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Universitas Scientiarum

Print version ISSN 0122-7483

Univ. Sci. vol.24 no.1 Bogotá Jan/Apr. 2019

https://doi.org/10.11144/javeriana.sc24-1.come 

Artículos

Checklist of marine elasmobranchs of Colombia

Lista de chequeo de elasmobranquios marinos de Colombia

Lista de verificação de elasmobrânquios da Colômbia

Paola A. Mejía-Falla1  2  * 

Andrés Felipe Navia1 

Juan Carlos Salcedo-Reyes

1Fundación colombiana para la investigación y conservación de tiburones y rayas, SQUALUS. Calle 10ª No. 72-35, Cali, Colombia.

2Wildlife Conservation Society. Avenida 5 Norte No. 22N-11, Cali, Colombia.


Abstract

A review and update to the shark and ray species recorded for the marine waters of Colombia was carried out. A total of 206 species had been recorded in the literature, of which 138 species (76 sharks and 62 rays) could be confirmed from museum records, catches, photographs, and videos. No evidence was found for 25 species, but their distribution included neighboring countries, and they were therefore classified as possible based on distribution. Thirty- six species were classified as improbable based on distribution and seven more were considered as misidentifications. The inventory of confirmed species includes 57 genera (30 shark and 27 batoid genera) and 34 families (18 shark and 16 batoid families). There was notably an addition of 26 confirmed species since 2007 as well as numerous modifications to group systematics and taxonomy, especially for batoids. The total number of confirmed elasmobranchs represented 12.1% of species known worldwide, and could even reach 14.5%, indicating that Colombia has one of the richest cartilaginous fish faunas in Latin America, behind Mexico and Brazil. This demonstrates that although Colombia cannot be considered an elasmobranch biodiversity hotspot or site of elasmobranch endemism globally, it does have good representativity of these species’ biodiversity at the regional level, especially regarding amphi-American species.

Keywords: Biodiversity; sharks and batoids; species list; richness

Resumen

Se llevó a cabo una revisión y actualización de los registros de especies de tiburones y rayas de aguas marinas colombianas. En la literatura se había registrado un total de 206 especies, de las cuales 138 (76 tiburones y 62 rayas) se habian podido confirmar con registros de museo, capturas, fotografías y videos. No se encontró evidencia de 25 especies, pero su distibución incluye países vecinos, por lo que fueron clasificadas como “posible basada en la distribución”. Treinta y seis especies se clasficaron como “improbable basada en la distribución” y siete más se consideraron identificaciones erróneas. El inventario de especies confirmadas incluye 57 géneros (30 tiburones y 27 géneros batoideos) y 34 familias (18 tiburones y 16 familias batoideas). De modo notable, hubo una adición de 26 especies confirmadas desde 2007, así como numerosas modificaciones de la sistemática y taxonomía del grupo, especialmente para batoideos. El número total de elasmobranquios confirmados representó el 12.1 % de las especies conocidas en el mundo, y podría aún alcanzar el 14.5 %, lo cual indica que Colombia tiene una de las faunas de peces cartilaginosos más ricas de Latinoamérica, después de México y Brasil. Esto demuestra que, aunque Colombia no puede ser considerada un punto caliente de biodiversidad de elasmobranquios o un sitio de endemismo de elasmobranquios a nivel global, sí tiene una buena representatividad de la biodiversidad de estas especies a nivel regional, especialmente respecto a especies anfi-americanas.

