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Marine Biology Research
ISSN: 1745-1000 (Print) 1745-1019 (Online) Journal homepage: https://www.tandfonline.com/loi/smar20
Elasmobranch species richness, fisheries,
abundance and size composition in the Azores
archipelago (NE Atlantic)
Régis Santos, Ana Novoa-Pabon, Hélder Silva & Mário Pinho
To cite this article: Régis Santos, Ana Novoa-Pabon, Hélder Silva & Mário Pinho (2020):
Elasmobranch species richness, fisheries, abundance and size composition in the Azores
archipelago (NE Atlantic), Marine Biology Research, DOI: 10.1080/17451000.2020.1718713
To link to this article: https://doi.org/10.1080/17451000.2020.1718713
Published online: 11 Feb 2020.
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ORIGINAL ARTICLE
Elasmobranch species richness, fisheries, abundance and size composition in
the Azores archipelago (NE Atlantic)
Régis Santos
a,b,c
, Ana Novoa-Pabon
b,d
, Hélder Silva
a,b,c,d
and Mário Pinho
a,b,c,d
a
IMAR Institute of Marine Research, University of the Azores, Horta, Portugal;
b
Okeanos R&D Centre, University of the Azores, Horta,
Portugal;
c
MARE Marine and Environmental Sciences Centre, University of the Azores, Horta, Portugal;
d
Faculty of Science and Technology,
Department Oceanography and Fisheries, University of the Azores, Horta, Portugal
ABSTRACT
Elasmobranchs are a vulnerable resource, more susceptible to overfishing than most teleosts,
and their assessment is complicated due to a general lack of information about their
fisheries, biology and ecology. This study aimed to analyse all fishery and survey data
available for elasmobranchs caught over the past c. 25 years around the Azores (NE Atlantic)
to provide a baseline information, which can be used to inform stock assessment and
management strategies. Elasmobranch species covered pelagic, benthopelagic and demersal
habitats, from shallow to deep-water strata in areas around the islands and seamounts.
These species are taken accidentally as by-catch of three main fisheries: swordfish fishery,
black scabbardfish fishery and demersal bottom longline fishery. The latter represents one of
the most important fishing activities in the Azores, and frequent elasmobranch by-catches
include Raja clavata,Galeorhinus galeus,Deania calcea,D. profundorum,Etmopterus pusillus
and E. spinax. A slight reduction in the abundance indices of these species was observed,
despite the implemented technical measures (e.g. minimum size, zero catch). Little is known
about resource dynamics for the Azorean region and no analytical assessments have been
conducted. This study highlights the vulnerability to overfishing of these resources and the
urgent need to develop management strategies.
ARTICLE HISTORY
Received 17 April 2019
Accepted 13 January 2020
SUBJECT EDITOR
Dr Rui Coelho
KEYWORDS
Sharks; skates and rays; long-
term changes; Azores EEZ;
ICES Subdivision 10.a.2
Introduction
Elasmobranchs present a set of challenges for fisheries
management and conservation. Their life-history
characteristics make them a vulnerable resource,
more susceptible to overfishing than most teleosts
(Bonfil1994). On the other hand, their assessment is
complicated due to a general lack of baseline infor-
mation about their fisheries, biology, and ecology. Fur-
thermore, fishing pressure on elasmobranchs is
increasing due to the high value of their meat, fins
and livers (Dulvy et al. 2014, and references therein),
as well as their frequent incidental capture by pelagic
or groundfish fisheries (Oliver et al. 2015).
The Azores is at the limit of the International Council
for the Exploration of the Sea –ICES statistical area (ICES
Division 27.10.a), which corresponds to an area of
environmental and faunal transition in the North Atlan-
tic Ocean (40° –50° N), and it is close to the limits of the
distribution of many marine species (Pinho and
Menezes 2009). In this area, fishing has been an impor-
tant cultural and economic activity, which has since
2010 average reported landings of 10M ton/year and
value in the order of 34M €(Santos 2017). The Azorean
fishery is typically artisanal and small-scale. About 90%
of the fishing vessels are less than 12 m and mainly
operate near the islands and seamounts using hooks
and lines (Diogo et al. 2015). Its fishery operation is
focused on economically important teleost fish
species, such as blackspot seabream Pagellus bogaraveo
and tunas, although the fisheries operate over the habi-
tats of different species, including sharks, skates and
rays, which are mostly caught as by-catch (ICES 2018).
Despite their noted vulnerability (Das and Afonso
2017), few studies have focused on elasmobranchs
from the Azores, being limited to some faunal check-
lists (e.g. Santos et al. 1997; Barreiros and Gadig 2011)
and a few species-specific works (e.g. Aranha et al.
2009; Sobral and Afonso 2014). The main objective of
the present study was to analyse all fishery and
survey data available for elasmobranchs (Class Elasmo-
branchii) caught over the past c. 25 years around the
Azores to provide baseline information about their
© 2020 Informa UK Limited, trading as Taylor & Francis Group
CONTACT Régis Santos regisvinicius@gmail.com IMAR Institute of Marine Research, University of the Azores, 9901-862, Horta, Portugal Okeanos
R&D Centre, University of the Azores, 9901-862, Horta, Portugal MARE Marine and Environmental Sciences Centre, University of the Azores, 9901-862, Horta,
Portugal
MARINE BIOLOGY RESEARCH
https://doi.org/10.1080/17451000.2020.1718713
Published online 11 Feb 2020
fisheries, biology and ecology, which can be used to
inform stock assessment and management strategies.
