An updated reef fish checklist of the southernmost Caribbean reef system, with comments on the lionfish invasion

Introduction

The continental coast of the southernmost portion of the Caribbean Sea, called Urabá Gulf, harbours particular ecological and geological features that differ markedly from other widely explored areas of the Caribbean (O´Dea, 2012). About 3.5 Myr ago, the area functioned as a deep ocean corridor connecting the fauna of the eastern Pacific and Caribbean Sea. After the closure of the Isthmus of Panama, two ecologically divergent areas were formed, with the Pacific side characterized by ocean-based environments and the Caribbean side dominated by coral reef ecosystems (Glynn, 1982).

This southernmost portion of the Caribbean Sea belongs to the Chocó-Darién biogeographic realm. It is regarded as a hotspot of global biodiversity, with high biological relevance for the Colombian Caribbean (Myers et al., 2000). The region encompasses large remnants of humid forest and a mosaic of coastal habitats, including riverine, estuarine and reef ecosystems (Díaz et al., 2000). Although the coastline is strongly influenced by large discharge of terrigenous sediment and freshwater from the Atrato River (Chevillot et al., 1993), fringing patch reefs flourish in such harsh conditions with a typical reef fish fauna and the largest living coral cover across the region (Díaz et al., 2000).

Despite its importance, the Chocó-Darién reef system remains poorly studied (but see Acero & Garzón, 1987a; Reyes-Nivia et al., 2004), with a limited knowledge on its ichthyofauna when compared to other areas of the Colombian Caribbean, such as the San Andrés and Providencia archipelago (Victoria & Gómez, 1984; Mejía & Garzón-Ferreira, 2000), Santa Marta (Acero & Garzón, 1987b; Acero & Rivera, 1992; Grijalba-Bendeck et al., 2004) and Islas del Rosario archipelago (Acero & Garzón, 1985; Delgadillo-Garzón & Zapata-Ramírez, 2009). Like other areas of the Colombian Caribbean, the Chocó-Darién reef has shown clear signs of degradation, evidenced by the dominance of macroalgae, pollution, unregulated tourism and, more recently, the occurrence of one of the invasive species of lionfish Pterois volitans (Betancur-R. et al., 2011; Gómez-López et al., 2018).

Lionfishes (P. miles and P. volitans) were the first non-native marine species to be established in the north-western North Atlantic to the Caribbean and Campeche Bank (Schofield, 2009). These species are considered voracious predators coupled with a high reproductive output (Côté et al., 2013). Hence, declines of native fish populations in reef systems have been correlated with the increment of their abundances (Green et al., 2012). Lionfishes have sharply dispersed across the Caribbean coral reefs after the first record at the Providencia Island, Colombia in 2008 (Betancur-R. et al., 2011). Over the last years, P. volitans has increasingly been reported at the Chocó-Darién reefs (Galvis & Galvis, 2016; García & Rueda 2018; Rojas-Vélez et al., 2019), which raises concern about the potential ecological outcomes in the near future.

This study provides an updated checklist of reef fish of the Chocó-Darién region, based on compiled data of visual censuses and literature, with notes on conservation status and species distribution. In addition, the current status on lionfish (P. volitans) invasion is discussed here. This compilation lays foundation for supporting ongoing and future studies for conservation of reef fishes and management of marine resources and services of the region.

Material and methods

Study area. The study region is located in the western tip of the coast of the Urabá Gulf, Colombia, the southernmost portion of the Caribbean Sea. This area includes three sampling localities: Capurganá Bay (8°38’13.45”N; 77°20’39.29”W), El Aguacate (8°37’5.86”N; 77°19’28.53”W) and Sapzurro (8°39’37.02”N; 77°21’40.37”W) (Figure 1).

Figure 1: Western Caribbean coast of Colombia where the samplings of reef fish were carried out.

The waters of the Urabá Gulf are affected by an overload of freshwater and sediments from the Atrato River, which plays a critical role for local biogeography (Restrepo & Kjerfve, 2004). The Chocó-Darién reef system is characterized by a mosaic of fringing reefs, mainly composed by large colonies of Siderastrea siderea (Figure 2a) and a less extensive coral cover of Porites porites, Pseudodiploria strigosa, Agaricia agaricites, Agaricia tenuifolia and Millepora complanata (Gómez-López et al., 2018).