Palabras clave: biodiversidad; tiburones y batoideos; lista de especies; riqueza

Resumo

Realizou-se uma revisão e atualização dos registros de espécies de tubarões e arraias de água marinha colombianas. Na literatura se encontrava registro de um total de 206 espécies, das quais 138 (76 tubarões e 62 arraias) foram possíveis de confirmação por meio de registros de museus, capturas, fotografias e vídeos. Não se encontrou evidencia de 25 espécies, mas suas distribuições incluem países vizinhos, sendo então classificadas como “possível com base na distribuição”. Trinta e seis espécies se classificaram como “improváveis com base na distribuição” e outras sete se consideraram identificações errôneas. O inventário de espécies confirmadas inclui 57 gêneros (30 tubarões e 27 gêneros de batóides) e 34 famílias (18 tubarões e 16 famílias batóides). Notavelmente, houve uma adição de 26 espécies confirmadas desde 2007, assim como numerosas modificações da sistemática e taxonomia do grupo, especialmente para batóides. O número total de elasmobrânquios confirmados representou um 12.1 % das espécies conhecidas no mundo, e poderia ainda alcançar 14.5 %, o que indica que Colômbia tem uma das faunas mais rica da América Latina em peixes cartilaginosos, depois de México e Brasil. Isto mostra que Colômbia, ainda que possa não ser considerada um ponto de referência de biodiversidade de elasmobrânquios ou um local de endemismo de elasmobrânquios a nível global, possui uma boa representatividade da biodiversidade de estas espécies a nível regional, especialmente com respeito a espécies anfi-americanas.

Palavras-chave: biodiversidade; tubarões e batóides; lista de espécies; riqueza

Introduction

Recent studies on shark and ray zoogeography in Colombia considered that the number of recorded species was high compared with the extension of the Colombian coasts, representing almost 15 % of worldwide richness (Navia etal., 2016). Despite this high representativity, since the first mention of sharks in fish checklists of Colombia (Posada, 1909), few detailed studies have been carried out on the richness and distribution of these species in Colombia (García, 2017).

Numerous studies reporting first records of species or expansions of geographic range have been published in recent decades (e.g. Acero P & Franke, 1995; Caldas et al., 2004; Acero et al., 2007; Grijalba-Bendeck & Acevedo, 2009; Mejía-Falla & Navia, 2009; Anguila et al., 2016 a,b; Acero et al., 2018), however, detailed listings of this group are rather scarce. The first specific checklists of elasmobranchs in Colombia were carried out by Mercado (1990), who included 61 species, and Mantilla (1998), who included 127 species. The latter author also included freshwater stingrays. Mejía-Falla et al. (2007), based on these checklists, on bibliographic references, and on physical and visual evidence, found that of 176 recorded species, only 121 could be considered confirmed for marine and freshwater environments of Colombia. The last chondrichthyan identification guide of Colombia included a total of 124 marine and freshwater elasmobranch species (Mejía-Falla etal., 2011).

A subsequent listing (Álvarez-León et al., 2013) based only on bibliographic compilation, and therefore lacking the evidence supports of the occurrence of the species, reported a total of 204 species of sharks and batoids for Colombia. This value greatly overestimates the elasmobranch richness of the country and contributes to perpetuating errors in the Colombian chondrichthyan biodiversity by including species as the great white shark (Carcharodon carcharias), the common thresher shark (Alopias vulpinus), electric rays as Discopyge tschudii and Narcine brasiliensis, and even sawfishes such as Pristis microdon, among others.

Since the publications by Mejía-Falla et al. (2007, 2011), there have been significant additions, and taxonomic and systematic modifications to this group internationally(Nayloretal.,2012; Lastetal.,2016a; Weigmann,2016). In particular, there have been changes to the classification of batoids and of some amphi-American sharks into different families and genera, and even the “resurrection” of families and species (Castro, 2011; Carvalho etal., 2016 a,b; Last etal., 2016 b,c; White & Naylor, 2016; White & Last, 2016 a,b,c). There have also been increases to the richness (Acero-P et al., 2016) and to the distribution of sharks and rays in Colombia (Navia et al., 2016; García, 2017), leading to current listings being out of date in terms of their composition locally (Mejía-Falla et al., 2007, 2011) and globally (Last et al., 2016 a; Weigmann, 2016), even more so regarding their taxonomic classification and systematics.

The objective of the present study was to contribute to the update and consolidation of the marine cartilaginous fish checklist of Colombia, based on supporting evidence that would allow to confirm, q uestion, or reject the presence of each analyzed species. Along with the updated checklist, annotations to modify the original lists were included as well as comments for species that present taxonomic or systematics problems.