For this, we updated the annotated list of elasmo-
branch species occurring in the Azorean Exclusive
Economic Zone (EEZ; ICES Subdivision 10.a.2);
described the related fishery information; characterized
the depth distribution of the main species; and evalu-
ated annual changes in their observed abundance
and size composition. We hypothesized that elasmo-
branch assemblage of the Azorean region is vulnerable
to overfishing, exhibiting a decrease in abundance
indices and changes in the length-frequency distri-
bution caused by size-selective fishing.
Material and methods
Study area
The Azores (Figure 1) is located along the Mid-Atlan-
tic Ridge (MAR) between 36° to 40°N and 24° to 32°
W, in the ICES Subdivision 10.a.2. The archipelago is
composed of nine volcanic islands (Western: Flores
and Corvo; Central: Faial, Pico, Graciosa, São Jorge
and Terceira; Eastern: São Miguel and Santa Maria)
characterized by the absence of a continental shelf,
steep slopes and irregular topography. The Azorean
EEZ is about 1 million km
2
with an average
depth of around 3000 m, and only 3% of the EEZ
is less than 1,000 m deep, and this has a discontinu-
ous distribution (Menezes et al. 2006). The
volcanic characteristic is represented by numerous
seamounts around the Azores with very different
configurations and occupying 37% of the EEZ
(Morato et al. 2008).
Data collection and analyses
Mostly four types of data were analysed in this study:
species occurrences, survey data, commercial landings
and commercial catch rates.
An updated checklist of elasmobranch (Class Elas-
mobranchii) species from the Azores EEZ was made
by adding species caught in the Azorean spring
bottom longline surveys (ARQDAÇO) to previous
occurrence lists from Santos et al. (1997), Barreiros
and Gadig (2011), and Das and Afonso (2017).
Species listed by these authors, but with (1) no
record published in scientific platforms, (2) occurrence
in the Azorean EEZ without confirmation, or (3) record
outside the Azorean EEZ were included in the check-
list as uncertain species.
Figure 1. The Azores archipelago (NE Atlantic Ocean) with depth contours layers and location of the nine islands (in black), and the
limit of the Exclusive Economic Zone (EEZ). The dashed line represents the approximate location of the Mid-Atlantic Ridge (MAR).
2R. SANTOS ET AL.
The ARQDAÇO surveys were conducted from 1995
to 2018 onboard the R/V ‘Arquipélago’and followed
a stratified random design around the islands, banks,
and major seamounts of the Azores archipelago. The
survey is currently designed for blackspot seabream,
which is the most economically important teleost
species in the Azorean region (Pinho 2003). Each
sampling area is divided into depth strata with 50 m
intervals down to 800 m depth and for some pre-
defined sets, down to 1200 m. The survey gear
(bottom longline for benthopelagic species) is similar
to the one used by the local commercial fleet. All
fishes caught are tallied by species and strata,
measured and weighed. Detailed information on
survey design can be found on Pinho (2003),
Menezes et al. (2006) and ICES (2010).
A relative abundance index (mean catch per unit of
effort weighted by area size) was calculated for each
species collected during the ARQDAÇO by depth
strata and statistical area. These abundance indices
were summed across depth strata and statistical
areas to compute an annual abundance index. The
length composition was also computed by the statisti-
cal area and stratum as a proportion by the length of
the mean catch per unit of effort weighted by area
size. These abundance indices by length were then
summed across depth strata and statistical areas to
compute an annual length composition. For more
details on abundance estimation procedure see Pinho
(2003).
Elasmobranchs collected during the ARQDAÇO
surveys were classified into four demersal fish assem-
blages according to Menezes et al. (2006): a shallow-
shelf/shelf-break assemblage at depths < 200 m, an
upper-slope assemblage at 200–600 m, a mid-slope
assemblage at 600–800 m and a deep mid-slope
assemblage at 800–1200 m. For each species, this
classification was based on the mean depth of occur-
rence weighted by the relative abundance (Menezes
et al. 2006). A fifth group (pelagic assemblage) was
used for all pelagic species.
In addition, the species were categorized into three
groups according to the relative abundance (i.e. the
abundance of an elasmobranch species divided by
the total abundance of all fish species caught) and
relative frequency of occurrence (i.e. the number of
sets where an elasmobranch species occurred
divided by the total number of sets). Frequent
species included species with relative abundance
values ≥1% and with an average frequency of occur-
rence ≥4%. Common species included species with
average relative abundance values between 0.01
and 1%, and frequency of occurrence between 0.1
and 4%. Rare species included species with relative
abundances ≤0.01% and a frequency of occurrence
≤0.1%.
Pelagic species and species not-captured during the
ARQDAÇO surveys were classified into the depth-
aligned assemblages and abundance categories
based on published data (Barreiros and Gadig 2011;
Menezes et al. 2012; Martins 2013; Sobral and Afonso
2014; Froese and Pauly 2018; IUCN 2018).
