Edited by: Maria Lourdes D. Palomares, FishBase Information and Research Group, Philippines
Reviewed by: Bernard Seret, ICHTYO CONSULT, France; João Pedro Santos Correia, Polytechnic Institute of Leiria, Portugal
*Correspondence: Diya Das
This article was submitted to Deep-Sea Environments and Ecology, a section of the journal Frontiers in Marine Science
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
A vulnerable species group, such as, the elasmobranchs, in a data-deficient context presents a complicated management problem. Evidence suggests that the Azores islands, a remote archipelago on the Mid-Atlantic Ridge, serve essential functions in the life-history of species across taxa. The diversity of marine resources within its EEZ are exploited by local to international fleets, and the full extent of fishing pressure can often be underestimated. Although sharks and rays appear to be of minor importance in the fishery, the possibilities of illegal, unreported, and unregulated fishing raises concerns about these threatened species. However, this group has failed to attract management attention, visible in the lack of regional studies focused on biodiversity, ecology, or threats of elasmobranchs. Our work attempts to review and update the information on elasmobranchs of the Azores and identify potential threats, mainly by the local fisheries. We aim to highlight knowledge gaps that require further research and conservation actions. We (1) update the annotated checklist of elasmobranch species, (2) compare species distribution across a biogeographically similar section of the North Atlantic, and (3) analyze the interaction of elasmobranch species with local fisheries. We confirm 61 chondrichthyan species for the Azores (39 sharks, 17 rays, and 5 chimaeras), adding 19 species to the previous annotated checklist of 1997. The Azores elasmobranch species assemblage most resembles Madeira, the neighboring Macaronesian archipelago. Biogeographic affinities between the chosen regions of the North Atlantic are reflected in the taxonomic structure of families. Although underestimated in the local fisheries, elasmobranchs constitute a regular but highly variable portion of total landings. Misreporting and misidentification is perhaps the greatest concern in the local fisheries records, further aggravated by few existing catch regulations for elasmobranchs. Local knowledge indicates that the Azores serves as essential habitat for at least a few species in coastal areas and shallow seamounts, and potentially so for a number of deep-sea elasmobranchs. The intersection of fishery threats and local essential habitat functions around the archipelago warrants greater research effort and studies.
The isolation of oceanic islands from continental masses often creates a unique gathering of species (Sandin et al.,
The unique traits of marine ecosystems around oceanic islands render them more vulnerable, deserving superior conservation and management. For instance, the populations and function of predatory species that play an essential role in maintaining ecological balance and ecosystem vitality. The top-down control of lower trophic-level species and ecosystem functions can be seriously disrupted in case of declines in predator populations (Pace et al.,
The main direct threat to elasmobranch species is fisheries exploitation, leading in some cases to extirpation and shifts in local species assemblages (Ward and Myers,
The Azores are a group of remote oceanic islands situated on the Mid-Atlantic Ridge surrounded by depths regularly exceeding 1,500 m (Santos et al.,
The exclusive economic zone (EEZ) of the archipelago occupies an expansive one million square kilometers, where a 100 nautical miles (NM) buffer from the coast is currently reserved for the regional and national fleet beyond which other European fleets are authorized to operate (European Council,
This situation raises conservation and management concerns for local shark and ray populations that are not always protected by catch regulations but are particularly susceptible owning to their life-history strategies (Afonso et al.,
Using the last complete annotated checklist from the region (Santos et al.,
The primary sources used were:
Scientific fishing surveys using bottom longlines carried out by the Department of Oceanography and Fisheries, University of Azores (DOP/UAz), Horta (Menezes et al., The MAR-ECO project by the Census of Marine Life (Fossen et al., An exploratory fishing survey of orange roughy ( Underwater visual census conducted by researchers of the Institute of Marine Research (IMAR—University of the Azores) each year in the shallow-water areas around the islands and offshore seamounts (Afonso et al.,
Species were classified into four classes to designate their presumed frequency of occurrence. The different classes were differentiated by color codes as follows:
Commonly encountered species were designated green—these species have multiple records and no known taxonomic conflicts; Species that occur occasionally around the Azores were yellow —they are rarely recorded despite susceptibility to commonly used fishing gears; Species with scant records, probably due to observational constraints were orange—these species only appear in fishing surveys using trawl gears (Melo and Menezes, Species with uncertain identification were designated red.
