Integrating Literature, Biodiversity Databases, and Citizen-Science to Reconstruct the Checklist of Chondrichthyans in Cyprus (Eastern Mediterranean Sea)

: Chondrichthyans are apex predators inﬂuencing the trophic web through a top-down process thus their depletion will affect the remaining biota. Notwithstanding that, research on chondrichthyans is sparse or data-limited in several biogeographic areas worldwide, including the Levantine Sea. We revise and update the knowledge of chondrichthyans in Cyprus based on a bibliographic review that gains information retrieved from peer-reviewed and grey literature, Global Biodiversity Information Facility (135 records of at least 18 species) and the Ocean Biodiversity Information System (65 records of at least14 species), and the citizen science project Mediterranean Elasmobranchs Citizen Observations (117 records per 23 species). Our updated checklist reports 60 species that account for about 70% of the Mediterranean chondrichthyan biota. The list includes 15 more species than the previous checklist and our study reports three new species for Cyprus waters, namely the blackmouth catshark Dalatias licha , the round fantail stingray Taeniurops grabatus , and the sawback angelshark Squatina aculeata . Our research highlights the need for conservation measures and more studies regarding the highly threatened blackchin guitarﬁsh Glaucostegus cemiculus and the devil ray Mobula mobular , and stresses the importance for training a new generation of observers to strengthen the knowledge and conservation of elasmobranchs in the region.


Introduction
Chondrichthyans (sharks, skates, rays, sawfish, and chimeras) play a pivotal role in the marine environment, providing stability to coastal and oceanic ecosystem structures and functions [1,2].Nevertheless, they are heavily overfished worldwide [3,4], with targeted fisheries and bycatch constituting the most significant threats to the conservation of demersal and pelagic species [4,5].This also holds true for the Mediterranean Sea, which used to be considered over the centuries as a chondrichthyan hotspot; at least 50% of its shark and ray species are now threatened with extinction, extirpation, and steep population declines [6][7][8].Limited economic resources, political instability, difficulties in species identification, and low population densities also hamper the conservation of Mediterranean aquatic resources and, in general, of chondrichthyan species [7,9].Illegal landings, mainly by North African fishing fleets, and slow progress in the implementation of an ecosystem approach to fisheries management-provisioned by the European Union (EU) Common Fisheries Policy and Food and Agriculture Organisation (FAO) declarationsare also jeopardizing population recoveries of these taxa in the Mediterranean Sea [8].Finally, declines are generally happening before we gain reasonable knowledge of several cartilaginous taxa, with 13 species of those living in the Mediterranean Sea still listed as "data deficient" according to the Red List evaluation of the International Union for the Conservation of Nature (IUCN) [10].
Open-access databases and citizen science are rapidly, and cost-effectively improving the extent and reach of shared information on marine biodiversity, often filling long-lasting knowledge gaps [11,12].Data sharing tools such as the Global Biodiversity Information Facility (GBIF, https://www.gbif.org/;accessed on 1 May 2020) and the Ocean Biodiversity Information System (OBIS, https://obis.org/;accessed on 1 May 2020) facilitate access to species records.Advances in social media and mobile-phone applications have strengthened citizen science [13], providing extensive information about occurrence data in several phylogenetic groups, including chondrichthyans [9,[14][15][16][17][18][19].The use of internet and crowdsourcing platforms for ecology (also known as "iEcology") moves beyond traditional research studies and generates data about ecological patterns and processes (e.g., species occurrences, distributional range shifts) from digitally stored sources that would otherwise be unavailable [20,21].They provide access to an unprecedented source of information that scientists have only recently started to explore [15,22].These "new-generation" tools are highly useful in supporting correct species identifications and creating more effective and data-driven conservation strategies.
We combined (i) an extensive literature review with information gained from (ii) the online GBIF and OBIS databases and (iii) a focused citizen science project (MECO, Mediterranean Elasmobranchs Citizen Observations) in order to update the knowledge about chondrichthyans living in Cypriot waters.Our aims were to revise the previous chondrichthyan checklist for Cyprus and subsequently better understand whether (i) citizen science can provide crucial data about the biology and ecology of threatened species; (ii) knowledge and conservation of elasmobranchs in the region can be pursued through various approaches.