Fisheries information (main fishing gear and associ-
ated fishery) was provided for all species using pub-
lished scientific data (e.g. Menezes et al. 2006;
Machete et al. 2011; Coelho et al. 2012; ICES 2018)
and expert knowledge when the information was not
published. Not applicable (NA) was used for main
fishing gear and fishery of species recorded but rarely
captured by the Azorean fishing fleet.
Only frequent, non-pelagic species associated with
the demersal fishery, and with data available from the
ARQDAÇO surveys, were selected for detailed ana-
lyses. Commercial landing data (catch, effort and
size) from the Azorean bottom longline fleet (Euro-
pean Commission’s Data Collection Framework –
DCF and Auctions service of the Azores –Lotaçor
S.A. databases) were examined for each selected
species.
Standardized catch-per-unit-effort (CPUE, kg 10
−3
hooks) was estimated for each selected species from
the available fishery data (DCF, 1990–2016). This esti-
mation was based on the Generalized Linear Modelling
approach using a hurdle model (Lo et al. 1992; Ortiz
and Arocha 2004; Zuur and Ieno 2016). The standardiz-
ation protocols assumed a hurdle model with a bino-
mial error distribution and logit link function for
modelling the probability that a null or positive obser-
vation occurs (proportion of positive catches), and a
lognormal error distribution with an identity link func-
tion for modelling the positive catch rates on successful
trips. For more details on CPUE standardization pro-
cedure see ICES (2018).
Analyses of variance with Dunn’s test as post-hoc
comparison technique were performed to test the sig-
nificance among abundances at different depths
(Kruskal–Wallis test, α= 0.05), and to test differences
in total lengths (L
T
) among depths and years (Mood’s
median test, α= 0.05).
All the analyses were conducted using the software
R-3.5.1 (R Core Team 2018) with additional packages
lmtest (Zeileis and Hothorn 2002), lattice (Sarkar
2008), influence.ME (Nieuwenhuis et al. 2012), lme4
(Bates et al. 2015) and lsmeans (Lenth 2016).
MARINE BIOLOGY RESEARCH 3
Results
Species checklist, taxonomy and categories
A total of 57 species (41 sharks, 16 batoid species)
belonging to 22 families of elasmobranchs have been
recorded in the Azorean region (Table I). Thirty-three
elasmobranch species (23 sharks, 10 batoid species)
belonging to 14 families were caught in the
ARQDAÇO surveys (Table I and II). The family Rajidae
was the most species-rich (eight species), followed by
the Somniosidae (seven species) and Carcharhinidae
(five species). About 41% of the species are benthope-
lagic, 33% demersal and 26% pelagic.
Fifteen species were assigned into a pelagic assem-
blage, nine species in the shallow-shelf/shelf-break
assemblage (<200 m), 11 species into the upper-slope
assemblage (200–600 m), three species into the mid-
slope assemblage (600–800 m), and 19 species in the
deep mid-slope assemblage (>800 m). Overall, the
number of benthopelagic and demersal species
increased from shallow-shelf/shelf-break to deep
waters.
Ten species were classified as frequent –Isurus oxy-
rinchus,Mobula birostris,Mobula tarapacana,Prionace
glauca,Deania calcea,D. profundorum,Etmopterus
pusillus,E. spinax,Galeorhinus galeus and Raja clavata.
The last six demersal species were caught in larger
numbers in the ARQDAÇO surveys (Table II) and were
selected for detailed analyses. The remaining species
were classed as either common (14 species) or rare
(33 species; Table I).
Fisheries
Elasmobranch landings in the Azorean region have
been mostly associated as by-catch from three main
fisheries: the swordfish Xiphias gladius fishery, black
scabbardfish Aphanopus carbo fishery, and the demer-
sal longline fishery (Table I).
Elasmobranch by-catch in the swordfish pelagic
longline fishery consists mainly of pelagic sharks,
such as shortfin mako and blue shark Prionace
glauca. Elasmobranchs caught in the black scab-
bardfish deep-water fishery are mostly benthopelagic
and demersal species (e.g. Centrophorus spp., Deania
spp., Etmopterus spp., Dalatias licha,Centroselachus
crepidater,Centroscymnus owstoni). The demersal
longline fishery represents one of the most important
fishing activities in the Azores, and its associated
elasmobranch by-catch frequently include thornback
ray Raja clavata, tope shark Galeorhinus galeus, bird-
beak dogfish Deania calcea, arrowhead dogfish
D. profundorum, smooth lanternshark Etmopterus
pusillus, and velvet belly E. spinax (Table I).
Commercial landings and species abundance
Total annual elasmobranchs landings in the Azores
have decreased from early 1990s to the 2000s and
increased thereafter (Figure 2). Demersal species
(mainly associated with black scabbardfish fishery
and demersal fishery) constitute the main group of
elasmobranchs landed in the Azores (Figure 2).
Reported annual landings for G. galeus and
R. clavata showed a decreasing trend from 1998/2000
to 2009, and some recovery after this period (Figure
3). In recent years, annual landings of R. clavata have
declined steeply (<80 t y
−1
). Standardized CPUE from
the fishery showed trends with behaviour slightly
similar to that described above for both species, con-
trary to those from survey-derived records showed a
more oscillating pattern over time.
