INTRODUCTION

Copepods are a widely distributed group of small crustaceans, present in almost all aquatic environments. They reach very high abundances and, together with nematodes, are considered the most abundant metazoan group on Earth (^{Boxshall and Halsey, 2004}). In the sea, copepods constitute between 60 and 80 % of the zooplankton biomass (Morales and Suárez-Morales, 2009), also reaching enormous abundances in benthic habitats. Their density varies between 100.000 and 1.000.000 harpacticoid copepods per square meter in intertidal sediments. Such densities decrease with depth, reaching 10.000 individuals per square meter in the deep sea (Boxshall and Halsey, 2004). Symbiotic and parasitic forms of copepods also number more than 1.500 species: they are also very diverse and have been found in almost all major metazoan phylums (^{Huys and Boxshall, 1991}). Currently, the subclass Copepoda includes more than 11.300 accepted species, and this number is permanently growing. In the last decade more than 1.000 species were described (^{Walter and Boxshall, 2018}). Copepods play an important role in the pelagic food chain as consumers of phytoplankton (^{Paffenhöfer, 1971}; ^{Mayzaud et al., 2002}; ^{Franco-Herrera, 2006}), and as main prey for others zooplankton, including the larvae of important commercial fish species (Brown and Marcotte, 1987; ^{Uye and Yamaoka, 1990}) and whales (^{Hardy, 1970}).

In Colombia, the first species of copepods recorded at the Caribbean were those reported by ^{Park (1970)} in the ecoregions Colombian Oceanic and San Andrés and Providencia Archipelago. Some years later, ^{Gómez (1975)} recorded planktonic copepods in Cartagena Bay. ^{Monsalve (1976)} published first records from the Pacific and ^{Renteria (1977)} new records from the Caribbean. Michel and Foyo (1977), in a faunal survey of the zooplankton of the Caribbean Sea, included copepod records of the Colombian Oceanic ecoregion. During their ecology studies, some authors mentioned copepod species from the neritic zone (^{Bernal, 1994}, 2000; Bernal and Zea, 2000). Additional records of planktonic copepods from San Andrés and Providencia (^{Giraldo and Villalobos, 1983}), Santa Marta region (^{Campos and Plata, 1990}), Providencia and Santa Catalina (^{Martínez-Barragán et al., 2009}) appeared subsequently. Among publications related to non-native species and the effects of marine traffic on the composition of zooplankton, several species of copepods were recorded (^{Rendón et al., 2003}; ^{Ahrens et al., 2011}). A study on copepod feeding focussing on the species Eucalanus subtenuis in the Colombian Caribbean was contributed by ^{Franco-Herrera (2006)}. Recently, articles on distribution of epipelagic copepods from the Colombian Pacific were published (^{López and Mojica, 2015}; Jérez-Guerrero et al., 2017).

Several undergraduate theses on zooplankton include copepod records (^{Samper, 1970}; ^{Alvarado, 1978}; ^{López and Mesa, 1983}; ^{Lozano, 1986}; ^{Marino and Merchán, 1993}; ^{Fisco, 2006}; ^{Uribe and Calero, 2006}; ^{Barón, 2007}; ^{Dorado-Roncancio, 2015}). Unfortunately, those documents were not formally published and species identifications were probably not confirmed by taxonomists. For instance, the report of Eucalanus finmarchicus in Santa Marta region (Samper, 1970) or of Microsetella norvegica in Cispatá Bay (Fisco, 2006) strongly point toward misidentifications. The existing information on Colombian Caribbean copepod diversity known until 2008, containing mainly planktonic species, was published by ^{Medellín-Mora and Navas (2010)}.

Over the last decade, copepods inhabiting phytal habitats of Gaira Bay have been intensively studied (^{Fuentes-Reinés and Suárez-Morales, 2017c}; Fuentes-Reinés et al., 2017; ^{Gómez and Fuentes-Reinés, 2017a}, 2017b; Suárez-Morales and Fuentes-Reinés, 2018), culminating in the description of seven new species and the addition of two species to the Caribbean species inventory. Moreover, planktonic species of Kelleria, Lubbockia, Farranula, and Oncaea (Fuentes-Reinés and Suárez-Morales, 2017b) and one species of Neocyclops (Fuentes-Reines and Suárez-Morales, 2017a) have been recorded. The discovery of the first Monstrilloid copepod found in Colombia (^{Dorado-Roncancio E.F. and J. Dorado-Roncancio, 2018}) was recently published.

