Intertidal and shallow water amphipods ( Amphipoda : Gammaridea and Corophiidea ) from Isla Pérez , Alacranes Reef , southern Gulf of Mexico

Tropical coral reefs are known to exhibit high levels of biodiversity. Amphipod crustaceans are successfully adapted to a wide range of marine habitats in coral reefs, but some regions, such as the Campeche Bank in southern Gulf of Mexico, are poorly studied or even unsurveyed for amphipods. To begin to address this paucity of information, the present study records amphipod species from Isla Pérez, an island of the Alacranes Reef National Park, southern Gulf of Mexico. Twenty sites were sampled in the intertidal zone and shallow water adjacent to the island. Thirty-one species of amphipod were identified, 15 of which represented a geographical range extension to the northern Yucatan Peninsula, with four new records for the Mexican south-east sector of the Gulf of Mexico; nine for the Gulf Coast of Mexico; and two for the entire Gulf of Mexico. Significantly, a difference in faunal composition between windward and leeward areas of the intertidal zone was found.


INTRODUCTION
Among the main types of coral reef (platform, barrier, fringing, and atoll), those that form islands (e.g.atoll) include an intertidal zone, an important habitat for species along the shoreline (Spalding et al., 2001).The intertidal zone of the coral reef islands (like that of the continent) is an area of transition between the sea and land, which represents an extreme habitat due to the periodic desiccation caused by tidal fluctuations (Knox, 2001).
Due to their high biodiversity, coral reefs have been compared to tropical rain forests (Connell, 1978).They display a great diversity of habitats, which are expected to harbor a correspondingly great diversity of species (Miloslavich et al., 2010).Much of (Bousfield, 1970).Nevertheless, because previous studies have focused heavily on the subtidal zone (McKinney, 1977;Winfield and Escobar-Briones, 2007;Lowry and Myers, 2009), amphipod diversity in the intertidal zone of the coral reef islands has not been adequately described.
Thus, although many intertidal amphipods have been reported in the Gulf of Mexico and Caribbean (Ortíz et al., 2007;LeCroy et al., 2009), with the exception of the relatively well-known amphipod fauna of the Florida Keys (Thomas, 1993), the amphipod species inhabiting the intertidal zone of the coral reef islands in the Gulf of Mexico are poorly documented.For the Gulf Coast of Mexico, studies of amphipods in coral reefs have mostly recorded families/species from the subtidal zone (McKinney, 1977;Escobar-Briones and Winfield, 2003;Escobar-Briones and Jiménez-Guadarrama, 2010;Winfield et al., 2011).Notably, Escobar-Briones and Jiménez-Guadarrama (2010) suggested that the western Campeche Bank is a "hotspot" of biological diversity for the macrocrustaceans associated with the carbonated bottoms on the continental shelf, with the greatest number of families found in the proximity of the bank reefs and coral reef islands.
The present study aims to improve knowledge of the marine benthic fauna associated with the Alacranes Reef, and forms part of a long-term effort to explore the diversity of poorly characterized taxa in the region (e.g.crustaceans, sponges, echinoderms, opisthobranchs, and cryptic fish).Preliminary results from this research have already been published by Anker (2010;2012), Anker and De Grave (2010), Moreno-Mendoza et al. (2011), andPaz-Ríos et al. (2013).Here, we describe the amphipod species (documenting the extension of their geographical range) of the intertidal zone and shallow waters from Isla Pérez, Alacranes Reef, southern Gulf of Mexico.