Elasmobranch taxonomy is a work in progress, with changes in nomenclature almost every year (Weigmann,
The updated species list was then used to analyze the biogeographical relationship of the Azorean elasmobranch assemblage within the North Atlantic. In order to maintain analytical coherence through a broad comparable environmental envelope, we focused our analysis on the section of the Atlantic bounded by the 42°N (northern extent of Azores EEZ) and 26°N (south of the Canary Islands) latitudes, thus including the Macaronesian archipelagos of Madeira and the Canaries, and the continental margins of the Atlantic to the east (Iberian Peninsula) and west (United States east coast). This section of the North Atlantic was assumed to represent the highest potential biogeographic affinity of species present in the Azores. Tropical regions such as, the archipelago of Cape Verde and Caribbean islands were excluded being separate biogeographic regions (Floeter et al.,
Species lists of the other regions were adapted from regional annotated checklists (Brito et al.,
First, we focused on the elasmobranch species occurring in the Azores and how they are shared with the study areas across the North Atlantic. We added current knowledge on migratory habits of these species (Fowler,
To determine threats to elasmobranchs at the regional level, we focused on the landing records of local fisheries; since there is no clear evidence of habitat destruction, pollution, or other factors threatening the local elasmobranch assemblage. The goal was to identify gear types more likely to land elasmobranchs and the species landed by these gears. Analysis of the landing records also provides the opportunity to recognize potential inaccuracies in the registration process itself. Local fisheries began recording elasmobranch landings in greater taxonomic resolution in official statistics since the mid-1990s. Thus, we chose a 19-year period from 1996 until 2014 to analyze how the local fishery interacts with elasmobranchs, using temporally aggregated landing information.
Landing records are collected from the auction houses (
Having no direct information on catch or effort, we scaled the impact of different métiers using two indicators. The first indicator was the weight of elasmobranchs landed proportional to other species by each métier. The weight of non-elasmobranch species was used as proxy for effort since they are often the target or more lucrative species. Thus, métiers with higher proportional weight landed of elasmobranchs, i.e., weight per unit effort (WPUE), could be preferentially landing these species. The second indicator was the frequency of elasmobranch landings per métier, measured as a percentage of total landings. Using the total number of landings per métier as a proxy for effort, métiers with higher percentage of landings with elasmobranchs, or landings per unit effort (LPUE), would be those more partial to these species.
WPUE was calculated by aggregating the total weight and elasmobranch weight landed by each métier for every month in the study period, separately. The weight of other species was obtained by subtracting weight of elasmobranchs from the total weight, and the ratio obtained for landed weight of elasmobranchs to other species. The arithmetic mean of the ratios was used to reduce the influence of disproportionately large values, and standard deviation used as an indication of variability. Similarly for LPUE values, the total number of landings per métier and the number of landings with elasmobranchs were aggregated to obtain the frequency of elasmobranch landings. All calculations and data analysis was executed in RStudio®.
The métiers were then separated into two categories to facilitate meaningful comparisons. One category featured métiers with higher elasmobranch LPUE (both proportional weight and landing frequency), thus greater tendency to catch and land these species, and a second category for métiers that land less elasmobranchs. The species composition of the two groups was analyzed separately. We used average weight of species per landing to identify species that are landed infrequently but could require greater management attention.
The species landed by the local fisheries were then related to their regional IUCN Red List (Nieto et al.,
Our literature search confirmed 61 chondrichthyans from the Azores EEZ (39 sharks, 17 batoids, and 5 chimaeras; Table
Final species checklist with color codes; green: common, yellow: rare, orange: rare due to gear constraints, red: uncertain identification.