Study Area
Cyprus is the third largest island in the Mediterranean Sea and is located in the Levantine Basin (eastern Mediterranean).Despite its small size (9.251km 2 ), the marine waters of the Cyprus Exclusive Economic Zone represent a significant water body of the eastern Mediterranean, equal to 98.240 km 2 (Figure 1).These waters are characterised by low nutrient availability (ultra-oligotrophic waters) and low primary production [23], complex water circulation with seasonal variations, sea temperature ranging from about 16 to 28 • C throughout the year, and salinity reaching up to about 39 PSU [14].The southern part experiences cooler waters due to upwelling caused by north-westerly winds [24,25].The coastline is predominantly composed of sand-gravel in the south to south-eastern part, whereas the south-western and the eastern coastline is dominated by rocky substrata [26].The local marine ecosystems and species assemblages are undergoing rapid changes due to multiple pressures acting synergistically, including invasive species, climate change, habitat loss, pollution, and overexploitation [27].
eastern Mediterranean, equal to 98.240 km 2 (Figure 1).These waters are characterised by low nutrient availability (ultra-oligotrophic waters) and low primary production [23], complex water circulation with seasonal variations, sea temperature ranging from about 16 to 28 °C throughout the year, and salinity reaching up to about 39 PSU [14].The southern part experiences cooler waters due to upwelling caused by north-westerly winds [24,25].The coastline is predominantly composed of sand-gravel in the south to southeastern part, whereas the south-western and the eastern coastline is dominated by rocky substrata [26].The local marine ecosystems and species assemblages are undergoing rapid changes due to multiple pressures acting synergistically, including invasive species, climate change, habitat loss, pollution, and overexploitation [27].In the context of this study, all available information within this range was concentrated to produce an updated checklist of chondrichthyans in the region.

Literature Review
We conducted a systematic literature review (up to July 2020), applying the Preferred Reporting Items for Systematic Reviews and Meta-Analyses approach [28].We collected chondrichthyan records from peer-reviewed publications archived in Google Scholar using the keyword "Cyprus" plus the search terms "chondrichthyan(s)", "elasmobranch(s)", "shark(s)", "batoid(s)", "ray(s)" and "skate(s)" to identify items with relevant titles, keywords, or abstracts.We selected "anytime" for the publication date.After duplicates were removed, 158 publications remained to be screened.
We furthermore searched for chondrichthyan records in government reports and policy documents.In particular, these included:

•
CYP EU Data Collection Framework (DCF) reports, published between 2005-2019 and available at the following webpage: https://datacollection.jrc.ec.europa.eu/ars;In the context of this study, all available information within this range was concentrated to produce an updated checklist of chondrichthyans in the region.

Literature Review
We conducted a systematic literature review (up to July 2020), applying the Preferred Reporting Items for Systematic Reviews and Meta-Analyses approach [28].We collected chondrichthyan records from peer-reviewed publications archived in Google Scholar using the keyword "Cyprus" plus the search terms "chondrichthyan(s)", "elasmobranch(s)", "shark(s)", "batoid(s)", "ray(s)" and "skate(s)" to identify items with relevant titles, keywords, or abstracts.We selected "anytime" for the publication date.After duplicates were removed, 158 publications remained to be screened.
We furthermore searched for chondrichthyan records in government reports and policy documents.In particular, these included:  [29] and 45 chondrichthyan species [30], respectively.
Data retrieved from all the above-mentioned sources included (when available) the fish species, the year of sighting, the location, the depth, and the year of publication.

Global Biodiversity Information Facility (GBIF) and Ocean Biodiversity Information System (OBIS)
The Global Biodiversity Information Facility (GBIF) is the largest open-access primary biodiversity database and contains over 1.5 billion species occurrence records [12,31].The Ocean Biodiversity Information System (OBIS), a global open-access database on marine biodiversity for science, conservation, and sustainable development, is focused on marine species and contains more than 6.5 million records for 137,215 species [32].We searched GBIF and OBIS for chondrichthyan records from the Cyprus Exclusive Economic Zone (as defined above) and downloaded them.We checked pictures and records to exclude duplicates from the two databases and the MECO dataset and converted the data to the MECO database format for analysis (see below).