During the development of a project on bioinvasions related to marine traffic, we studied copepods in coastal waters of three main Caribbean ports: Coveñas, Cartagena, Santa Marta, in contrast to adjacent reference areas characterized by less international shipping activity. Additionally, zooplankton contained in ballast water of ships anchored in the Morrosquillo Gulf was studied. Several new records and non-native species were found (^{Ahrens et al, 2011}).

The aim of the present article is to publish an update of the species list of planktonic and benthic copepods of the Colombian Caribbean, based on a critical revision of published and unpublished literature. Additionally, we describe the ecoregions inhabited by the known species and the new records, and call attention to the less studied groups and habitats.

METHODS

The present article is the result of a revision and update of the species registered hitherto in plankton and benthos of the Colombian Caribbean. The location of the geographical area analysed is shown in Figure 1.

Figure 1: Marine and coastal ecoregions of the Colombian Caribbean: GUA, Guajira; PAL, Palomino, TAY, Tayrona; MAG, Magdalena; MOR, Morrosquillo; ARCO, Coralline Archipelago; DAR, Darién, SAN, San Andrés and Providencia Archipelago; CAO, Oceanic Caribbean. Numbers indicate localities with records after 2010 (Tables 1 and 2): 1, Santa Marta Bay and Gaira Bay; 2, Pozos Colorados; 3, Cartagena Bay; 4, Barú-Barbacoas; 5, Coveñas and Cispatá. Map redrawn from ^{Díaz and Acero (2003)}. 

The checklist includes: 1) Copepod records of the project on bioinvasions in coastal waters of the Colombian Caribbean (^{Ahrens et al, 2011}, 2012) (Table 1); 2) Records from articles published until 2010 and compiled by ^{Medellin-Mora and Navas (2010)}; 3) Records from unpublished references until 2010. These species were marked as "not confirmed" records if they appeared solely there; 4) Species described or recorded after 2010 by several authors, from coastal waters of Gaira and Cartagena Bays. Genera mentioned in the references or as the result of the mentioned project without species determination, were not considered in the present checklist.

Table 1 Taxonomic list of copepods registered in the project "Evaluation of marine bioinvasions in coastal wetlands and their relationship with sea traffic in three major harbor zones of the Colombian Caribbean: Cartagena, Santa Marta and Coveñas" (^{Ahrens et al., 2012}): sampling locality (see Figure 1), date and inventory number of voucher material (UJTL-LL, collection Universidad Jorge Tadeo Lozano, Laboratory of Limnology, Bogotá; SG-COP, copepod collection of S. Gaviria). ? Identification not confirmed, * taxa identified in samples of the collection after the project end by SG (S. Gaviria) or JD (J. Dorado); ** no voucher material available. ▲first record for the Colombian Caribbean. 1, Santa Marta and Rodadero; 2, Pozos Colorados; 3, Cartagena Bay; 4, Barú-Barbacoas; 5, Coveñas and Cispatá Bay; ballast water of ships Chemtrans Sky (I), 

Table 1 shows the species of copepods recorded during the project. Samples of zooplankton containing copepods were collected in surface waters of the neritic zone using a standard plankton net with 130 mesh size. Collection of samples was done in March and October 2010 at the following areas: 1) adjacent waters of Santa Marta and Gaira (El Rodadero) Bays, 2) Pozos Colorados, 3) Cartagena Bay, 4) Barú-Barbacoas, and 5) Coveñas and Cispatá Bay. In October 2010 samples of zooplankton were taken from ballast waters of four ships anchored several kilometers off Coveñas. Samples of the water tanks were collected via vertical trawls with the same plankton net. Sampling locations are enumerated in Figure 1. The list also includes inventory numbers of the specimens of the reference collection of most of the species registered.

The checklist (Table 2) was elaborated based on the model published nine years ago by ^{Medellín-Mora and Navas (2010)}, with some modifications. The inventory was completed using published and unpublished records. In the present inventory, we considered taxa reported exclusively in unpublished references as "not confirmed records" (Table 2). With exception of two epibenthic species of Pseudodiaptomus, the inventory of 2010 only mentioned planktonic species.