Chimaeriformes | Rhinochimaeridae | Holt and Byrne, 1909 | ||
Chimaeridae | Linnaeus, 1758 | |||
Luchetti et al., 2011 | ||||
de Brito Capello, 1868 | ||||
Hardy and Stehmann, 1990 | ||||
Orectolobiformes | Rhincodontidae | Smith, 1828 | ||
Lamniformes | Odontaspididae | Risso, 1810 | ||
Alopiidae | Lowe, 1841 | |||
Cetorhinidae | Gunnerus, 1765 | |||
Lamnidae | Linnaeus, 1758 | |||
Rafinesque, 1810 | ||||
Guitart, 1966 | ||||
Bonnaterre, 1788 | ||||
Carcharhiniformes | Pentanchidae | Saemundsson, 1922 | ||
Collett, 1904 | ||||
Pseudotriakidae | de Brito Capello, 1868 | |||
Triakidae | Linnaeus, 1758 | |||
Carcharhinidae | Snodgrass and Heller, 1905 | |||
Poey, 1861 | ||||
Péron and Lesueur, 1822 | ||||
Linnaeus, 1758 | ||||
Sphyrnidae | Linnaeus, 1758 | |||
Hexanchiformes | Chlamydoselachidae | Garman, 1884 | ||
Hexanchidae | Bonnaterre, 1788 | |||
Bonnaterre, 1788 | ||||
Squaliformes | Centrophoridae | Bloch and Schneider, 1801 | ||
Barbosa du Bocage and de Brito Capello, 1864 | ||||
Bonnaterre, 1788 | ||||
Lowe, 1839 | ||||
Smith and Radcliffe, 1912 | ||||
Etmopteridae | Reinhardt, 1825 | |||
Collett, 1904 | ||||
Lowe, 1839 | ||||
Linnaeus, 1758 | ||||
Somniosidae | Barbosa du Bocage and de Brito Capello, 1864 | |||
Barbosa du Bocage and de Brito Capello, 1864 | ||||
Garman, 1906 | ||||
Kukuev and Konovalenko, 1988 | ||||
Bloch and Schneider, 1801 | ||||
Risso, 1827 | ||||
Günther, 1877 | ||||
Oxynotidae | Frade, 1929 | |||
Dalatiidae | Bonnaterre, 1788 | |||
Smith and Radcliffe, 1912 | ||||
Torpediniformes | Torpedinidae | Bonaparte, 1835 | ||
Rajiformes | Rajidae | Parnell, 1837 | ||
Linnaeus, 1758 | ||||
Linnaeus, 1758 | ||||
Lafont, 1871 | ||||
Linnaeus, 1758 | ||||
Stehmann, 1978 | ||||
Forster, 1967 | ||||
Garrick, 1961 | ||||
Myliobatiformes | Dasyatidae | Garman, 1880 | ||
Linnaeus, 1758 | ||||
Bonaparte, 1832 | ||||
Geoffroy Saint-Hilaire, 1817 | ||||
Myliobatidae | Linnaeus, 1758 | |||
Mobulidae | Walbaum, 1792 | |||
Bonnaterre, 1788 | ||||
Philippi, 1892 |
NB: The appendix in Santos et al. (
Alopiidae
Santos et al. (
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Pelagic longlines
Local primary literature where species appears: (Simões,
Pentanchidae
The first published record of
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom trawls
Local primary literature where species appears: Appears as
Rajidae
Frequency of occurrence: Red (species identification uncertain)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: Appears as
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: (Menezes,
Dasyatidae
Two specimens of
Frequency of occurrence: Red (species identification uncertain)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines?
Local primary literature where species appears: Confirmed for
Rhinochimaeridae
The first published record of this species occurs in Melo and Menezes (
Frequency of occurrence: Orange (observation constraint)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom trawls
Local primary literature where species appears: (Melo and Menezes,
Chimaeridae
A recently described Holocephalan that is known only since 2011 (Luchetti et al.,
Frequency of occurrence: Red (species identification uncertain)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: ?
Local source: D. Catarino (IMAR/Azores) pers. comm. 2016.
Lamnidae
The first published record of this species from the Mid-Atlantic Ridge is based on two specimens caught north-west of the Azores (Queiroz et al.,
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Pelagic longlines
Local primary literature where species appears: (Martins,
Pentanchidae
First published record of this species in the Azores EEZ was a single specimen caught at a depth of around 1,000 m by longline surveys (Menezes et al.,
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Gear susceptibility: Bottom longlines
Local primary literature where species appears: (Menezes et al.,
Chlamydoselachidae
This rare deepsea species was first recorded from the Azores when an experimental fishing expedition of Atlantic orange roughy (
Frequency of occurrence: Orange (observation constraint)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom trawls
Local primary literature where species appears: (Melo and Menezes,
Centrophoridae
This is a poorly known and rarely sampled species, often confused with its congener
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: Not available
Etmopteridae
This species is rarely recorded in regional demersal fisheries surveys, but is confirmed to occur in the region.
