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Front. Mar. Sci. | doi: 10.3389/fmars.2019.00113

Fish biodiversity in three northern islands of the Seaflower Biosphere Reserve (Colombian Caribbean)

Arturo Acero P.1*,  Jose J. Tavera2,  Andrea Polanco F.3 and Nacor Bolaños-Cubillos4
  • 1Universidad Nacional de Colombia, Colombia
  • 2University of Valle, Colombia
  • 3José Benito Vives de Andréis Marine and Coastal Research Institute, Colombia
  • 4Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Providencia y Santa Catalina (CORALINA), Colombia

1 Background
The archipelago of San Andres, Providence and Santa Catalina was declared by the United Nations Educational, Scientific and Cultural Organization (UNESCO) as the Seaflower Biosphere Reserve in the year 2000. With 180000 km2, the archipelago boasts a variety of ecosystems and relatively high levels of biodiversity within the region. In light of the urgent need to appraise the value of marine biodiversity within the reserve and understand its role in contributing to food security for the resident human population, the Colombian government has organized three annual expeditions to three different northern islands. The dataset presented here summarizes the information on fish biodiversity collected in three of the reserve’s northern islands, namely Roncador, Serrana, and Serranilla during 2015-2017. In order to include all the information about the Colombian northern islands of the archipelago, data from Quitasueño were also added despite is has not been visited yet by this series of annual expeditions.
2 Data description
2.1 Study Area
The archipelago of San Andres, Old Providence and Santa Catalina (Colombia) occupies a relatively small, yet important portion of the central western Caribbean Sea between 82 and 86 °W meridians and 12 and 16 °N parallels. The three main islands are populated by “raizales” (i.e. an Afrocolombian ethnic group mainly dedicated to fishing and trade among the islands of the reserve), mainland Colombians, and foreigners. According to the national laws, fishing is only allowed for raizales, yet enforcement is weak and illegal fishing by fleets from Jamaica, Nicaragua, Honduras, and others, is common. Enforcement is particularly challenging on the smallest islands of the reserve, as these are patrolled by an often small number of officials and vessels of the Colombian naval force. The archipelago encompasses about three fourths of the more than one hundred Colombian coralline formations. Since 2014 the Colombian government through the Comisión Colombiana del Océano (CCO) has carried out three annual scientific expeditions to the reserve visiting one island at a time. To date, three northern islands have been intensively surveyed, namely Roncador in 2015 (13.533333 N, -80.05 W), Serrana in 2016 (14.383333 N, -80.2 W), and Serranilla in 2017 (15.833333 N, -79.833333 W).
2.2 Methods
Here we compile a fish biodiversity dataset for Roncador, Serrana, and Serranilla from various sources. The first one is a published checklist of species (n =653) distributed in 121 families constructed based on 28 papers (peer-reviewed and non-peer-reviewed) published since 1944, as well as on unpublished data gathered by the authors over the past two decades (Bolaños-Cubillos et al., 2015). The second source corresponds to a series of unpublished biological records which are partially available at the Biodiversity Information System of Colombia (SIB Colombia) and were collected during the 2015, 2016, and 2017 Seaflower Expeditions (Acero P. 2018; Acero P. et al. 2018; Polanco F. 2018). The third and last source comprised a list of species found on the deep shelves and upper slopes of the islands of the reserve (Robertson & Van Tassell 2015; Polanco F. 2015). For the sake of completeness, all information available from Quitasueño (the only northern island of this archipelago not visited yet by these series of expeditions), usually from Robertson & Van Tassell (2015) or from unpublished short visits by Colombian scientist, is included.
During the expeditions organized by the CCO data were collected by scuba diving as well as snorkeling over a total of 250 man-hours of underwater observation, using the 30-min timed free swim method in depths ranging between 0 and 35 m. As our main objective was to focus on species richness, six ecological units (sensu Invemar-ANH, 2012) were surveyed, namely Octocoral-Sponges, Macroalgae-Octocoral-Sponge Meadows, Bioturbated Sediment – Calcareous Algae, Leafy Algae over Rubble, Acropora palmata-Octocorals, Seagrass Meadow and Encrusting Algae-Encrusting Sponge-Octocoral, and Coral Mixture. Specimens collected or photographed by several expedition members were also identified and included. In the case of Serranilla, seven species were recorded by video cameras during the project “Elasmobranch diversity and abundance estimates using baited remote underwater video stations” developed by Colombia Azul Foundation, Universidad de los Andes, and Florida International University. Scientific names of species follow the Catalog of Fishes (Eschmeyer et al., 2018) and the classification follows Eschmeyer et al. (2018) for cartilaginous fishes and Betancur-R. et al. (2017) for bony fishes.