Figure 2: A small representation of the reef fish diversity recorded for the Chocó-Darién reef system, Colombia. A, Sparisoma viride, Thalassoma bifasciatum and Cephalopholis cruentata over a colony of Siderastrea siderea coral at El Aguacate; B, P. volitans at the Capurganá bay, ca. 7 m depth; C, Aetobatus narinari at the Capurganá bay.

Checklist compilation. The checklist was compiled from three sources: visual censuses in field expeditions, literature survey of peer-reviewed articles, and unpublished data (dissertations/theses).

Six visual censuses were performed, using roving diving technique (snorkeling) to quantify reef fish species richness in the Capurganá coastal reefs on April 2011 (Hill & Wilkinson, 2004). Three fringing coastal reefs were chosen, based on a previous survey and information on reef spatial arrangement (Díaz et al., 2000).

In the sampling sites, two divers freely swam for 30 minutes, identifying the fishes and, when possible, recording images and videos. The distance from the observer to the fish was a maximum of three meters, depending on the transparency, to avoid possible taxonomic errors. New records were only considered when two divers recorded the same species, or when a high-resolution image was available. Identifications of species in photos and videos were confirmed by comparisons with those provided by Reef Fish Identification Guide (Humann & Deloach, 2003).

The list of bony fishes was organized based on Eschmeyer’s Catalog of Fishes (Van der Laan et al., 2021), except for Labridae, in which Scarinae was included (Westneat & Alfaro, 2005), whereas Weigmann (2016) was followed for elasmobranchs. Genera and species are listed in alphabetical order. For each species included in the list, we confirm the geographic distribution based on Fishbase (Froese & Pauly, 2019). We also included the conservation status according to the Colombian National Red Book of marine fishes (Chasqui et al., 2017).

Results

Species list. A total of 212 reef fish species were compiled (Table 1), with 68 species recorded by the visual census. Eight out of the 212 species (3.7 %) had no previous published records: Coryphopterus dicrus, Dactylopterus volitans, Diodon holocanthus, Epinephelus adscensionis, Epinephelus guttatus, Ginglymostoma cirratum, Hypanus americanus, and Trachinotus falcatus. The latter species is a new record for the area and was sighted in our visual censuses. Additionally, we report a species of the Mugil curema complex (Nirchio et al., 2017) (Table 1).

Chocó-Darién reef fishes are distributed in 21 orders and 57 families, the most representative orders being Perciformes plus Perciformes incertae sedis (43.86 %), followed by Gobiiformes (8.49%), Blenniiformes (8.49 %), and Tetraodontiformes (8.02 %). The most speciose families were Labridae (9.91 %), followed by Gobiidae (8.49 %), Serranidae (8.02 %), Haemulidae and Pomacentridae (5.66 %). Likewise, the most speciose genera were Haemulon (n = 9), followed by Halichoeres and Lutjanus (n = 7), Sparisoma, Stegastes and Coryphopterus (n = 6).

From the recorded fishes, 96 are widespread species of the Western Atlantic, 50 of the Greater Caribbean, 33 Trans-Atlantic, seven Circumtropical, four Transatlantic and Mediterranean, two Circumglobal and one restricted to the Pacific Ocean (Figure 3). The latter species is the introduced lionfish P. volitans (Figure 2b).

Figure 3: Relative frequency of the geographic range categories of reef fish recorded for the Chocó-Darién reef system, Colombia. CG, circumglobal; CT, circum-tropical; PAC, Pacific; TA, Transatlantic (Western Atlantic and Eastern Atlantic); TA+MED, Transatlantic and Mediterranean; WA, Western Atlantic; WCA, Western Central Atlantic (Caribbean); WI, Western Atlantic and Oceanic islands.

Of the 212 species, one is listed as Data Deficient (DD), one species as Least Concern (LC), seven as Near-threatened (NT), seven as Vulnerable (VU), two as Endangered (EN) and one as Critically Endangered (CR). A total of 10 species are in a threat category for the Chocó-Darién coral reef, based in the National Red Book (Chasqui et al., 2017). The Nassau grouper (Epinephelus striatus) is Critically Endangered. In addition, the Queen Triggerfish Balistes vetula and the Midnight Parrotfish Scarus coelestinus are categorized as Endangered. However, most species (186) have not yet been evaluated in Colombia.

