Introduction

The Mesoamerican Caribbean Reef System (MCRS) is regarded as the second-largest reef system after Australia’s Great Barrier Reef and is one of 200 global priority ecoregions worldwide (^{Contreras-Silva et al., 2020}). This huge ecosystem extends almost 1,600 km along the coastline of Mexico, Belize, Guatemala, and Honduras in the northwest sector of the Caribbean Sea and is comprised mainly of coral reefs along with mangroves, seagrass beds, and lagoon-inlet systems. The longest sector of this system is known as the Mexican Caribbean Sea (MEXCS), which is not only defined as a hotspot of endemic species, where numerous species can inhabit for feeding, nesting, and protection, but also has been impacted by coastal development, tourism, fishing (^{Perera-Valderrama et al., 2020}), pollution, and invasive sargasso (^{Rodríguez-Martínez et al., 2020}). Therefore, during the last 4 decades, the coastline ecosystems have been damaged by intensive urban and touristic expansion that has modified the structure, composition, and abundance of both benthic and pelagic communities.

As a result of natural ecological connectivity, knowledge of biodiversity in the MEXCS is required to design conservation, protection, and multidisciplinary management programs from those marine protected areas. So far, numerous organisms belonging to macroalgae, seagrass, mangroves, invertebrates, and chordates have been analyzed, either through species richness or abundance-distribution in this region (^{Ardisson et al., 2011}; ^{Contreras-Silva et al., 2020}; ^{Rioja-Nieto et al., 2019}). In the case of peracarid crustaceans, which includes isopods, amphipods, tanaids, and 6 other orders, the taxonomic and ecological information is fragmentary throughout the MEXCS.

The order Amphipoda is comprised of almost 10,200 nominal species grouped in 6 suborders (^{Lowry & Myers, 2017}; ^{Horton et al., 2021}). These peracarid crustaceans are associated with hard and soft bottoms, inhabiting areas from the coastline to the abyssal plain. Because of their abundance and wide-ranging geographic distribution, such benthic amphipods are involved in the trophic dynamics of marine communities as grazers, filter feeders, predators, scavengers, and prey (^{LeCroy et al., 2009}). In coral reef ecosystems, amphipods are associated with sediments, coral rubble, seagrass beds, macroalgae mats, and sessile invertebrates such as corals, sponges, bryozoans, echinoderms, and tunicates, among others (^{Thomas, 1993}a).

Due to their ecological importance, numerical abundance, and sensitivity to a variety of toxins and pollutants, amphipod crustaceans are recognized as bioindicators in a broad variety of ecosystems, particularly in the tropics (^{Thomas, 1993b}). Nevertheless, their incorporation into bioassessment programs on coral reefs and coastlines depends on taxonomic studies and inventories being completed (^{Monroy-Velazquez et al., 2017}).

During 2015 and 2016, 2 benthic sampling campaigns in the Coral Reef Puerto Morelos National Park (APM) and the Coral Reef Sian Ka’an Biosphere Reserve (SKAR), Quintana Roo, Mexico, were carried out to determine the biodiversity of benthic amphipods inhabiting several ecosystems and hard-soft bottoms. Also, the previously documented data on these peracarids from Contoy Island to the Xcalak Coral Reef were included in this paper. Therefore, the present study constitutes the first checklist of benthic amphipods along the MEXCS, including new records of benthic amphipod species in the Caribbean Sea, and provides a baseline of the existing marine amphipod biodiversity.