Table 2: Taxonomic list of copepod taxa reported in the Colombian Caribbean. Recently added marine ecoregions of already known taxa are indicated in bold. For abbreviations of ecoregions, see Figure 1. * unpublish references; ** species reported after the 2010 inventory; pl, plankton, epi, epibenthos, ben; benthos; par, parasite; ?, record not confirmed; ü, identification considered reliable. Acronyms collections: CBUMAG: MEI, Centro de Colecciones Biológicas Universidad del Magdalena (Santa Marta); ICML-EMUCOP, Instituto de Ciencias del Mar y Limnología (Mazatlán); SG-COP, copepod collection of S. Gaviria (Viena); UARC, Colecciones Biológicas Universidad del Atlántico (Barranquilla); UJTL-LL, Universidad Jorge Tadeo Lozano, Limnological Laboratory (Bogotá) 

Taking into account that over the last decade the copepod fauna of benthic environments has started to be surveyed, we also include in the updated checklist benthic copepods (^{Fuentes-Reinés and Suárez-Morales, 2017c}, 2018; Fuentes-Reinés et al., 2017; ^{Gómez and Fuentes-Reinés, 2017a}, 2017b), collected in phytal habitats of coastal waters of Gaira Bay. Two of those publications also reported planktonic cyclopoids (Fuentes-Reinés and Suárez-Morales, 2017a, 2017b) for the same study area.

The checklist includes the report of the first monstrilloid copepod found in Colombia (^{Dorado-Roncancio and Dorado-Roncancio, 2018}) collected in an inner branch of the Cartagena Bay. Additionally, a parasitic species of Siphonostomatoida is also indicated (Dorado-Roncancio, 2014), but its taxonomy needs to be confirmed.

The inventory also summarizes the distribution of each species for the different ecoregions of the Colombian Caribbean, based on the division proposed by Díaz and Acero (2007): Guajira (GUA), Palomino (PAL), Tayrona (TAY), Magdalena (MAG), Morrosquillo (MOR), Coralline Archipielagos (ARCO), Darién (DAR), San Andrés and Providencia Archipelago (SAN), and the Oceanic Caribbean (CAO) (Figure 1). Ecoregions with reported presence of species lacking confirmed identification were also included in Table 2, but indicated as “not confirmed”, pending confirmation of the species. The species list includes habitat, the respective reference collection of the species and bibliographic references. Nomenclature follows WoRMS Editorial Board (2019), based on Walter and Boxshall (2019) and Boxshall & Halsey (2004).

RESULTS

A total of 43 species of planktonic copepods (18 calanoids, 21 cyclopoids, 4 harpacticoids) were reported based on samples collected during the project on bioinvasions of the Colombian Caribbean (^{Ahrens, 2012}). Five additional species (Candacia varicans, Bestiolina mexicana Corycaeus clausi, Onychocorycaeus latus and Oithona pulla) were found during later examination of the zooplankton collection (Table 1). Fourteen of those 48 species were also found in ballast waters of the four ships examined. Three of the species reported in ballast water (Bestiolina mexicana, Pseudodiaptomus pelagicus and Oithona colcarva) were found exclusively in the tanks of ships and hence cannot be considered part of the Colombian copepod fauna, as they have not been found yet in natural waters. Two species found only in ballast waters (Undinula vulgaris and Calanopia americana) are common inhabitants of the plankton of the Colombian Caribbean (^{Park, 1970}; ^{Michel and Foyo, 1976}; ^{Giraldo and Villalobos, 1983}; ^{Bernal, 2000}; Bernal and Zea, 2000; ^{Martínez-Barragán et al., 2009}) and, thus, form part of the Colombian copepod fauna.

Ten species identified during the project in natural waters were new records for the Colombian territory: Candacia varicans, Tortanus angularis (Calanoida), Corycaeus crassiusculus, Oithona attenuata, Oithona decipiens, Oithona pulla, Oithona simplex, Oncaea scottodicarloi, Pachos puntatum (Cyclopoida) and Goniopsyllus rostratus (Harpacticoida). Records of three species (Oithona attenuata, Oithona decipiens and Oithona simplex) were found during the first phase of the project (^{Ahrens et al, 2011}). Three cyclopoid species identified as Agetus limbatus?, Oncaea curvata? and Oncaea prolata?, should be considered as taxa without confirmed identification.