Both G. galeus and R. clavata landed by the local
fishing fleet showed a large and significative annual
variability in the L
T
(χ
2
= 62052.3, d.f. = 26, P< 0.001;
χ
2
= 42565.6, d.f. = 26, P< 0.001, respectively), but no
clear trend was observed in the data (Figure 4). For
survey data, R. clavata were significantly smaller
between 2002–2004 (χ
2
= 461.0, d.f. = 18, P< 0.001)
when compared to the other years. Individuals of
G. galeus were caught in significantly larger sizes in
1997, 2016 and 2017 (χ
2
= 328.3, d.f. = 18, P< 0.001).
Overall, 25–75% (Q3) of the individuals from both data-
sets presented L
T
between 55–169 cm for G. galeus and
between 45–78 cm for R. clavata (Figure 4).
Landings of Etmopterus species have been reported
in a generic category, and its values were almost zero
(Figure 3). Consequently, there are no data to estimate
abundances from the fishery. Abundance indices from
surveys were calculated for E. spinax and E. pusillus sep-
arately, and they showed decreasing trends since 2000/
2003 (Figure 3). Etmopterus spinax were significantly
smaller in 2018 (χ
2
= 76.4, d.f. = 18, P< 0.001), but
E. pusillus did not show significat differences in their
L
T
over the study period (χ
2
= 58.2, d.f. = 18, P> 0.05).
The Q3 of the individuals presented L
T
between 29–
42 cm for E. spinax and between 26–45 cm for
E. pusillus (Figure 4).
As for Etmopterus species, annual landings for
Deania spp. are almost zero, mainly after 2010
(Figure 3). Consequently, there are also insufficient
data to estimate abundances from the commercial
fishery. Abundance indices from the scientific surveys
showed an oscillation over time, with a decreasing
trend since 2010 for both D. profundorum and
4R. SANTOS ET AL.
Table I. Elasmobranch species recorded in the Azores region (NE Atlantic, ICES Subdivision 10.a.2), their assigned fish assemblage
and abundance categorization, and related fishery information.
Family Species Common name Habitat
Fish
assemblage
Abundance
categorization
Main
fishing gear Fishery Source
Hexanchidae Hexanchus griseus Bluntnose sixgill
shark
BP U Rare LLS D ABCD
Heptranchias perlo Sharpnose
sevengill shark
BP U Rare LLS D ABCD
[Chlamydoselachidae] [Chlamydoselachus
anguineus]
Frilled shark BP D NA NA NA D
Rhincodontidae Rhincodon typus Whale shark PPRare NA NA BCD
Odontaspididae Odontaspis ferox Smalltooth sand
tiger
BP U Rare NA NA BCD
Lamnidae Carcharodon carcharias Great white shark PPRare NA NA BCD
Isurus oxyrinchus Shorfin mako PPFrequent LLD S, R BCD
Isurus paucus Longfin mako PPRare LLD S D
Lamna nasus Porbeagle shark PPCommon LLD S, R BCD
Cetorhinidae Cetorhinus maximus Basking shark PPRare NA NA BCD
Alopiidae Alopias superciliosus Bigeye thresher PPCommon LLD S CD
Alopias vulpinus Thresher shark PPRare LLD S BC
Pentanchidae Apristurus laurussonii Iceland catshark B D Rare NA NA AD
Apristurus manis Ghost catshark B D Rare NA NA A
Galeus murinus Mouse catshark B D Rare LLS D ACD
Scyliorhinidae Scyliorhinus canicula Lesser-spotted
dogfish
B S Rare NA NA C
Pseudotriakidae Pseudotriakis microdon False catshark B D Rare LLS D ABCD
Triakidae Galeorhinus galeus Tope shark BP S Frequent LLS, LHM,
LTL
D, S, R ABCD
Carcharhinidae Carcharhinus
galapagensis
Galapagos shark PPRare LLD S, R BCD
Carcharhinus leucas Bull shark BP S Rare NA NA C
Carcharhinus
longimanus
Oceanic whitetip
shark
PPRare NA NA BCD
Galeocerdo cuvier Tiger shark BP S Rare NA NA BCD
Prionace glauca Blue shark PPFrequent LLD, LTL S, D, B,
R
ABCD
Sphyrnidae Sphyrna zygaena Smooth
hammerhead
BP S Rare LLS, LHM D, S ABCD
Dalatiidae Dalatias licha Kitefin shark BP M Common LLS, LHM D, B ABCD
Squaliolus laticaudus Spined pygmy
shark
BP D Common LLS, LHM D ABCD
Etmopteridae Centroscyllium fabricii Black dogfish BP D Rare LLS D CD
Etmopterus princeps Great lanternshark BP D Common LLS D, B ABCD
Etmopterus pusillus Smooth
lanternshark
BP D Frequent LLS D, B ABCD
Etmopterus spinax Velvet belly BP M Frequent LLS D, B ABCD
Somniosidae Centroscymnus
coelolepis
Portuguese
dogfish
B D Common LLS D ABCD
Centroscymnus owstoni Shortnose velvet
dogfish
B D Common LLS D, B ABCD
Centroselachus
crepidater
Longnose velvet
dogfish
BP D Common LLS D, B ABCD
Scymnodalatias garricki Azores dogfish BP D Rare NA NA BCD
Somniosus
microcephalus
Greenland shark BP U Rare NA NA CD
Somniosus rostratus Little sleeper shark B D Rare LLS D ACD
Zameus squamulosus Velvet dogfish BP D Common LLS D AD
Oxynotidae Oxynotus paradoxus Sailfin roughshark B U Rare NA NA BCD
Centrophoridae Centrophorus
granulosus
Gulper shark BP D Common LLS D, B ABCD
[Centrophorus
lusitanicus]
Lowfin gulper
shark
BP D NA LLS D D
Centrophorus
squamosus
Leafscale gulper
shark
BP D Common LLS D, B ABCD
Deania calcea Birdbeak dogfish BP D Frequent LLS D, B ABCD
Deania profundorum Arrowhead
dogfish
BP M Frequent LLS D, B ABCD
Torpedinidae Tetronarce nobiliana Electric ray BP U Rare LLS D ABCD
Rajidae Dipturus batis Common skate B U Common LLS D AC
[Dipturus intermedius] Blue skate D S NA LLS D D
Dipturus oxyrinchus Longnosed skate B U Rare LLS D AD
Leucoraja fullonica Shagreen ray B U Common LLS D ABCD
Raja brachyura Blonde ray B U Rare LLS D ABCD
(Continued)
MARINE BIOLOGY RESEARCH 5
Table I. Continued.