Materials and methods

Construction and homogenization of cartilaginous fish databases

Based on checklists by Mejía-Falla et al. (2007, 2011) a baseline list of marine elasmobranch species of Colombia was created, to which newly available records were added (e.g. Gámez-Barrera et al., 2012; Acero-P et al., 2016, 2018; Anguila et al., 2016 a,b; García, 2017). Considering that the sole mention of a species in a document did not guarantee the presence of that species in the study area, a confirmation process for the presence of each species recorded in the initial list was performed. For this verification, the following activities were carried out:

  1. A search of records of species in national and international ichthyological collections. Web pages were consulted, with an emphasis on spatial location data where each species was collected in order to validate its presence within the marine limits established for Colombian Pacific and Caribbean waters. For this study, it was assumed that a correct identification process had been undertaken for each of the recorded specimens in the ichthyological collections. However, when a species presented a record for Colombia but its natural distribution does not correspond to or close to Colombian waters, that record was considered a potential identification error.

  2. The following national collections were consulted: INV-PEC: Marine Natural History Museum of Colombia (INVEMAR, Santa Marta), ICN-MHN: Natural Science Institute, Natural History Museum (Bogotá), IAvH: Ichthyological Collection of the Alexander von Humboldt Institute (Tunja), CIUA: Fish collection of the Universidad de Antioquia (Medellín), CICH-CHbCH: Hydrobiological Collection of Chocó, Universidad Tecnológica del Chocó (Quibdó), PNNG: Reference Marine Biological Collection of the Biological Station “Henry von Prahl” of the Gorgona Natural National Park (Gorgona Island), UNSSA: Universidad Nacional de Colombia in San Andrés (San Andrés). All the collections consulted, except UNSSA, are included in the National Registry of Biological Collections. Although the reference collection of the Universidad del Valle (CIRUV) was taken into account for a previous checklist (Mejía-Falla et al. 2007), it could not be included in the present study by the curator’s request, as a revision of all specimens was underway. However, this did not affect the results of the present study, as all species previously confirmed in that collection were also reported by other museums, or there were records of capture or sightings.

The International collections reviewed were: AMNH: American Museum of Natural History (Washington), CAS: California Academy of Sciences (San Francisco), GCRL: Gulf Center Research Laboratory (Ocean Springs), FLMNH: Florida Museum of Natural History (Gainesville), NRM: Swedish Museum of Natural History (Sweden), USNM: Smithsonian National Museum of Natural History (Washington), SIO: Scripps Institution of Oceanography (San Diego, California), MNHN: Muséum National D’Histoire Naturelle (Paris), MCZ: Museum of Comparative Zoology, Harvard University (Cambridge), TCWC: Texas A&M University, Cooperative Wildlife Collection (Texas), CMNFI: Canadian Museum of Nature Fish Collection, FMNH: Field Museum of Natural History (Zoology) Fish Collection (Chicago), SAIAB: The South African Institute for Aquatic Biodiversity (South Africa), AfroBIS: Iziko South African Museum, Shark Collection (South Africa).

Identification catalogues that included geolocation information in the species records (Robertson & Allen 2015, Robertson etal., 2015) were also consulted, as well as the Global Biodiversity Information Facility (GBIF) and the Information System on Marine Biodiversity of Colombia (SIBM).

A search ofcapture records andinsitu observations ofindividuals for different locations in Colombian Pacific and Caribbean waters. For these records several different information sources were consulted:

  1. Documents related to checklists, updates or new records offish species for Colombian Pacific and Caribbean waters or for particular areas within them, based on captures and/or visual observations, and for which there were descriptions and photographs that could validate the identification of the mentioned species.

  2. Documents related to biological, ecological, and genetic studies of fish species within Colombian Pacific and Caribbean waters that included the diagnostic characteristics of the studied species and would therefore validate the presence of the species in the area.

  3. Photographic catalog of the Squalus Foundation, created from different projects carried out in Colombian Pacific and Caribbean waters, which allowed to validate the identity of the species and to record locations of capture or observation.