A total of 214 species belonging to the order Calanoida (158), Cyclopoida (38), Harpacticoida (15), Mormonilloida (2) and Monstrilloida (1) are now known from the Colombian Caribbean (Table 2) and are summarized at Table 3. Seventeen additional species (eight calanoids, six cyclopoids, two harpacticoids, one siphostomatoid) reported merely in unpublished theses are considered yet not confirmed. Calanoid species without confirmed identification are Acartia spinata, Acartia longiremis, Calanus finmarchicus, Candacia bipinnata, Xanthocalanus marlyae, Labidocera fluviatilis, Pontellopsis perspicax and Pseudodiaptomus acutus. Cyclopoid species considered not confirmed are Ditrichocorycaeus amazonicus, Dioithona oculata, Oithona atlantica, Oithona robusta, Oithona setigera and Sapphirina auronitens. Harpacticoid species Microsetella norvegica and Miracia efferata are also considered as taxa without confirmed identification. That is also true for the only siphonostomatoid copepod reported, namely, Caligus curtus.

Table 3: Number of families, genera and species of the copepod orders of the Colombian Caribbean, (for taxonomic details and distribution ranges, see Table 2). *Including family Clausiidae without genus and species determination. 

Of the 214 species listed in Tables 2 and 3, twentyfour species (3 calanoids, 11 cyclopoids, 9 harpacticoids and 1 monstrilloid) correspond to records obtained after the last inventory of marine copepods from the Colombian Caribbean (^{Medellín-Mora and Navas, 2010}). Besides the 10 new records of the mentioned project, 11 new species or new records were found at Gaira Bay (^{Fuentes-Reinés and Suárez-Morales, 2017a}, 2017b, 2017c; Fuentes-Reinés et al., 2017; ^{Gómez and Fuentes-Reinés, 2017a}, 2017b; Suárez-Morales and Fuentes-Reinés, 2018). The cyclopoid Oncaea scottodicarloi was reported in both studies, one near Coveñas (Morrosquillo ecoregion, ^{Ahrens et al., 2012}) and Gaira (Tayrona ecoregion, Fuentes-Reinés and Suárez-Morales, 2017b). The register of the monstrilloid copepod corresponds to Cartagena Bay (^{Dorado-Roncancio E.F. and J. Dorado-Roncancio, 2018}). Most of the species are planktonic (201), 10 are benthic and 3 epibenthic.

Table 2 includes information on the presence of each species in the Caribbean ecoregions. The Colombian Oceanic ecoregion, with 127 known species, shows the highest species richness, followed by Tayrona (94 species), Magdalena (82) and Morrosquillo (78). Moreover, 65 species were recorded at Darien and Guajira and 64 species at Palomino and Coralline Archipielago. The lowest number (49 species) corresponds to San Andrés and Providencia.

The updated anlaysis of the distribution of species in the afore mentioned ecoregions yielded 28 records of confirmed species previously unreported. These correspond to Tayrona, Magdalena and Morrosquillo, where new faunal surveys have been done after 2010.

Calanoida, with 26 families, 63 genera and 158 species with reliable identification, is the order with the highest number of records. The most speciose genera of calanoids currently known in the epipelagic zone continue to be the same as in 2010: Lucicutia (12 species), Haloptilus (8 species) and Candacia (7 species) (Table 1). The family Tortanidae with Tortanus angularis, found in the Magdalena ecoregion, is new for the inventory. The family Pseudodiaptomidae shows additional species, i.e. Pseudodiaptomus cokeri, collected in coastal waters of Santa Marta (^{Fuentes-Reinés et al., 2017}) and Pseudiaptomus pelagicus, found in the ballast water of a ship in the harbor of Coveñas (Dorado-Roncancio, 2012). The latter cannot be considered as part of the Colombian inventory because it has not been found in natural waters. Eucalanus elongatus, found in ballast water in the Magdalena ecoregion (^{Rendón et al., 2003}; ^{Medellín-Mora and Navas, 2010}), is apparently also present in natural waters of the Oceanic Caribbean (^{Park, 1970}).