Family Species Common name Habitat
Fish
assemblage
Abundance
categorization
Main
fishing gear Fishery Source
Raja clavata Thornback ray B S Frequent LHM, LLS D ABCD
Raja maderensis Madeira skate B U Rare LLS D ABC
Rajella bigelowi Bigelow’s skate B D Rare NA NA BCD
Arhynchobatidae [Bathyraja pallida] Pale ray D D NA LLS D D
Bathyraja richardsoni Richardson’s ray B D Rare NA NA D
Dasyatidae [Bathytoshia centroura] Roughtail stingray D S NA NA NA D
Dasyatis pastinaca Common stingray B S Common LHM D ABCD
Pteroplatytrygon
violacea
Pelagic stingray PPRare LLD S ABCD
Taeniurops grabatus Round fantail
stingray
B S Rare NA NA BCD
Myliobatidae Myliobatis aquila Eagle ray BP S Rare LLD, LLS S, D ABCD
Mobulidae Mobula birostris Giant manta PPFrequent NA NA BCD
Mobula mobular Devil fish PPRare NA NA BD
Mobula tarapacana Sicklefin devil ray PPFrequent NA NA CD
Habitat: P–pelagic, BP –benthopelagic, B –demersal. Fish assemblage: P–pelagic, S –shallow-shelf/shelf-break, U –upper-slope, M –mid-slope, D –deep
mid-slope. Main fishing gear: LLS –set longlines, LHM –handlines and pole-lines, LLD –drifting longlines, LTL –trolling lines. Fishery: D –demersal, B –
black scabbardfish, S –swordfish, R –recreational. NA: not applicable. Source: A –ARQDAÇO surveys, B –Santos et al. (1997), C –Barreiros and Gadig
(2011), D –Das and Afonso (2017). Square brackets highlight that authenticated records from the Azorean EEZ are required to confirm the species occur-
rence. Frequent species selected for detailed analysis are in bold.
Table II. Total number of individuals (n), average number of individuals per year, absolute frequency (number of sets from which
the particular species was caught), depth range (m) and mean and range of length (cm L
T
) for each elasmobranch species caught in
the ARQDAÇO surveys (1995–2018).
Species
Total number of
individuals (n)
Average number of
individuals per year
Absolute
frequency
Depth range
(m)
Mean (min-max) of length
(cm L
T
)
Etmopterus spinax 2902 152.7 913 200–1200 35 (17–52)
Raja clavata 2869 151.0 704 0–600 63 (26–139)
Deania profundorum 2738 144.1 897 250–1200 76 (31–109)
Galeorhinus galeus 1427 75.1 365 0–650 100 (25–185)
Deania calcea 1137 59.8 467 400–1200 90 (51–113)
Etmopterus pusillus 1078 56.7 750 100–1200 36 (16–56)
Centroselachus crepidater 214 11.3 157 650–1200 68 (33–87)
Dipturus batis 156 8.2 127 0–850 95 (34–177)
Prionace glauca 114 6.0 73 50–1150 131 (100–200)
Dalatias licha 102 5.4 100 150–850 118 (43–150)
Squaliolus laticaudus 55 2.9 50 150–1100 24 (17–27)
Centrophorus squamosus 38 2.0 34 550–1200 94 (60–134)
Leucoraja fullonica 37 1.9 25 250–650 73 (53–167)
Centroscymnus owstoni 22 1.2 19 400–1200 85 (31–142)
Centrophorus granulosus 11 0.6 10 550–1200 120 (108–134)
Dasyatis pastinaca 11 0.6 9 0–150 64 (53–73)
Centroscymnus coelolepis 10 0.5 10 700–1200 97 (64–141)
Zameus squamulosus 8 0.4 7 550–1200 84 (65–115)
Etmopterus princeps 7 0.4 7 800–1200 68 (65–70)
Heptranchias perlo 6 0.3 5 100–450 100 (57–123)
Pteroplatytrygon violacea 6 0.3 5 0–150 67 (58–95)
Sphyrna zygaena 5 0.3 4 0–150 81 (65–92)
Pseudotriakis microdon 4 0.2 4 700–1200 174 (41–225)
Raja maderensis 4 0.2 3 0–450 91 (91–91)
Galeus murinus 3 0.2 3 1000–1200 45 (45–45)
Myliobatis aquila 3 0.2 3 50–150 73 (55–90)
Hexanchus griseus 2 0.1 2 300–650 NA
Dipturus oxyrinchus 2 0.1 2 400–550 127 (124–129)
Raja brachyura 2 0.1 2 400–600 NA
Apristurus laurussonii 1 0.1 1 850–900 66 (66–66)
Apristurus manis 1 0.1 1 50–100 39 (35–42)
Somniosus rostratus 1 0.1 1 900–950 NA
Tetronarce nobiliana 1 0.1 1 450–500 100 (100–100)
Total number of sets 9329
Total number of sets with
elasmobranch species
3525
Total number of sampled fishes 139350
Total number of sampled
elasmobranchs
12977
6R. SANTOS ET AL.