Reports of catches and visual observations were obtained from institutions such as the Squalus Foundation (SF), Malpelo Foundation (MF), EAT-Fishing consulting (EAT), Universidad del Valle (UV), and Marine and Coastal Research Institute, INVEMAR (INV). Geolocated records that appeared in “Shorefishes of the Tropical Eastern Pacific: online information system” (Record TEP) and “Shorefishes of the Greater Caribbean: online information system” (Record SGC) were also included, as well as records in published documents that included photographs of the specimens and allowed to validate their identity. Based on evidence found (museums, catches, visual observations, or literature records), the species cited in the present study were grouped into three large categories: 1. Confirmed species: species that appeared in A) national and/or international museum records, or B) records of fisheries catches (catch) or in situ observations (visual record). 2. Unconfirmed species, possible based on distribution: Species that had been mentioned in different scientific documents, for which there was no physical evidence in any collection or geolocated visual confirmation. However, the known species distribution included the marine waters of neighboring countries, and therefore its presence in Colombian Pacific or Caribbean waters could not be rejected. 3. Unconfirmed species, improbable based on distribution: Species that, despite being included in marine fish checklists of Colombia or in regional identification guides, had distribution areas that did not encompass the study area, or even belonged to distant areas (e.g. Atlantic Ocean, Indo-Pacific, Indian Ocean, Mediterranean), to antitropical areas, or waters colder than those of the Eastern Pacific and Western Atlantic, which meant that their presence in Colombian Pacific or Caribbean waters would be improbable. The appearance of these species could have resulted from incorrect identifications or from being inadequately included based on previous checklists that did not verify sources. For unconfirmed species, two types of evidence were considered: C: regional or worldwide identification guides, and D: national references.

Since the taxonomy and systematics of this group has changed significantly over the past five years, it was necessary to update several orders, families, genera, and species. To do this were used as reference documents by Naylor et al. (2012), Carvalho et al. (2016 a,b), Last et al. (2016 a,b,c); White & Naylor (2016), White & Last (2016 a,b,c), and Weigmann (2016). This process allowed to present an updated checklist in terms of species nomenclature, and to avoid the duplication of species that could correspond to synonymies.

Results

A total of 138 marine elasmobranchs were confirmed in this study, 76 sharks and 62 rays (Table 1), adding 26 species to the checklist by Mejía-Falla et al. (2007). This number of confirmed species for Colombia represents 12.1 % of the world’s total, as well as 30.5 % of genera, 58.6 % of families, and 80.0 % of orders (Fig. 1). A total of 90 species (57 sharks and 33 rays) were confirmed for the Colombian Caribbean and 67 species (36 sharks and 31 rays; Table 1) were confirmed for the Colombian Pacific. Consequently, the representation percentage of genera and families was greater for the Caribbean than for the Pacific, whereas there were 11 orders found in each region (Fig. 1).

Table 1 Species of confirmed elasmobranchs for the Colombian Pacific (P) and Caribbean ©, with their corresponding category (A: recorded in national and/or international museums; B: recorded in fisheries [catch] or in situ observations [visual record]) and type of support (see methods for details). Species added with respect to Mejía-Falla et al. (2007) are shaded in light blue, and species that presented modification in their systematics or taxonomy are shaded in light green. (*) specimens are presented in the indicated collection but have not yet been assigned a catalog number. (**) specimens correspond toholotypes. 

Figure 1 Numerical representation of the richness of orders, families, genera and species of elasmobranchs from Colombian Caribbean and Pacific, compared to the worldwide richness according to Weigmann (2016)

Twenty-five species (13 sharks and 12 batoids) could not be confirmed but were considered possible according to available records and the known distribution of the species (Table 2), whereas 36 species (15 sharks and 21 batoids) were catalogued as improbable due to their known distribution (Table 3). Although seven species presented collection records in locations within Colombia’s Economic Exclusive Zone, there was only one record for each, or they were far from the known distribution of those species; they were therefore assumed to be incorrect identifications (Table 4).

Table 2 List of elasmobranch species not confirmed, but possible by distribution for the Colombian Pacific (P) or Caribbean ©. The type (C, D) and reference of support are indicated (see methods for details). Species with modifications in their systematics or taxonomy are shaded in light green. 

Table 3 List of elasmobranch species cited in scientific documents but without physical or visual support, and considered unlikely for the Colombian Pacific (P) or Caribbean ©, given its known distribution. The type (C, D) and the reference of support are indicated. Species that presented modification in their systematics or taxonomy are shaded in light green. 

Table 4 Species that although it has museum number, visual o catch record in Colombian waters, they are considered a bad identification. 