Citizen Science: The Mediterranean Elasmobranchs Citizen Observations (MECO) Project
The MECO project was launched in 2014 in response to enthusiastic scuba divers uploading pictures of sharks and rays from their dives [33].It aims to collate knowledge on chondrichthyan occurrence, seasonality, and distribution using citizen science and social media.The project involves the collaboration of local scientists, which gradually expanded operation to eleven countries and ten Facebook groups (www.facebook.com/pg/theMECOproject; accessed on 1 May 2020).In MECO, participants report their sightings with photographic evidence.Scientific experts request further information, when needed, such as date, location, specimen length and weight, number of individuals observed, and depth of the observation (if applicable).The experts then check pictures for authenticity by using a Google automatic image recognition tool, and identify all original pictures to the lowest possible taxonomic level.Whenever possible, experts also record data such as maturity, gestation, and sex.Finally, there is also a two-way dialogue between citizen participants and scientific experts to retrieve historical records based on old pictures and social media posts.

Updated Taxonomy and Nomenclature
Bibliographic data were critically analysed and taxonomically updated to the latest nomenclature available.Specimens recorded through open-access databases and the MECO project were identified to the lowest taxonomic level possible following [34,35].Species nomenclature follows the Eschmeyer's Catalog of Fishes [36].

Updated Checklist of Chondrichthyans in Cyprus
The literature review revealed 12 publications reporting chondrichthyan records in Cypriot waters (Table 1 and references therein).Twenty more articles mentioned cartilaginous fishes to occur around Cyprus, but they did not have sufficient information about sightings to be included in our review (e.g., general reports with no coordinated or declared areas around Cyprus, reports of species found in auction markets, papers based on International Commission for the Conservation of Atlantic Tunas (ICCAT) data working with offshore longlining boats potentially in international waters, field identification guides, and publications from other locations (e.g., Spain) that appeared in the search), and thus were excluded.
The updated checklist of chondrichthyans in Cyprus is reported in Table 1.It is now composed of 60 species, 15 more than the previous checklist (see [30]), with three species first recorded from Cyprus during this review.A1).Over half (54%) of the records were collected between June and September.Around half of the records came from recreational fishers (Figure 2B), 17% from scuba-divers (Figure 2C), 15% from snorkelers (Figure 2C), and 10% from professional fishers (Figure 2A).Most specimens were identified to species level, and the most common reports included the blackchin guitarfish Glaucostegus cemiculus (Geoffroy Saint-Hilaire, 1817) (n = 15), the common stingray Dasyatis pastinaca (Linnaeus, 1758) (n = 11), and the bull ray Aetomylaeus bovinus (Geoffroy St. Hilaire, 1817) (n = 10).Observations of the round fantail stingray Taeniurops grabatus (Geoffroy St. Hilaire, 1817) and of the sawback angelshark Squatina aculeata (Cuvier, 1829) also constituted the first records of these species in Cyprus (Table 1; Figure 3).The updated checklist of chondrichthyans in Cyprus is reported in Table 1.It is now composed of 60 species, 15 more than the previous checklist (see [30]), with three species first recorded from Cyprus during this review.

Discussion
The updated chondrichthyan fauna of Cyprus now includes 32 species of sharks and 28 species of batoids (skates and rays), and accounts for about 70% of the total chondrichthyan biota known from the Mediterranean Sea [7].We do not expect that this list is complete or free from errors.In fact, shallow habitats around Cyprus are indeed targeted by recreational and professional fishers, and are regularly dived year-round by locals and tourists, thus providing a wealth of photographic records of inshore chondrichthyans.However, the deep-sea waters around Cyprus are almost unexplored,