2.3 Description of the dataset
The dataset presented here comprises a depurated inventory of the fish species reported from Roncador, Serrana, and Serranilla (the three of them already visited by the recent CCO expeditions), as well as from Quitasueño, the largest and westernmost island, which has not been yet visited by the CCO expeditions. The dataset includes all the fish species observed during the expeditions carried out between 2015 and 2017 (Table 1) plus the reports previously published in Bolaños-Cubillos et al. (2015), Polanco F. (2015), and Robertson & Van Tassell (2015). The six fields included per species within this dataset are listed and described in detail below.
Taxon ID and Scientific Name ID: This field includes a unique and stable-through-time alphanumeric identifier (taxonomic identifier) provided by Life Science Identifier (LSID), recovered from World Register of Marine Species (WoRMS) (AphiaID).
Basis of record: As the data set includes records based on human observations, machine observations (Baited Remote Underwater Video Stations - BRUVs) or preserved specimens this field contains this specific information for each species.
Bibliographic Citation: This field includes the reference that explicitly reports the species on the northern islands of the Seaflower Biosphere Reserve.
Reference: URLs associated to georeferenced occurrences of the species found in the dataset.
Locality: Specific localities where the species have been recorded in the northern islands are presented in this field. Four localities were defined considering the islands Quitasueño, Roncador, Serrana, Serranilla and a locality named North for species found on the northern area among the banks.
Locality ID: The Marine Regions Geographic Identifier (MRGID) provided by for each island and the MRGID for the Seaflower Marine Protected Area for the locality named “North”.

2.4 Outcomes and discussion
A total of 411 species are recorded here for our study area, that is the northern islands of the reserve (i.e. Roncador, Serrana, and Serranilla) and the westernmost island Quitasueño. Considering that a total of 1694 fish species (including shelf and slope fishes) are reported for the Greater Caribbean region (Robertson & Van Tassell, 2015), our study area harbors 24% (i.e. close to one fourth) of the region’s fish species richness. Fifty four percent of the species reported here (i.e. 220) were inventoried by the authors (Table 1) during expeditions to Roncador in 2015 (n = 140), Serrana in 2016 (n = 155), and Serranilla in 2017 (n = 166). With 1577 fish species reportedly native to and resident in the shallow waters (< 100 m) of the Greater Caribbean (Robertson & Van Tassell 2015), our findings demonstrated that just three of the smallest islands of the reserve encompass a remarkable proportion (i.e. 14%) of Greater Caribbean marine fish species richness. This high diversity is concentrated in an area less than 5% of Greater Caribbean extension. Interestingly, only 42% species (n = 92) were common to the three islands. When clustering sites based on fish community structure using the Jaccard index of similarity, relatively low values are observed between pairs of islands indicating that each island harbors relatively distinct fish communities. The fish faunas of Roncador and Serrana, for instance, are 62% similar, and those of Roncador and Serranilla are alike only by 52%. This result emphasizes the urgent need to protect the valuable and unique fish assemblages of these and other small islands and banks comprising the archipelago.

Another point worth remarking is the consistent absence (or at least rarity) of several large-bodied, commercially valuable species throughout the reserve threatened by overfishing (Chasqui et al., 2017). Most striking is the absence of the Nassau grouper, Epinephelus striatus, one of the most typical large epinephelines of Caribbean coral reefs (Bent-Hooker 2012). High levels of overfishing are also apparent for large-bodied parrotfishes. The rarity of the blue parrotfish Scarus coeruleus, and the absence of the rainbow parrotfish S. guacamaia, suggest that these have been likely extirpated from the islands for several decades (Acero and Polanco, 2017). Serranilla has particularly depleted grouper populations. The yellowmouth grouper Mycteroperca interstitialis, the tiger grouper M. tigris, and the yellowfin grouper M. venenosa, for instance, have never been observed by any contemporary researcher in that island. Other relatively valuable fishes such as the greater amberjack Seriola dumerili, the permit Trachinotus falcatus, and the jolthead porgy Calamus bajonado are also commercially extinct or very close to extinct throughout the reserve.