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: (Menezes and Giacomello,
Somniosidae
This cold-water species occurs infrequently in the Azores EEZ, with 2 individuals reported from bottom longline surveys north of the Azores (Fossen et al.,
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Gear susceptibility: Bottom longlines and trawls
Local primary literature where species appears: (Fossen et al.,
First published record from the Azores of one individual in Menezes et al. (
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: (Wenneck et al.,
Synonymous with
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Gear susceptibility: Bottom longlines and trawls
Local primary literature where species appears: Appears as
Arhynchobatidae
This species is captured infrequently, known from only 12 specimens (Orlov et al.,
Frequency of occurrence: Yellow (rare)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: (Fossen et al.,
First published record from the region appears in bottom trawl survey for Atlantic orange roughy (Menezes et al.,
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Local gear susceptibility: Bottom longlines
Local primary literature where species appears: (Fossen et al.,
Myliobatidae
Frequency of occurrence: Green (common)
Record for Azores in FAO Fish Finder (Ebert and Stehmann,
Depth range (Ebert and Stehmann,
Gear susceptibility: ?
Local primary literature where species appears: (Sobral and Afonso,
Records of
Since the distribution of
Distribution of species shared between the Azores and the study regions in the North Atlantic, and their currently known migratory status. The size of the circles are relative to total species diversity.
The elasmobranch assemblage was most similar between the Azores archipelago and Madeira (Figure
Similarity between biogeographic regions by cluster analysis; y-axis represents binary distances. USA, United States east coast; AZO, Azores; MAD, Madeira; CAN, Canaries; POR, Portugal continental shelf.
Configuration of elasmobranch diversity by families across the North Atlantic. USA, United States east coast; AZO, Azores; MAD, Madeira; CAN, Canaries; POR, Portugal continental shelf.
Not all archipelagos of the Macaronesian biogeographic unit clustered together; the Canaries and Portugal continental shelf formed a separate group (Figure
There was a clear separation between the elasmobranch species composition of the western and eastern halves of the North Atlantic (Figure
Local vessels operating within the Azores EEZ landed elasmobranchs regularly, but landings were highly variable within and across métiers. All longline gears had greater landings of elasmobranchs per unit effort (proportional weight and frequency), even when compared to other métiers using hooks such as handlines (Figure
Proportional weight landed of elasmobranchs per unit weight of other species, by fishery métier. INSET, After removing métier pelagic longline.
Pelagic longlines landed by far the largest quantity, proportion (average 0.95 kg elasmobranch WPUE, Figure
Frequency of elasmobranch landings (% of total landings) per métier.
Handlines, gillnets, and fish traps landed between 0.05 and 0.01 kg elasmobranch WPUE with less than 10% elasmobranch LPUE. Six of the 13 métiers recorded in the local fisheries database had minimal interaction with elasmobranchs (<0.01 WPUE, Figure
The longline gears were analyzed separate from the other métiers for species composition by average weight per landing. The average weight per landing of most species was associated with a great degree of variability, deep bottom longline recorded the highest average weight (>1,500 kg/landing) for a species appearing as
Species composition, by regional Red List status, and average weight per landing of métiers using longlines; semi-transparent bars for species with only one landing record. NB, Y-axis different for each panel.
The elasmobranch landings of the remaining métiers visibly differed in species composition from the longline métiers. Instead of a few species dominating landings, multiple species were landed in comparable quantities. Handlines landed the highest diversity of species, with slope species (e.g., genus
Species composition, by regional Red List status, and average weight per landing of remaing métiers (considering only landings with elasmobranch); semi-transparent bars for species with only one landing record. NB, Y-axis different for each panel.