Discussion

This work represents an extensive compilation on the ichthyofauna diversity of the Chocó-Darién reef system, Colombian Caribbean. Previous studies have documented contrasting number of fish species, such as 146 (Acero & Garzón, 1987a) and 119 (Reyes-Nivia et al., 2004), which is possibly due to the use of different sampling methodologies.

The most speciose families recorded in this work (e.g., Labridae, Gobiidae, Serranidae, Haemulidae and Pomacentridae) are commonly found in the continental margins of the tropical Atlantic (Floeter, 2008). Nevertheless, the fish richness recorded for the study area (212 species) represents only 30 % of the total species accounted across the Caribbean region, indicating its relatively low richness. For example, Acero & Garzon (1987 b) recorded 372 species at the Santa Marta reef systems, Colombian Caribbean, and Starck (1968) recorded 389 species at the Alligator reef, Florida Keys.

Recently, a biogeographic analysis for fish data of both reef and soft bottom divided the Caribbean region into three major provinces: (1) a central, tropical province comprising the West Indies, Bermuda and Central America; (2) a southern, upwelling-affected province spanning the entire continental shelf of northern South America; and (3) a northern, subtropical province that includes all of the Gulf of Mexico, Florida and south-eastern USA (Robertson & Cramer, 2014). The Chocó-Darién reef system is located at the southern province covering the entire continental shelf of northern South America, holding the lowest number of fish species and percentage of local endemics (3.4 %). Likely, the particular environmental conditions of this region, such as the high loads of nutrients, low pH, temperature and salinity variations caused by the Atrato River (McLaughlin et al., 2003, Manzello, 2010) explain, in part, the low species richness of the region.

Most of the listed species present distributions across the Western Atlantic. Biogeographically, the Western Atlantic comprises the Greater Caribbean and Brazil, with their faunas considered until recently to be partially separated by the freshwater discharge from the Amazon and Orinoco river mouths (Floeter et al., 2008). However, an extensive and diverse reef system was recently mapped for the Amazon region (called Great Amazon Reef), which represents the northern limit of the Brazilian Province and may function as an ecological corridor connecting the fauna of the Brazil and Caribbean (Francini-Filho et al., 2018). Importantly, the Caribbean shelters a higher species richness (774 species) and endemism levels (57 %) compared to Brazil (Kulbicki et al., 2013, Pinheiro et al., 2018), which, in turn, explains the high percentage of Caribbean or Western Central Atlantic endemics species in our study (23 %).

The presence of the species Gnatholepis thompsoni and Pterois volitans in the Chocó Darién region is related to different events. G. thompsoni, native from the Indian Ocean, possibly dispersed to the north Atlantic during the last interglacial period, and its expansion range has been spreading in face of climate change (Rocha et al., 2005). On the other side, P. volitans was introduced in the Florida Keys coastal waters in the 1980’s, as a consequence of escapes of the aquarium trade (Morris et al., 2009). Its range has increased over the years, reaching a broad extension of the tropical and subtropical Western Atlantic and Caribbean (Schofield, 2009; Betancur-R et al., 2011). In Colombia, this lionfish was firstly reported in the oceanic islands, and subsequently in the coastal areas of the Caribbean (Betancur-R. et al., 2011). Our study raises concerns of the species´ invasion at the Chocó-Darién reef system (Galvis & Galvis, 2016; Rojas-Vélez et al., 2019), and supports the previous reports of the expansion of P. volitans toward southernmost portion of the Caribbean Sea. This species feeds on a wide variety of juveniles of large-bodied fish (Green & Côté, 2014), and crustaceans, as already reported for Colombian Caribbean regions (Muñoz-Escobar & Gil-Agudelo, 2012; Acero et al., 2019). Such feeding behavior may trigger impacts on local fish populations, and consequently, in the food web dynamics (Valdez-Moreno et al., 2012).

The present study contributes to fill up the knowledge gap on reef fish of the Chocó-Darién reef system. Further research including new technologies such as ROVs (Auster, 1997) and baited remote underwater video systems (BRUVs) (White et al., 2013) are recommended, which would enable exploring remote reef areas, such as mesophotic and rariphotic ecosystems (cf. Francini-Filho et al., 2019). Finally, in face of the fast invasion of the P. volitans and the high occurrence of threatened fishes, we recommend strengthening fish monitoring programs to subsidize management and conservation measures at the Chocó-Darién reef system.