The reserve is, however, a natural laboratory where several actively speciating groups show high species richness. About two thirds of the 18 recognized species of Hypoplectrus, a genus of small hermaphroditic serranids endemic to the Greater Caribbean, occur in the reserve with at least nine of them on the northern islands. Elacatinus, a genus of cleaning and sponge dwelling gobies also endemic to the western tropical Atlantic, includes 35% of its 20 recognized species on the reserve reefs, five of them in them occurring on the northern islands. Those genera, as well as several others, must be studied in detail to help understand Caribbean connectivity patterns and develop suitable management strategies.

Lastly, 9 % (n = 19) of the species detected during the CCO Colombian expeditions are new reports for the reserve or at least to its northern part. These species are distributed in 15 families, namely Carcharhinidae (Rhizoprionodon terraenovae), Dasyatidae (Hypanus sabinus), Gobiidae (Cryptopsilotris batrachodes), Fistulariidae (Fistularia tabacaria), Chaenopsidae (Acanthemblemaria aspera, A. maria, A. spinosa, Emblemariopsis sp.), Labrisomidae (Stathmonotus gymnodermis), Gerreidae (Eucinostomus lefroyi), Priacanthidae (Priacanthus arenatus), Labridae (Doratonotus megalepis), Antennariidae (Antennarius pauciradiatus, Histrio histrio), Diodontidae (Chilomycterus antillarum), Monacanthidae (Monacanthus ciliatus, Stephanolepis setifer), Kyphosidae (Kyphosus cinerascens), and Serranidae (Serranus tortugarum). Obtaining such high percentage of new reports through a relatively limited sampling effort indicates that if scientific fish ichthyocides were used the biodiversity of this unique Caribbean region will be more thoroughly evaluated and perhaps currently reported levels would most likely increase.
3. Data Availability Statement
The dataset “Fish biodiversity in three northern islands of the Seaflower Biosphere Reserve (Colombian Caribbean)”, which includes the most recently updated list of species in the northern area of the reserve, was assembled using the Darwin Core standard (DwC) and is available through the Integrated Publishing Tool of the Ocean Biogeographic Imation System (OBIS) and the Global Biodiversity Information Facility (GBIF) Colombian nodes (SIBM - SIB Colombia) ( Future updates of this list will be published in the latter repository. Changes incorporated to each new version of the list will be summarized in the respective metadata section of the electronic resource.

4. Conflict of Interest
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.

5. Author Contributions
All the authors contributed to this study. AAP, JJT, APF, NBC: Built the database; AAP, APF, JJT: Contributed to the writing and correction of the manuscript; APF, AAP: Devised the data set. All the four authors reviewed the final version of the manuscript and contributed to the discussion.
6. Funding
This research was supported by Universidad Nacional de Colombia, Universidad del Valle, INVEMAR, Coralina, and CCO through Colombia BIO – Colciencias project, agreement No. 341 of 2017 with the aim of joining efforts to characterize the biodiversity in areas of scientific interest with poor biological information in order to strengthen the scientific collections and the generation of genetic information of Colombian biodiversity. Projects involved: “Biodiversidad íctica de la Isla Cayo Serrana durante la Expedición Seaflower 2016” – Seaflower Expedition 2016, Universidad Nacional de Colombia, Universidad dela Valle, Coralina; “Biodiversidad íctica de la Isla Cayo Serranilla durante la Expedición Seaflower 2017” – Seaflower Expedition 2017, Universidad Nacional de Colombia, Universidad dela Vallle, INVEMAR, Coralina; “Evaluación física y biológica de las unidades ecológicas someras en la isla Cayo Serranilla de la Reserva de Biósfera – Seaflower” – Seaflower Expedition 2017, INVEMAR, Coralina.

Keywords: Inventory, New records, Fish species, Actinopterygii, Chondrichthyes, Roncador, Serrana, Serranilla

Received: 21 Sep 2018; Accepted: 25 Feb 2019.

Edited by:

Sonia Bejarano, Leibniz Centre for Tropical Marine Research (LG), Germany

Reviewed by:

Hudson T. Pinheiro, California Academy of Sciences, United States
Badi R. Samaniego, University of the Philippines Los Baños, Philippines
Andres López-Perez, Universidad Autónoma Metropolitana, Mexico  

Copyright: © 2019 Acero P., Tavera, Polanco F. and Bolaños-Cubillos. 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) and the copyright owner(s) 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.

* Correspondence: Dr. Arturo Acero P., Universidad Nacional de Colombia, Bogotá, Colombia,