MATERIAL AND METHODS
Alacranes Reef is an atoll-like platform reef located approximately 130 km off northern Yucatan Peninsula in the Campeche Bank, SE Gulf of Mexico (Fig. 1A), forming part of the North America's marine ecoregion 14 (Southern Gulf of Mexico) situated on the Campeche/ Yucatanean Outer Neritic region (Wilkinson et al., 2009).Alacranes Reef contains a large variety of relatively well-conserved habitats (Liceaga-Correa and Hernández-Núñez, 2000;Jordán-Dahlgren and Rodríguez-Martínez, 2003), and many coral patches and microatolls in the reef lagoon (Arias-González et al., 2012).The atoll-like platform has a semi-elliptic shape with an extension of approximately 26 km in length and a width of 15 km (Liceaga-Correa and Hernández-Núñez, 2000), including five sandy coral reef islands: Chica, Desterrada, Desertora or Muertos, Pájaros or Blanca and Pérez (Fig. 1B).Isla Pérez is the only inhabited island and the second largest island (just below the Isla Desterrada) according to the estimated data (area and perimeter) of Liceaga-Correa and Hernández-Núñez (2000).Isla Pérez is a low-lying sand cay that varies in outline as dictated by seasonal storms and wind directions (Kornicker et al., 1959;Folk and Robles, 1964).The tidal range in Isla Pérez is about 0.9 m (Folk and Robles, 1964), slightly greater than the range (0.7 m) for the coastal zone on northern Yucatan peninsula (Cuevas-Jimenéz and Euán-Ávila, 2009).Folk and Robles (1964) and Folk (1967) presented the sedimentary description of Isla Pérez.
Twenty sites were arbitrarily selected on the intertidal zone and shallow water adjacent to Isla Pérez (Fig. 1C; Tab.1); three of them (8, 14 and 20) were sampled twice at different times.Collection of samples involved different sampling devices (core, hand, Riley push-net, shovel, and suction sampler) and no standardized area or volume of sampling was used.Several types of coastal habitats were probed, such as beaches of homogeneous white sand, coral rubble bars, sea grass beds of Thalassia testudinum (Banks ex König, 1805), sandy bottoms, and shallow coral reef flats.All samples were treated with MgCl 2 , and then fixed with 10% formalin solution buffered with seawater before storage.In the laboratory, samples were washed through a 500 µm size mesh and transferred to 70% ethanol.Species were sorted and identified to the lowest possible taxonomical rank.Specimens are deposited and vouchered at the regional collection 'Crustáceos de Yucatán' (YUC-CC-255-11), UNAM-Sisal.Species classification follows LeCroy et al. (2009) and species composition is presented in the form of a checklist of species; only those species with a geographical range extension were annotated.Geographical range is represented by three nested spatial scales: i) Mexican south-east sector of the Gulf of Mexico, ii) Gulf Coast of Mexico, and iii) Gulf of Mexico.
The species distribution around Isla Pérez was explored at those stations of the intertidal zone located to the East on the windward side (stations 1, 6-15) and to the West on the leeward side (stations 2-5) of the island (Fig. 1C).A non-metric multidimensional scaling ordination analysis (MDS) was applied to a species matrix of presence/absence with the Sorensen coefficient as similarity index due to the differences in sampling effort and sampling devices at the different stations.To test the significance of species distribution explored in the MDS, an analysis of similarities (ANOSIM) was applied and an analysis of similarity percentages (SIMPER) with a cut off for low contributions of 75% was carried out to identify the main species on each side of the island.The statistical software used for analyses was PRIMER v6 (Clarke and Gorley, 2006).

RESULTS
A total of 1217 specimens were collected, belonging to 31 species, 26 genera, 17 families and two suborders (Tab.2).The families Aoridae, Leucothoidae and Melitidae showed the greatest richness, accounting 47% of the dominance of amphipods.The most abundant species were Colomastix sp., Cymadusa filosa Savigny, 1816, Eudevenopus honduranus Thomas and Barnard, 1983, Melita planaterga Kunkel, 1910, Metharpinia floridana (Shoemaker, 1933), Parhyale hawaiensis (Dana, 1853), and Tethorchestia antillensis Bousfield, 1984, which together accounted for about 90% of the amphipods collected in the intertidal zone and shallow water.Fifteen species defined a geographical range extension to the northern Yucatan Peninsula (Tab.2).Four of them are new records for the Mexican south-east sector of the Gulf of Mexico, nine for the Gulf Coast of Mexico and two for the Gulf of Mexico; these species are annotated below.