This review allowed to update the taxonomy and systematics of the group. Modifications to the scientific name of two sharks and 20 rays and skates were identified, as well as changes to some batoid orders, families and genera with exclusive distribution in the American continent (Last et al., 2016 b,c). The most significant results for sharks were: 1) the division of Ginglymostoma cirratum into separate species, with G. cirratum for the Atlantic and Caribbean, whereas Pacific populations received the name Ginglymostoma unami. 2) The separation of Carcharhinus porosus as a species exclusively for the Caribbean and the resurrection of C. cerdale as the valid species for the Pacific. 3) The description of a new angel shark species (Squatina david ) based on specimens from the Colombian Caribbean (holotype), and consequently, according to Vaz & Carvalho (2018), this species replaces S. dumeril; so that the specimens previously identified as S. dumeril possibly correspond to S. david. 4) The first record of the sleeper shark (Somniosus sp.) for deep waters of the southern Caribbean of Colombia; although it was not possible to confirm the species, the authors (Acero-P et al., 2018) remarked that it is highly possible that the specimen could be the Greenland shark, S. microcephalus (Bloch & Schneider, 1801).

The batoid group presented the greatest quantity of modifications over the past few years, such as: Changes to the genus of the species Torpedo nobiliana and Torpedo tremens that are now valid as Tetronarce nobiliana and Tetronarce tremens (Carvalho et al., 2016a). The union of the old orders Rhinobatiformes and Pristiformes into Rhinopristiformes, as well as the modification of the genus Rhinobatos into the genus Pseudobatos for guitarfish from the American continent (Last et al., 2016b). Within this same order, species from the genus Zapteryx were taken out of the Rhinobatidae Family and assigned to the Trygonorrhinidae Family (Last & Séret, 2016).

Within the Rajidae Family, the genus Raja was modified for neotropical species, and is now recognized as Rostroraja (Last et al., 2016c). The species name Anacanthobatis americanus was changed to Schroederobatis americana (Last etal., 2016c; Séret etal., 2016). Within the Dasyatidae Family, the genus name Dasyatis was changed to Hypanus, valid only for the rays of this family on the American continent (Last et al., 2016d).

The species Manta birostris was moved into the genus Mobula (White et al., 2018), whereas the Aetobatus narinari family name was changed; the family name Aetobatidae was revived, and the species was separated into different species for the Pacific (Aetobatus laticeps) and Atlantic (Aetobatus narinari) (Last etal., 2016). Another significant change occurred for the species Himantura pacifica and H. schmardae, which were moved from the family Dasyatidae into the family Potamotrygonidae, and were also assigned a new genus and are now recognized as Styracura pacifica and Styracura schmardae (Carvalho et al., 2016b). Finally, Urotrygon asterias, U. caudispinosus and U. serrula are now synonymous with U. munda (Weigmann, 2016).

Conclusions

The 138 elasmobranch species confirmed for Colombia represented 12.1 % of the known worldwide elasmobranch richness (Weigmann, 2016); this means that Colombia is the third country in terms of elasmobranch diversity in Latin America, behind Mexico (214, del Moral-Flores etal., 2015) and Brazil (165, Rosa & Gadig, 2014), and before Argentina (105, PAN-Tiburones, 2009) and Chile (92, Lamilla & Bustamante, 2005). There were also 25 potential species records that were not confirmed for Colombia, which could increase richness to 163 species, representing 15.10 % of worldwide elasmobranch species richness.

Compared with neighboring and/or bordering countries, Colombia has more shark and ray species than Venezuela (74, Cervigón, 1999; Robertson et al., 2015), Ecuador (94, Martínez-Ortiz & García-Domingo, 2013), and Peru (115, Cornejo et al., 2015). However, it should be noted that the published checklists of Venezuela and Ecuador have not been updated.