Materials and methods

The MEXCS is located in the northwest Caribbean Sea, along the coastline of the Quintana Roo State, Mexico, spreading from Contoy Island on the northern side to Xcalak Coral Reef to the south (Fig. 1). It includes 16 protected marine areas (PMAs), which have been characterized as flora and fauna protection areas, national parks, biosphere reserves, and one sanctuary (^{Rioja-Nieto et al., 2019}). According to ^{Contreras-Silva et al. (2020)} , this Mexican sector of the Caribbean Sea is divided into 5 main regions, Northern, Center, Southern, Cozumel, and Banco Chinchorro. The PMA belongs to the Northern region, with a total area of 9,067 ha, 21 km in length, and 4.5 km seaward in addition to several well-preserved reef sites and extensive areas of seagrass beds (^{Monroy-Velázquez et al., 2017}; ^{Perera-Valderrama et al., 2020}). Moreover, the Center region comprises both the Sian Ka’an Biosphere Reserve and the SKAR, which has a total marine area of 33,566 ha, 110 km length, and a maximum coral growth depth of 25 m.

Figure 1 Map showing the Protect Marine Areas throughout the Mexican Caribbean Sea (shadow ellipses); CC, Cozumel Channel. 

The information that the present study compiled on benthic amphipods arises essentially from the analysis of samples collected from macroalgae mats, seagrass beds, sponges, cnidarians, coral rubble, soft bottom, and wood debris from the APM and the SKAR during July 2015 and June 2016 (DGOPA.01024.110213.0236 and PPF/DGOPA-051/15 permits granted) as part of the “Macrocrustáceos asociados a los arrecifes de coral” project, which was supported by the Universidad Nacional Autónoma de México-DGAPA-PAPIIT. Such substrates were removed from 14 sample sites in both coral reefs by SCUBA diving between 0.5 and 25 m depth. The crustaceans associated with these substrates were separated, put into plastic bags, and preserved with 70% ethanol. Amphipods were divided from each crustacean sample and transported to the Facultad de Estudios Superiores Iztacala (FESI-UNAM). These specimens were examined and dissected using a stereoscopic microscope Motic SMZ-168 and optical microscope Leica DM750, both with camera lucida, at the Laboratorio de Crustáceos.

The taxonomic analysis was essentially based on ^{Barnard and Karaman (1991)} , ^{LeCroy (2000}, ²⁰⁰², ²⁰⁰⁴, ^{2007), Lowry and Stoddart (1997)}, ^{Ortiz et al. (2014)} , and ^{Thomas and Klebba (2007)} . The classification system of ^{Lowry and Myers (2017)} was adopted for this study. The specimens collected were deposited in the Colección Nacional de Crustáceos (CNCR), Instituto de Biología, (UNAM-México).

For the whole amphipod assemblage identified from both the APM and SKAR, specific amphipod richness and the total and relative abundances of each species were quantified, either for family, substrate, or site; additional information for each novel species recognized as a new record with geographic extension in the MEXCS, such as material examined, date, spatial distribution, depth, and substrate type, were provided. Also, new records of amphipods from the Caribbean Sea were documented to elucidate information regarding novel species, material examined, geo-referenced coordinates, the main morphological features, and previous geographic distribution where each species had been documented.

Finally, in addition to the amphipod species collected from the AMP and SKAR, we present previous amphipod records to summarize the benthic amphipods checklist which we compiled using published references from the MEXCS and verified according to the comprehensive taxonomic list for the ecoregions of the Caribbean Sea published by ^{Ortiz et al. (2007)} and ^{Martin et al. (2013)} . Every suborder, family, genus, and species are presented in an alphabetical rather than phyletic order, and the references where every species was reported along the MEXCS are included in the checklist.

Results

The present study documented a total of 120 nominate species grouped into 70 genera and 34 families, belonging to Amphilochidea (14 families), Colomastigidea (1 family), and Senticaudata (19 families) suborders. The most diversified amphipod families in this large sector of the Caribbean Sea were (in decreasing order): Maeridae, Aoridae, Leucothoidae, Ampeliscidae, Ampithoidae, Amphilochidae, Melitidae, Lysianassidae, and Pontogeneiidae. Also, and as a result of the 2 oceanographic campaigns carried out in APM and SKAR, Quintana Roo, not only 82 benthic amphipod species were identified, out of which 41 species had not been previously recognized along the MEXCS, but also 5 species represented new amphipod records from the Caribbean Sea.