D. calcea (Figure 3). Deania profundorum were signifi-
cantly bigger in 1997 and smaller in 2005 (χ
2
= 83.5,
d.f. = 18, P< 0.001). On the other hand, D. calcea did
not show significat differences in their L
T
over the ana-
lysed years (χ
2
= 22.9, d.f. = 18, P> 0.05). The Q3 of the
individuals were 65–99 cm L
T
for D. profundorum and
79–99 cm L
T
for D. calcea (Figure 4).
Depth distribution
Galeorhinus galeus was caught with significantly higher
abundances (H= 573.2, d.f. = 23, P< 0.001) and smaller
L
T
(χ
2
= 128.7, d.f. = 23, P< 0.001) in shallow waters (0–
150 m) and showed a decreasing trend in captures, and
an increasing trend in L
T
, with increasing depth (Figure
5). Raja clavata showed an abundance trend similar to
G. galeus, with significantly higher captures (H= 912.8,
d.f. = 23, P< 0.001) in shallow waters (0–250 m).
However, no statistical difference in its L
T
(χ
2
= 38.3,
d.f. = 23, P> 0.05) was observed between the depths
analyzed (Figure 5).
Etmopterus spinax was significantly more abundant
between 400–750 m (H= 701.7, d.f. = 23, P< 0.001)
and E. pusillus showed significantly higher abundances
between 500–1050 m (H= 309.0, d.f. = 23, P< 0.001;
Figure 5). Significant increases in L
T
of E. spinax (χ
2
=
288.9, d.f. = 23, P< 0.001) and E. pusillus (χ
2
= 171.5,
d.f. = 23, P< 0.001) were observed as a function of
increasing depth (Figure 5).
Deania profundorum and D. calcea were caught with
significant higher abundances in deep waters between
500–900 m (H= 699.1, d.f. = 23, P< 0.001) and between
850–1,200 m (H= 830.0, d.f. = 23, P< 0.001), respect-
ively (Figure 5). No significant statistical difference
was observed in the bathymetric distribution of these
species (D. profundorum:χ
2
= 74.1, d.f. = 23, P> 0.05;
D. calcea:χ
2
= 50.8, d.f. = 23, P> 0.05; Figure 5).
Discussion
Elasmobranch species richness
The variety of the sampling methods used and the
limited amount of directed research on elasmobranch
diversity conducted in the Azorean region raises
doubts on the completeness of available elasmobranch
checklists. The most recent species account (Das and
Afonso 2017) updated the work of Santos et al.
(1997). They listed 56 elasmobranchs (39 sharks, 17
batoid species), and are mostly in agreement with
the species listed in the present study.
Five species listed by the authors above were not
included here as there are either an absence of
records published in scientific platforms and/or need
for further investigation to confirm their occurrence
in the Azorean region (lowfin gulper shark Centro-
phorus lusitanicus, blue skate Dipturus intermedius and
roughtail stingray Bathytoshia centroura), or that the
records were from waters outside the Azorean EEZ
(Frilled shark Chlamydoselachus anguineus and pale
ray Bathyraja pallida).
On the contrary, species such as bull shark Carchar-
hinus leucas, lesser-spotted dogfish Scyliorhinus cani-
cula, common blue skate Dipturus batis and Madeiran
Figure 2. Total annual commercial landings of elasmobranch species in the Azores archipelago.
MARINE BIOLOGY RESEARCH 7
ray Raja maderensis, were listed by Barreiros and Gadig
(2011) and in the current checklist, but were not con-
sidered by Das and Afonso (2017).
Despite the possible incompleteness of the Azorean
elasmobranch checklists, data available in this study
clearly show that the Azorean elasmobranch fauna has
a similar species richness compared to neighbouring
waters from the Macaronesian region (Brito et al. 2002;
Wirtz et al. 2008) and also mainland Portugal
(Machado et al. 2004; Correia et al. 2016). In the Azores
area, five main species assemblages have been ident-
ified according to their habitat and depth preferences:
pelagic assemblage, and four depth-related demersal
assemblages (shallow, upper-slope, mid-slope and
deep; Menezes et al. 2006). The largest observed abun-
dance and species richness of deep-water species
observed reflect the characteristics of the predominant
deep-water habitats in the Azorean EEZ.
