrecifes degradados; abundancia de

peces; ictiofauna; biodiversidad marina; BRUVS.

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