New records of amphipods from the Caribbean Sea Shoemakerella lowryi^{Gable & Lazo-Wasem, 1990}. Material examined: APM; 20°50’28.57” N, 86°52’25.45” W; 12 m depth; 6-VI-2015; 8 specimens, M. Lozano-Aburto and I. Winfield, colls.; I. Winfield and M. Ortiz det., CNCR36044. This species can be recognized by the dorsal process on the peduncle of uropod 3, the proportion between basis and ischium of gnathopod 2, and the shape of basis of pereopod 7. Also, S. lowryi differs from S. cubensis in the relative lengths of propodus of peraeopod 7 (length 9.5 x width vs. length 5-6 x width in S. cubensis). This shallow species had been only documented in Bermuda (^{Gable & Lazo-Wasem, 1990}; ^{WoRMS, 2021}), the occurrence of this species in APM associated with coral rubble, represents the first new record from the Caribbean Sea.

Stenothoe minuta Holmes, 1905. Material examined: SKAR; 20°04’09.30” N, 87°28’09.30” W; 13 m depth; 19-VI-2016; 2 specimens, M. Lozano-Aburto and I. Winfield, colls., I. Winfield and M. Ortiz det., CNCR36050. This stenothoid species is identified by outer ramus of uropod 2 shorter than inner ramus, gnathopod 1 propodus posterior margin straight and shorter than palmar margin, gnathopod 2 palmar angle weakly angled-unrounded, without spinose lobe, peraeopod 7 basis broad with posterior margin convex, uropod 3 peduncle longer than article 1 of ramus. This shallow species had been only documented in several shoreline ecosystems along the Gulf of Mexico, from northeast Florida to the southwest of the Gulf of Mexico (^{LeCroy et al., 2009}). The presence of S. minuta in macroalgae mats in SKAR is the second new record from the Caribbean Sea.

Bemlos tigrinus (A.A. Myers, 1979). Material examined: APM; 20°52’06.9” N, 86°50’51.6” W; 10 m depth; 6-VI-2015; 5 specimens, M. Lozano-Aburto and I. Winfield, colls., I. Winfield and M. Ortiz det., CNCR36068. This species can be distinguished by peraeon segments 2-4 with mid-ventral sternal process, third the largest, pigmentation pattern on body composed of dorsal dark bands combined along the body, gnathopod 2 merus and carpus setose on anterior margin, peraeopods 5-6 basis with margin short simple setae. This shallow species had been recorded from West Florida Bay, NW Gulf of Mexico (^{LeCroy et al., 2009}), a consequence of such species, which was collected from APM in T. testudinum, is a new record for the Caribbean Sea.

Protohyale (Protohyale) frequens Bousfield & Hendrycks, 2002. Material examined: APM; 20°52’23.43” N, 86°51’9.95” W; 10 m depth; 9-VI-2015; 140 specimens, M. Lozano-Aburto and I. Winfield, colls., I. Winfield and M. Ortiz det., CNCR36082; SKAR; 20°00′40.07″ N, 87°28′07.41″ W; 3 m depth; 18-VI-2016; 5 specimens, M. Lozano-Aburto and I. Winfield, colls., I. Winfield and M. Ortiz det., CNCR36083. This species can be distinguished by the antenna 2 flagellum long, gnathopod 1 propodus elongate and subrectangular, gnathopod 2 propodus with anterior margin lacking robust setae, uropod 1 peduncular distolateral spine short, uropod 3 ramus slightly shorter than peduncle. This shallow species had only been recorded from coastline habitats, NE Gulf of Mexico (^{LeCroy, 2000}), therefore, the finding of this species in APM, and SKAR, in wood debris, wood dock, and macroalgae mats, represents a new record from the Caribbean Sea.