Fisheries
Reported elasmobranch landings from the Azorean
region have been mostly associated with four main
fisheries (ICES 2018). Three of these fisheries target
Figure 3. Landings (bars) and relative abundance indexes from the surveys (black colour) and derived from commercial catch and
effort (standardized CPUE) data (blue colour) of elasmobranch species in the Azores archipelago. Both abundance series have been
scaled to their respective means. Dotted lines represent 95% confidence intervals for the standardized CPUE. Abundance estimation
from the commercial CPUE data was only possible for Galeorhinus galeus and Raja clavata.
8R. SANTOS ET AL.
teleosts (swordfish, black scabbardfish and demersal
fishes), in which elasmobranch species are taken acci-
dentally as by-catch. The only Azorean fishery that
specifically targeted elasmobranchs was the fishery
for kitefin shark Dalatias licha, which stopped at the
end of 1990, possibly as a result of economic problems
related to markets (Perrotta 2004).
Elasmobranch by-catch of the swordfish fishery in
the Azores consists mainly of pelagic sharks, particu-
larly the blue shark and shortfin mako. This result is
comparable to those obtained from Portuguese longli-
ners targeting swordfish in the Atlantic Ocean (Coelho
et al. 2012; Roxo et al. 2017). Landings of elasmo-
branchs from the swordfish fishery in the Azores are
Figure 4. Boxplot of length (L
T
) of elasmobranchs species by year (1990–2018) from the Azorean demersal spring bottom longline
survey (black colour) and from the commercial landings (blue colour). Boxes show the quartiles (25–75%), horizontal lines inside
each box show the median, and the limits are shown with whiskers. Empty circles symbol identify outliers and asterisks are extreme
outliers. Length data from landings are only available for Galeorhinus galeus and Raja clavata.
MARINE BIOLOGY RESEARCH 9
considered much smaller than the total by-catch by
swordfish fisheries in the area because of high discards
and fleets operating from the continent.
The black scabbardfish fishery in the Azores started
in 1998, with a two-year experimental phase and only
one vessel engaged in it. It was an almost unexploited
resource in the Azores, and the low local market price is
probably the limiting factor for the development of the
fishery (Machete et al. 2011). Since this fishery is under-
developed, we assume that by-catch by black scab-
bardfish fisheries in the Azores is low. However, as
black scabbardfish may be considered an alternative
resource for Azorean fisheries (see Machete et al.
2011), its by-catch should be monitored appropriately.
Figure 5. Relative abundance index (mean ± 0.95 confidence interval) and boxplot of length (L
T
) of elasmobranch species by
stratum from the Azorean demersal spring bottom longline survey (1995–2018). Boxes show the quartiles (25–75%), horizontal
lines inside each box show the median, and the limits are shown with whiskers. Empty-circle symbols identify outliers and asterisks
are extreme outliers.
10 R. SANTOS ET AL.
Whilst elasmobranchs are not a major by-catch of
the demersal fishery, tope shark and thornback ray
are frequently landed. Landings probably underesti-
mate the catch rates, since discarding is thought to
be high (Fauconnet et al. 2019), particularly of smaller
(immature) specimens. Several deep-water elasmo-
branch species are also taken as by-catch in this
fishery (Centrophorus spp., Centroscymnus spp., Deania
spp., and Etmopterus spp.), particularly whenever the
gear fishes deeper than 600 m, yet most of these are
discarded due to management measures introduced
(zero catches).
Commercial landings and species abundance
A decreasing trend in the landings for thornback ray and
tope shark in the last 2–3 years (Figure 3) is probably
caused by the increase of the discards. Two factors
may be forcing this: (1) the market for these species to
be very limited, with little domestic consumption and
limited demand for export, and (2) the management
measures introduced, particularly the TAC/quotas and
minimum landing size (52 cm L
T
for R. clavata;Figure 6).
In fact, Fauconnet et al. (2019) observed an upward
trend between 2010 and 2014 of total discard amount
by bottom longline and handline fisheries. However,
the methodology used by these authors is limited in
accounting for the temporal trends in discarding prac-
tices resulting from changes in the market and in catch-
limitation regulations. Also, no information on the dis-
carding of skates and tope shark is available for the
recent 2–3 years.
An alternative way to confirm our assumption is to
observe the survey-derived abundance indices and
standardized CPUE from fishery. Fishery-independent
data present an unbiased accounting of stock health
since they are not influenced by specific management
measures or socioeconomic factors. However, abun-
dance indices for R. clavata and G. galeus, presented
a great oscillation over time, with no trend probably
related to sampling design. For R. clavata, this oscil-
lation in abundances may be associated with the varia-
bility of habitats (sandy and rocky grounds) sampled,
where years with high catches would be associated
with years in which the samplings occurred in a
sandy bottom. For G. galeus, the high variability in
abundances may be associated with the low catchabil-
ity of fishing gear used in the surveys. On the other
hand, standardized CPUE from fishery data showed a
more stable trend over time for both species, which
lead us to support the idea that the reduction of land-
ings is associated with the increase of discards. It is
important to emphasize that the standardized CPUE
and abundance indices may be not considered as
proxies of the local abundances because the reliability
of the data, and so, they have not allowed to validate
the stock assessments for skates and also for the
migratory G. galeus in the Azores. Consequently, the
ICES has applied for these species the precautionary
approach to fisheries management (ICES 2018).