Remarks: This is the first record for the Mexican south-east sector of the Gulf of Mexico.The main identifying characteristics of this species are antenna 1 shorter than antenna 2; articles 3-4 of antenna 2 peduncle with dorsal clumps of setae; mandible with welldeveloped palp; pleon without dorsal process; coxal gills 2-5 dendritic; urosome carinate with segments 2-3 fused; telson deeply cleft with terminal spine on lobes.This species is very similar to Nototropis urocarinatus (McKinney, 1980), another species of the genus in the Gulf of Mexico; these species are highly related such that a synonymization has been proposed in LeCroy et al. (2009).
Remarks: This is the first record for the Gulf Coast of Mexico.The main characteristics that distinguish this species from other species in the genus Leucothoe are dactyl of gnathopod 1 long (reaching beyond tip of carpal lobe); propodus of gnathopod 2 with nearly transverse palm; propodus of gnathopod 2 with long, blade-like anterodistal process.
Records in the Gulf of Mexico: Loggerhead Key (Thomas and Klebba, 2007).
Remarks: This is the first record for the Gulf Coast of Mexico.The main identifying characteristics of this species are the extremely long dactyl of gnathopod 1; anteroventral margin of head with slight concavity; propodus of gnathopod 2 with palm linear and two or three strong tubercles; females are distinct among Western Atlantic species in having a tuft of numerous long posterodistal setae on basis of gnathopod 1.
Records in the Gulf of Mexico: Looe Key Reef; Lee Country; Hillsborough Country (Thomas and Barnard, 1985;Krapp-Schickel and Vader, 2009).
Remarks: This is the first record for the Gulf Coast of Mexico.The main characteristics identifying this species are inner plate of maxilliped with slender process on each side of distal margin; antenna 1 with accessory flagellum four-articulated; body setose dorsally; gnathopod 2 of male, right and left sides dissimilar, one side much larger than other; uropod 3, rami subequal in length; telson with strong dorsolateral spines at midpoint of each lobe.
Remarks: This is the first record for the Gulf Coast of Mexico.The main identifying characteristics of this species are antenna 2 with a small flagellum; propodus with dorsal and ventral margins almost parallel, palm with three tubercles; epimeron 3 having three ventrolateral tufts of robust setae.
Records in the Gulf of Mexico: Long Key (LeCroy, 2000).
Habitat: Among algae on rubble or sand bottoms; depth range from 1 to 2 m (LeCroy, 2000).
Remarks: This is the first record for the Gulf Coast of Mexico.Based on LeCroy (2000), this species is different to other known Gulf of Mexico species of Elasmopus by virtue of a posteroventral margin with very small tooth or cusp on coxa 1, an enlarged carpus with a sharply angled dorsal margin and a broad carpal lobe on gnathopod 2 and a concave, distally narrowing basis on peraeopod 5. Krapp-Schickel and Ruffo, 2001 (Fig. 2G) and Ruffo, 2001;Ortíz et al., 2007).

Maeracoota galani
Records in the Gulf of Mexico: Previously unreported.
Habitat: Shallow rubble or rock habitats with abundant algal growth, sea grass beds of Thalassia sp. and sometimes in night plankton tows over sea grass beds and rubble bottoms; depth range from the intertidal to 5 m (Lazo-Wasem and Gable, 1987;LeCroy, 2000;LeCroy et al., 2009).Melita planaterga has recently been recorded in a continental water body called Cenote Aerolito on Cozumel Island by Trujillo-Pisanty et al. (2010).Cenotes commonly occur in the Yucatan peninsula; they are classified as anchialine since they are characterized by a salinity gradient due to the connection with the sea (Mejía-Ortíz et al., 2006).
Remarks: This is the first record for the Mexican south-east sector of the Gulf of Mexico.Even though there were already records from the Gulf of Mexico, Gable et al. (2010) listed this species for Bermuda as endemic.The main identifying characteristics of this species are palm of gnathopod 2 entire or oblique with inner facial surface adjacent to palm forming depression; pleon dorsally smooth; epimeron 3 produced behind to form large tooth; urosome segment l with short medial mucronation on posterior margin, and urosome segment 2 with lateroposterior spine.