Because the order Poecilostomatoida is now considered to be part of the Cyclopoida (^{Khodami et al., 2017}), the order now includes eight families in the Colombian Caribbean: Clausiidae, Corycaeidae, Cyclopidae, Kelleridae, Lubbockiidae, Oithonidae, Oncaeidae and Sapphirinidae, with 13 genera and 38 species with reliable identification. Eleven species are new for the region: Corycaeus crassisculus and Oncaea curvata collected at the Morrosquillo ecoregion, Neocyclops ferrari, Kelleria reducta, Oithona attenuata, Oithona decipiens, Conaea rapax, Oncaea prolata and Pachos punctatum from the Magdalena ecoregion, and Oithona simplex and Oncaea scottodicarloi in both ecoregions (Dorado-Roncancio, 2012, 2014). Oithona colcarva was found only in ballast water of a ship in the Gulf of Morrosquillo. Oncaea conifera is now placed in the genus Triconia (^{Boettger-Schnack et al., 2011}).

The order Harpacticoida is now represented by 10 families, 13 genera and 15 species with reliable identification (Table 2 and 3). The families Cletodidae, Dactylopusidae, Darcythompsonidae, Laophontidae and Tisbidae comprise benthic species, while Aethidae, Clytemnestridae, Ectinosomatidae and Euterpinidae contain exclusively planktonic species. One of the harpacticoid families (Miracidae), comprise planktonic and benthic genera. New species records after the 2010's inventory are the meiobenthic harpacticoids Geehydrosoma brevipodium, Goniopsyllus rostratus, Diarthrodes bodini, Diarthrodes gomezi, Darcythompsonia inopinata, Leptocaris colombiana, Leptocaris vicina, Echinolaophonte armiger, Echinolaophonte villabonae and Tisbrintra monroyi (^{Fuentes-Reinés and Suárez-Morales, 2017a}, 2017b, 2017c; Fuentes-Reinés et al., 2017; ^{Gómez and Fuentes-Reinés, 2017a}, 2017b; Suárez-Morales and Fuentes-Reinés, 2018). All originated from recent samplings in coastal waters of Gaira Bay at the Tayrona ecoregion.

The order Monstrilloida is represented by one species Cymbasoma chelemense. This record corresponds to a planktonic adult female found in estuarine waters of Cartagena (^{Dorado-Roncancio and Dorado-Roncancio, 2018}). Within the order Mormonilloida, only two species, Mormonilla phasma and Neomormonilla minor, are known in the studied area (^{Michel and Foyo, 1976}).

The order Siphonostomatoida was only known through genus Caligus (Carmona, 1979). Larvae of Caligus curtus were identified in a planktonic sample from Cartagena Bay (^{Dorado-Roncancio, 2015}), but its identification still needs confirmation.

DISCUSSION

CONCLUSIONS

Considering only species with realiable identification, the copepod fauna of the Colombian Caribbean currently comprises 214 species (201 planktonic, 10 benthic, 3 epibenthic). Twenty additional species, while mentioned in the checklist, are considered as "not confirmed", due to their only record being unpublished in undergraduated theses or doubtful identification. Recent studies of benthic harpacticoids associated with coastal habitats, a record of an monstrilloid at Cartagena Bay, as well as new surveys of plankton of three harbour zones corresponding to the Tayrona (Santa Marta and Gaira Bays), Magdalena (Pozos Colorados and Cartagena), and Morrosquillo (Barú-Barbacoas and Coveñas) ecoregions, are responsible for the increased species number in the current inventory compared to the previous one. Twenty-four species (3 calanoids, 11 cyclopoids, 9 harpacticoids, and 1 monstrilloid) constitute new records.

The total number of 214 species in Colombia represents less than 50 % of the diversity of copepods known in the Great Caribbean. Compared to Mexico, with 223 species, the richness is slightly lower.

The benthic representatives of harpacticoids, which constitutes most of the species of the order, have been poorly studied. No species of the parasite order Siphonostomatoida has been identified so far. Benthic substrates between intertidal and deep sea continue to be poorly known in Colombia. The highest diversity of copepods currently is found in the Oceanic Caribbean ecoregion, wheras the lowest is found in the San Andrés and Providencia Archipelago.

As already mentioned by ^{Medellín-Mora and Navas (2010)}, the deep-sea layers of the Oceanic region (mesopelagic - 200 to 750 m -, batypelagic - 750 to 3000 m, and abyssal - below 3000 m) are still poorly investigated habitats. Thus, species numbers in the Colombian Caribbean should increase with the study of mesopelagic to abyssal layers, benthic habitats and parasitic copepods.