Melita elongata Sheridan, 1980. Material examined: SKAR; 20°00’40.07” N, 87°28’07.41” W; 4 m depth; 18-VI-2016; 2 specimens, M. Lozano-Aburto and I. Winfield, colls., I. Winfield and M. Ortiz det., CNCR36104. This species can be distinguished by gnathopod 1 parachelate, gnathopod 2 oval, female with anterior lobe of coxa 6 with a large hook backward, telson without robust dorsal setae. According to ^{LeCroy et al. (2009)} , it is distributed along the coastline of the Gulf of Mexico, from W Florida to Términos Lagoon. This species was found in coral rubble and soft bottoms in SKAR, consequently, it is a new record from the Caribbean Sea.

Discussion

The present study contributes to the first inventory of benthic amphipod species along the MEXCS documented from 1977 to date, including those species collected and analyzed in this work from both the APM and the SKAR, Quintana Roo, in 2015 and 2016. Previously, ^{Paz-Ríos et al. (2021)} documented some species richness ranges in benthic amphipods for the Western Caribbean ecoregion.

The MEXCS coastline includes beaches, rocky shores, seagrass beds, coral reefs, mangroves, and karstic bottoms, where the freshwater aquifer and seawater are frequently mixed (^{Rodríguez-Martínez et al., 2020}). Such ecosystems make up a complex semi-continuous coral reef barrier with the key geomorphological features of back-reef, reef-crest, and front-reef (^{Rioja-Nieto & Álvarez-Filip, 2019}). Throughout the MEXCS the benthic amphipods occur in diverse types of substrates, but are predominantly associated with coral rubble (88 species) and macroalgae mats (60 species), decreasing in species richness in seagrass beds and soft bottoms (22 species in each). According to the information summarized in this amphipod inventory, both the APM (38%, 83 species) and the SKAR (24%, 52 species), located in the north and central sectors of the MEXCS, represented the protected natural areas with the largest amounts and percentages of benthic amphipod species, with decreases in peracarids from the north sector to the south sector: Isla Mujeres (3%, 6 species), Isla Cozumel (7%, 17 species), Bahía Ascención (13%, 29 species), Banco Chinchorro (12%, 26 species), and Chetumal-Belice border (3%, 8 species). Besides, 84% of amphipod records belong to shallow water substrates (either soft-hard bottoms or living substrata), and 16% are from deep coral rubble (deeper than 25 m).

Although most coral reef works have documented tens of sponges hosting amphipod species belonging to Colomstigidae, Leucothoidae, Aoridae, and Maeridae, only Leucothoe spinicarpa, Leucothoe saron, Ampithoe marcuzzii, and Ericthonius brasiliensis have been recorded in sponges throughout the MEXCS. This fact is a result of the multidisciplinary management strategies proposed by the Protected Natural Areas Agency-Mexico, where the conservation and protection of numerous benthic invertebrates, such as sponges, represents a key component as a refuge for feeding, protection, and reproduction for several invertebrate species. Thus, knowledge of biodiversity and interactions between amphipod-sponges are fragmentary in the MEXCS.

Until now, 13 benthic amphipod species have been reported in most coral reef protected areas belonging to the MEXCS, out of which only Leucothoe spinicarpa, Lysianopsis alba, Elasmopus rapax, and E. levis occur throughout the whole MEXCS (Table 2). Recent analyses on biogeographic aspects showed 2 of these species (E. rapax and L. spinicarpa) are widely distributed across the warm Northwest Atlantic ecoregions (^{Paz-Ríos et al., 2021}). Until the amphipod inventory is completed for the Mexican Caribbean Sea protected areas, we cannot determine if the geographic distribution pattern of such benthic crustaceans is continuous or if it is defined as “patches” in each coral reef protected area. ^{Thomas (1993a)} suggested that the ecological features of these amphipod assemblages in each coral reef ecosystem, such as substrate specificity and biological adaptations, should be analyzed by microhabitats rather than a huge macrohabitat, which is a hypothesis to be tested in future research.