Contrary to what is observed for skates and tope
shark, our hands-on experience shows a low post-
release survival rate for deep-sea sharks captured in
surveys (unpublished data). This fact, associated to
high discards of these species in Azorean fisheries (Fau-
connet et al. 2019), may be the reason for the slightly
observed reduction in the survey-derived index of
abundance of Etmopterus spp. and Deania spp.,
especially after 2010 when zero TAC was implemented
for deep-sea sharks (Figure 6).
Population dynamic aspects
As observed for R. clavata (Chevolot et al. 2006; Maran-
del et al. 2018), the distribution and length composition
observed for D. profundorum and Etmopterus spp.
suggest that their stock in the Azores can be con-
sidered distinct management units. Studies demon-
strate that all the maturity stages of E. spinax (Aranha
et al. 2009) and D. profundorum (ARQDAÇO unpub-
lished data) are observed in the Azores archipelago,
but there is no connectivity study confirming the exist-
ence of Azorean stocks.
Detailed studies on population structure of other
deep-sea sharks, such as Centrophorus squamosus (Ver-
íssimo et al. 2011), Centroscymnus coelolepis (Veríssimo
et al. 2012; Catarino et al. 2015) and Centroscymnus cre-
pidater (Cunha et al. 2012) have evidenced genetic
similarity at the intra-oceanic scale, as well as the
capacity of deep-water species to undertake long
migrations (Rodríguez-Cabello and Sánchez 2014).
For D. calcea, the migration capacity was high-
lighted by Clarke et al. (2002). As in the present
study, these authors captured mainly adult fishes in
the Irish waters, while Machado and Figueiredo
(2000) captured smaller fishes in Portuguese waters.
Thus, Clarke et al. (2002) suggested the existence of
possible migration between the Irish and Iberian
waters. Nevertheless, there are some controversies to
this idea (see Paiva et al. 2011) and further studies
should be implemented to clarify the stock identity
and migration processes in the whole NE Atlantic area.
It is important to emphasize that the population
connectivity has two components: genetic and demo-
graphic (Lowe and Allendorf 2010). Despite the impor-
tance of this second component for defining
MARINE BIOLOGY RESEARCH 11
management units, defining appropriate thresholds for
demographically-connected populations has received
relatively little attention in the literature (Marandel
et al. 2018, and references therein). Therefore, more
detailed studies on life history traits and movement
rates of deep-sea sharks are fundamentals for appropri-
ate management advices.
Some of the population dynamic aspects especially
those related to depth distribution were clarified in this
study. In general, bigger-deeper behaviour has been
observed and it is the pattern generally associated with
the species analyzed here (Compagno 1984; Coelho
and Erzini 2007;Aranhaetal.2009; Sousa et al. 2009;
Coelho et al. 2009a,2009b; Ebert and Stehmann 2013).
However, this behaviour was more strongly evidenced
in shallow species (G. galeus and R. clavata)thanin
deep-sea sharks (Figure 5). One of the main reasons is
that the ARQDAÇO survey is not specifically designed
to catch elasmobranchs, and so cannot provide reliable
quantitative information for some species, especially
those with deeper distribution or smaller lengths.
The non-specificity of the fishing gear and operation
also justifies the accidental capture of elasmobranchs by
bottom longlines to be composed mainly by adults (i.e.
larger individuals; Table II,Figure 4). Besides that, the
slow growth rates, which are common in elasmobranch
species, have little effect on the size distribution caused
by size-selective fishing or recent management
measures. Therefore, the results observed here should
be interpreted with caution.
The database used in this study is insufficient for a
formal assessment on the health status of exploited
species but it currently represents one of the main
data sources for management purpose in the Azores.
Abundance estimates should be well adjusted to con-
sider factors such as population structure and environ-
mental characteristics, which may affect the
relationship between catch rates and densities.
Final considerations
Unfortunately, the stock status of some fished species
remains uncertain or unknown due to the poor knowl-
edge of the resource dynamic for the Azorean region.
There is a need to understand more about the
biology, ecology and population structure of elasmo-
branchs to make valuable predictions on the long-
term effects of fishing and ensure that the fisheries
interacting with these species can be sustainably
managed into the future. Consequently, it is suggested
that further studies critically analyse the adequacy of
the survey as data suppliers for monitoring the abun-
dance of both the target species and elasmobranchs
in Azorean waters.
Figure 6. Chronology of the main events and technical measures that influenced fishing opportunities in the Azorean region.
12 R. SANTOS ET AL.
Acknowledgements
The authors thank all who participated in field surveys and
sampling processing onboard the R/V ‘Arquipélago’. Ricardo
Medeiros (ImagDOP/UAz) is thanked for the generation of
the map. An early version of this paper was presented at
ICES Annual Science Conference, held at Hamburg,
Germany between 24 and 27 September 2018.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This study was funded by the Azorean Government under the
European Commission’s Data Collection Framework and the
DEMERSAIS project. Régis Santos was funded by the IMAR
Instituto do Mar, through a Post-doc fellowship [ref. IMAR/
DEMERSAIS/001-2018]. Ana Novoa-Pabon was funded by a
FCT Ph .D. fellowship [ref. SFRH/BD/124720/2016].
ORCID
Régis Santos http://orcid.org/0000-0002-4167-3573
Ana Novoa-Pabon http://orcid.org/0000-0002-7194-7176
Hélder Silva http://orcid.org/0000-0001-7181-1976
Mário Pinho http://orcid.org/0000-0002-8045-2546
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