Discussion
The updated chondrichthyan fauna of Cyprus now includes 32 species of sharks and 28 species of batoids (skates and rays), and accounts for about 70% of the total chondrichthyan biota known from the Mediterranean Sea [7].We do not expect that this list is complete or free from errors.In fact, shallow habitats around Cyprus are indeed targeted by recreational and professional fishers, and are regularly dived year-round by locals and tourists, thus providing a wealth of photographic records of inshore chondrichthyans.However, the deep-sea waters around Cyprus are almost unexplored, and this may be why, since the last list provided by [30], 15 new species have been recorded in the past 15 years.Finally, four species are listed here with caution, namely Sphyrna mokarran (Rüppell, 1837), Carcharhinus brevipinna (Valenciennes, 1839), and Carcharhinus melanopterus (Quoy & Gaimard, 1824), whose Mediterranean records are generally very scarce and often based on misidentifications [7], and Dasyatis marmorata (Steindachner, 1892), whose records should be confirmed through molecular means [7].
Despite these potential limitations, results of the present study confirm the importance of open-access biodiversity databases and citizen science approaches.Alongside these data, EU guidelines for data policy (EU REG 2017/1004), the Open Data Directive that entered into force on 16 July 2019 (Directive (EU) 2019/1024) to promote "open access policies" from publicly funded research and the FAIR (findability, accessibility, interoperability, and reusability) principles should be also taken into consideration for the elaboration of an open-access and transparent framework for commercial and survey fisheries data, in parallel to what is already in use for data in other areas including the ICES area.GBIF and OBIS records respectively accounted for 42.5% and 20.4% of the final dataset, including a species new for Cyprus.Funding and institutional support to such databases are critical, as these data may be useful in order to influence science-based policy decisions [12,50].
The citizen science MECO project yielded more than 100 unpublished elasmobranch records in a single year, including those of two species newly recorded here from Cyprus.It also allowed us to trace relevant data regarding historical ecology and species biology and ecology.As an example, until our work, the big eye thresher shark Alopias superciliosus Lowe, 1841 was only known from Cyprus based on records held in 2010 and 2015 [45].We collected evidence that the species had been recorded from Cyprus since at least ~1970, but was probably misidentified in the past as the common thresher Alopias vulpinus (Bonnaterre, 1788).Our data also confirm the findings of [49], who suggested that Cyprus should be considered a crucial area for the conservation of G. cemiculus, a species listed as critically endangered by the IUCN Red List and whose populations have drastically decreased all along the African coastline due to overfishing [51].In addition to Cyprus, this taxon now only survives in few locations in the Mediterranean Sea, namely, the Gulf of Gabes [52], the Israel coast [53], and Iskenderun Bay [54].In addition, we recorded a pregnant G. cemiculus, suggesting that members of this species nurse and potentially spawn in Cyprus; a specimen of A. bovinus observed on different days in Akrotiri Bay (south coast of Cyprus), suggesting site fidelity by this species; migration routes by M. mobular, with aggregations of large specimens occurring in late winter-early spring; and in general, spawning aggregations of stingrays (Dasyatis pastinaca and Bathytoshia lata), with pregnant females observed during spring and summer seasons.
Apart from the data and the observations new reported here, we noticed that professional fishers communicated (caught) elasmobranchs listed as Vulnerable, Endangered, or Critically Endangered by the IUCN Red List in 67% of the cases, whereas this percentage decreased to 52% when analysing data provided by recreational fishers.These numbers agree with other Mediterranean studies; for example, about 50-60% of the elasmobranch landings in Greek sites were threatened species [55].However, it is also possible that fishers mostly communicated to us species perceived as rare, while other common taxa (such as, for example, Raja species) were usually considered as of "no interest".Finally, we traced ten illegal fishing activities, accounting for 8% of the MECO records available.In addition, one participant posted on social media an encounter with the vulnerable species Isurus oxyrinchus Rafinesque, 1810, but then a spear fisher used this information to locate and kill the fish.Although the fisher may have been potentially unaware of its protection status and conservation importance, the Department of Fisheries and Marine Research of Cyprus initiated legal procedures against him, with the results of this procedure still pending.Such information is vital in understanding interactions of fishers with vulnerable and threatened species as well as illegal incidents that might occur.

Conclusions
Our study highlights the knowledge gaps that exist in elasmobranch occurrence, ecology, and interactions with human activities.In response, Cyprus has recently increased the scientific team involved in the data collection framework through the DFMR, recognising a major opportunity for capacity building in monitoring programs with more on-board fisheries observations.Given the success of citizen science projects in other regions and the emergence of MECO project, the training of divers and snorkelers using bespoke local identification guides may offer another cost-effective means of obtaining data on diversity, abundance, and seasonality of elasmobranchs around Cyprus.Satellite tracking, acoustic tagging, and baited remote underwater video cameras may also offer a suite of more technical tools to recognise the importance of Cypriot waters for Mediterranean chondrichthyans.An ongoing EU-LIFE project (Elasmobranch Low Impact Fishing Experience) includes the training of monitoring authorities and fishers on species identification, relevant legislation, safe release of individuals, as well as satellite tagging to estimate mortalities following incidental by-catch.In addition, the DFMR, in cooperation with a regional FAO project (EastMed and General Fisheries Commission of Mediterranean), organised a tailored species identification webinar for scientific observers, officers, and control inspectors, in order to enhance data quality and acquisition.This activity is provisioned to be an ongoing process and was already proposed at the last EastMed project annual coordination committee meeting (by the Cyprus delegation) to have a regionalised application.The hope is that all these efforts will reduce fishing impacts and will turn the tide in favour of heightened protection of the Cypriot and Mediterranean chondrichthyans and biota in general.