Azorean fisheries broadly target all the three main marine habitat types in the region: coastal (gillnets and handlines), island slopes and seamounts (handlines, drifting deep, and fixed bottom/deep bottom longlines) and pelagic (surface longlines). The sparse empirical information available suggests the presence of EFH for elasmobranchs in each of these three habitats, including nurseries and adult aggregation sites inshore and in the open-ocean, and deepwater ray egg deposition sites (J. Pichazek, pers comm. 2017). Blue sharks use the region's pelagic environment as a nursery for small juveniles that remain in the area for up to 2 years, and maybe even as a pupping ground (Vandeperre et al.,
The species composition of the chondrichthyan assemblage around the Azores is dominated by species that are either oceanic or deep-sea, reflecting the dominant marine habitat surrounding the archipelago. The fact that they are underwhelmingly known becomes evident in the lack or misrepresentation of species occurrence records in regional and global species catalogs. However, the Azorean elasmobranch assemblage emerges as more diverse than expected. Most of the new species additions are a result of nearly two decades of additional sampling effort and the use of different sampling gears. Species like the frilled shark
Continental margins are often richer in biodiversity because of their greater productivity and older geological age. It is thus not surprising that the elasmobranch species on the Azores archipelago are less diverse compared to the continental margins of the Atlantic, a trend common to bony fishes as well (Santos et al.,
Biogeographic studies showed that the Azores have greater proportion of coastal fish species from outside north-east Atlantic compared to the entire Lusitanian province (Almada et al.,
Local fisheries in the Azores operate at a much smaller scale compared to mainland Portugal and other European fleets, where elasmobranch landings can be almost 20 times greater by weight (Correia et al.,
The kite-fin shark
Records from the deepwater drifting longline fishery targeting black scabbardfish are similarly riddled with inconsistencies. Observer reports from the experimental fishery in the Azores (Machete et al.,
Regionally abundant species such as the demersal lantern sharks
The landings of deepwater sharks present an interesting case influenced strongly by legislation as well as commercial value. Misreporting and unreported discards are notorious problems in landing records from deep-sea fisheries (Musick and Musick,
In the Azores EEZ, the fisheries pressure on blue shark is severely underestimated in local records, as a majority of the catches are landed in ports outside the Azores. Our results show that, within the local fishery, reported landings of blue shark can be 20 times higher than landings of other species by weight. These results do not consider the discard or unreported landings, estimated to be up to 80% more than reported landings (Pham et al.,
Blue shark catch by surface longlines has generally not been considered a grave threat to the population status (Cortés et al.,
Of the other species appearing in the pelagic fishery landings, short-fin mako is ranked second most vulnerable out of the 11 pelagic elasmobranch species in the North Atlantic, suggesting it is at high risk of overexploitation (Cortés et al.,
Regional fisheries legislation prohibits the use of any longline gear within a buffer of 6 NM from the coast, but handlines are allowed to operate within buffer limits. This métier seems to opportunistically land elasmobranchs that constitute a regular, though small fraction of their total landings. However, landings from the gillnet fishery, though much smaller in quantity, require special attention. The gillnet fishery in the Azores is regulated by catch limits for both target and non-target species and only operates inshore since it is prohibited below 30 m deep (Portaria n.91,
Based on our results we propose three broad areas of further research that can help to further determine the importance of the wider Azores region for elasmobranchs.
The first data-gap that requires closer inspection are errors and omissions in local fishery data. Robust estimates on the extent of unreported/misreported and discarded catch are required to gauge the actual impact of the local fishery on regional stocks of sharks and rays. Since landings cannot provide a holistic overview of local population status, sentinel or fishery-independent surveys are also imperative to monitor the local elasmobranch populations. Some of these could use non-invasive techniques such as, baited remote cameras for coastal nurseries and deepwater sharks on slopes and seamount summits. Additionally, fisheries studies would benefit from an analysis of socio-economic incentives for landing or discarding of different species. This could provide clues regarding future exploitation trends. The second major gap is the lack of region-specific studies focused on the biology and ecology of local elasmobranchs. Finally, and perhaps most importantly, the essential habitat function of the Azores as nursery, mating, migration, feeding needs to be studied in detail, and across species and habitats. Resolving the importance of the Azores in the wider context of the Atlantic will need many more studies on connectivity of shark and ray populations with, or isolation from, other parts of the species distribution ranges. Population dynamics and tagging studies using electronic, genetic or chemical markers, for example, together with the continued monitoring of species occurrence, will further elucidate the importance of the region as an ontogenetic, permanent, or transitionary habitat, and help pinpoint critical habitats for eventual protection as well as future species range shifts in light of current climatic change scenarios.
PA and DD have equally contributed to: conception and design of this study, data acquisition, analysis, and interpretation, drafting the manuscript and revising it critically for important intellectual content, final approval of the version to be published. Both authors agree to be fully accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of this study are appropriately investigated and resolved.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors are very grateful to Dr. Gui Menezes (IMAR/DRAM, Azores, Portugal), Dr. Pedro Pascual (IEO, Canaries, Spain) and Dr. Mafalda Freitas (OOM/MARE, Madeira, Portugal) for contributing their time to correct the species list from their respective study areas. The authors would like to thank Ms. Dalia Reis (DOP/IMAR) for her help with obtaining the fisheries data, and Dr. Diana Catarino (DOP/IMAR) for pointing out the taxonomic conflict between