Comparing basins, the 90 Caribbean elasmobranch species represented 86.5 % of the species reported for the Greater Caribbean coastal zone (Robertson etal., 2015) and 42.2 % of the species reported for the North West Atlantic (Weigmann, 2016), whereas representativeness was lower for the Pacific basin, with 58.2 % of the species reported by Robertson & Allen (2015) for the Tropical Eastern Pacific and 43.8 % of the species to the North Eastern Pacific (Weigmann, 2016). Shark and batoid richness for the Colombian Caribbean was greater than that of Venezuela and Panama (Robertson et al., 2015), whereas shark and batoid richness for the Pacific was lower than that reported by Martínez-Ortiz & García-Domingo (2013) for Ecuador (61 shark species and 43 batoid species), by Cornejo et al. (2015) for Peru (66 shark species and 43 batoids species) and by Espinoza etal. (2018) for Costa Rica (81 elasmobranch species). However, it should be noted that Peru and Ecuador are strongly influenced by fauna from temperate waters of the southern Pacific, which increases significantly their diversity, as they provide species from different biogeographic provinces. Elasmobranch richness for the tropical zone of the Pacific basin of Colombia was greater than that of Panama in both coasts and greater than those of Costa Rica in the Caribbean Sea (Robertson & Allen, 2015; Espinoza etal., 2018).

Despite the great species richness found in a regional context, Colombia was far below shark biodiversity hotspots, which have been identified in southeastern Japan, Taiwan, and Australia, with nearly 85 species per 1ox 1ocell. The elasmobranch endemism level was also very low in Colombian waters in comparison with endemism hotspots identified by Lucifora et al. (2011), which were also located in southern Japan, Taiwan, Australia, as well as southern Brazil and the southeastern United States.

Shark richness values for the Caribbean and Pacific of Colombia agreed to bimodal distribution patterns described by Lucifora et al. (2011), who suggested a greater number of species towards intermediate latitudes of the northern and southern hemispheres than towards the tropics. However, these authors reported species numbers below those found in this study for Colombian Caribbean and Pacific waters. This could be due to the low number of studies on richness carried out in Colombia that are available in scientific journals with large circulation, as most publications have been published in Spanish, resulting in information available at the national level not being visible to researchers from other countries.

This demonstrates that although Colombia cannot be considered an elasmobranch diversity or endemism hotspot globally, there is great biodiversity representation of these species regionally, especially of amphi-American species. This is particularly important as several areas with moderate shark richness have shown high functional richness, suggesting that these species play unique roles, that they are not very redundant and are therefore very important for maintaining the structure and function of marine ecosystems. In this regard, the Pacific and Caribbean coasts of Colombia are one of the 15 hotspots of irreplaceability of endemic threatened marine chondrichthyans identified by Dulvy et al. (2014). These authors identified these hotspots to guide conservation priorities given that they contain the most unique chondrichthyan biodiversity.

Therefore, detailed knowledge of the richness and distribution of sharks and rays is an important tool for planning diversity management and conservation measures, especially in this type of group that includes an important number of highly migratory species. Finally, if the 11 species of freshwater stingrays confirmed for Colombia (Lasso et al., 2016; Do Nascimiento et al., 2017) are added to marine elasmobranch species, total richness would be 174 species, representing 15.3% of worldwide richness, a value that confirms the importance of Colombia for the diversity of this taxonomic group.

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Andrés Felipe Navia His main research interest is directed to the evaluation of the ecological function of top predators in marine ecosystems and the effect of fishing on food webs. He has conducted research about determination of the relationship between life history characteristics of elasmobranchs and their vulnerability. He recently initiated studies on the essential habitats of elasmobranchs and ecological processes that determine their richness and distribution. orcid: https://orcid.org/0000-0002-6758-7729

Paola Andrea Mejía-Falla Her research focused on the life history strategies and demographics of elasmobranchs, as well as to assess the effect of fishing on such population parameters. She has conducted research on reproduction, age and growth of various species of elasmobranchs, both marine and freshwater. She has initiated studies on essential habitats of elasmobranches and on the macro-ecological processes that determine the distribution of these species. orcid: https://orcid.org/0000-0003-2220-6969

Funding: N.A.

Electronic supplementary material: N.A.

Como citar este artículo Mejía-Falla PA, Navia AF. Checklist of marine elasmobranchs of Colombia, Universitas Scientiarum, 24 (1): 241-276, 2019. doi: 10.11144/Javeriana.SC24-1.come

Conflict of interest The authors declare having no conflict of interest

Received: June 28, 2018; Accepted: September 24, 2018

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