Figure 1 .
Figure 1.The Exclusive Economic Zone of the Republic of Cyprus.In the context of this study, all available information within this range was concentrated to produce an updated checklist of chondrichthyans in the region.

Figure 1 .
Figure 1.The Exclusive Economic Zone of the Republic of Cyprus.In the context of this study, all available information within this range was concentrated to produce an updated checklist of chondrichthyans in the region.

Figure 2 .
Figure 2. Percentage of observations per: (A) broader area as reported by citizen scientists to the MECO project (numbers represent the percentage of observations) and (B,C) types of observers (i.e., professional, recreational fishers, and scuba divers-snorkelers, respectively) in different conservation statuses.Critically Endangered (CR) = in a particular and extremely critical state; Endangered (EN) = very high risk of extinction in the wild; Vulnerable (VU) = meets one of the five red list criteria and thus considered to be at high risk of unnatural (human-caused) extinction without further human intervention; Near Threatened (NT) = close to being at high risk of extinction in the near future; Least Concern (LC) = unlikely to become extinct in the near future.Data Deficient (DD) = lack of sufficient data to evaluate the species status.

Figure 2 .
Figure 2. Percentage of observations per: (A) broader area as reported by citizen scientists to the MECO project (numbers represent the percentage of observations) and (B,C) types of observers (i.e., professional, recreational fishers, and scuba divers-snorkelers, respectively) in different conservation statuses.Critically Endangered (CR) = in a particular and extremely critical state; Endangered (EN) = very high risk of extinction in the wild; Vulnerable (VU) = meets one of the five red list criteria and thus considered to be at high risk of unnatural (human-caused) extinction without further human intervention; Near Threatened (NT) = close to being at high risk of extinction in the near future; Least Concern (LC) = unlikely to become extinct in the near future.Data Deficient (DD) = lack of sufficient data to evaluate the species status.

Figure 3 .
Figure 3. (A).Aggregation of Mobula mobular observed in 2020 in Cyprus.Photo credit: Marios Chisophorout.(B).A Carcharhinus plumbeus juvenile caught and released by a recreational fisher in 2018 in Cyprus.(C).A Squatina aculeata individual caught by a recreational fisher in 2020 in Cyprus.Photo credit: Stelios Kotzikas.(D).A female Glaucostegus cemiculus caught and released by a recreational fisher in 2010 in Cyprus.Photo Credit: Pampos Stavrou (E).A possible record of Dasyatis marmorata reported by Marine and Environmental Research Lab in 2020 from Cavo Greco, Cyprus.Photo Credit: Demetris Kleitou (F).A Taeniurops grabatus individual reported from a photo record that dates back in 1977 from Cyprus.Photo Credit: George Karamanos.

Figure 3 .
Figure 3. (A) Aggregation of Mobula mobular observed in 2020 in Cyprus.Photo credit: Marios Chisophorout.(B) A Carcharhinus plumbeus juvenile caught and released by a recreational fisher in 2018 in Cyprus.(C) A Squatina aculeata individual caught by a recreational fisher in 2020 in Cyprus.Photo credit: Stelios Kotzikas.(D) A female Glaucostegus cemiculus caught and released by a recreational fisher in 2010 in Cyprus.Photo Credit: Pampos Stavrou (E) A possible record of Dasyatis marmorata reported by Marine and Environmental Research Lab in 2020 from Cavo Greco, Cyprus.Photo Credit: Demetris Kleitou (F) A Taeniurops grabatus individual reported from a photo record that dates back in 1977 from Cyprus.Photo Credit: George Karamanos.

Table 1 .
Updated checklist of chondrichthyan species recorded from Cyprus (eastern Mediterranean Sea), with number of records obtained through the various unpublished sources (GBIF, Gb; MECO, Me; OBIS, Ob) and references.Abbreviations used: * species newly recorded here; ** species listed with caution.