Remarks: This is the first record for the Gulf Coast of Mexico.The main identifying characteristics of this species are anterior margin of rostrum weakly concave; peraeon segment 1 with narrow central notch on dorsal carina; basis of peraeopods 5-6 with posterior lobe reduced.
Remarks: This is the first record for the Mexican south-east sector of the Gulf of Mexico.The main characteristics for identifying this species are rostrum entire and broad at base; eye well-developed; carpus of gnathopods 1-2 elongate, distinctly longer than merus; merus and carpus of peraeopods 5-6 slender to slightly expanded, moderately spinose; and dactyl of peraeopods 5-7 short.
Records in the Gulf of Mexico: Florida Keys to Marco Island (LeCroy, 2011).
Remarks: This is the first record for the Gulf Coast of Mexico.The main characteristics for identifying this species are antenna 2, peduncle slender, subequal to or shorter than flagellum; gnathopods 1-2 subchelate; propodus of peraeopod 7 with setal tufts on the distomedial margin; peduncle of uropod 1 with well-developed dorsolateral distal spine, outer ramus of uropod 1 without marginal spines; and ramus of uropod 3 cylindrical, tapering distally and tip subacute.
Remarks: This is the first record for the Gulf Coast of Mexico.This species was identified here with female specimens; therefore, no subspecies of B. spinicarpus (Bemlos spinicarpus inermis [Myers, 1979] or Bemlos spinicarpus spinicarpus [Pearse, 1912]) could be determined because these subspecies are indistinguishable in females (LeCroy, 2002).The main characteristics for identifying females of this species are body with pigmentation; ocular lobe rounded; coxae 1-4 contiguous, wider than deep; propodus of gnathopod 1 subequal to carpus in length, with palmar margin flat, convex and without defining tooth; basis of peraeopods 5-7 slender; distoventral process on peduncle of uropod 1 long; inner ramus of uropod 3 longer than peduncle.
Remarks: This is the first record for the Gulf Coast of Mexico.This subspecies, along with subspecies Lembos unifasciatus unifasciatus Myers, 1977, actually belongs in the genus Bemlos, pending its formal transfer to that genus (Myers, A.A. personal communication in LeCroy, 2002).The short distoventral process of L. unifasciatus reductus on the peduncles of uropods 1 and 2 distinguishes this species from those of other Bemlos (Myers, 1981;LeCroy, 2002).
Records in the Gulf of Mexico: Previously unreported.
Remarks: This is the first record for the Gulf of Mexico.So far the genus Pseudamphithoides contains only two species in the tropical western Atlantic reported by Ortíz et al. (2007): Pseudamphithoides bacescui Ortiz, 1976 and P. incurvaria.The latter species is mainly distinguished from P. bacescui by the narrower inner plate of maxilla 1, more robust setae (9) on the outer plate of maxilla 1 (5 on P. bacescui) and setose posterior margin of basis on peraeopod 4 (Karaman and Barnard, 1979).Pseudamphithoides incurvaria from Alacranes Reef corresponds well to the description of the material from Barbados by Just (1977); the only difference is the presence of two robust setae on apex of inner ramus on uropod 3 (without robust setae in P. incurvaria from Barbados).

Species distribution on Isla Pérez
The MDS ordination analysis divided sampling stations into roughly two groups representing the faunal composition of the intertidal zone on the East (windward) side and West (leeward) side of Isla Pérez, respectively (Fig. 3).Although the sampling methods employed varied and the sampling areas have different environmental and oceanographic characteristics, this result suggests broad similarity of faunal composition across each of the two regions identified, i.e. the windward and leeward sides of the island.The contribution (explained variance) to the ordination by the windward sites was 55%, whereas the contribution to the ordination by the leeward sites was 45%.The ANOSIM test reinforced this statement, detecting a significant difference (R = 0.321, p = 0.006) between the faunal composition of both side of the island.The SIMPER analysis identified the main species distinguishing each side of the island, giving abundance and relative contribution (Ind, %): on the windward side, Melita planaterga (52 Ind, 94%) was the major species, while on the leeward side the major species were Cymadusa filosa (34 Ind, 27%) and Tethorchestia antillensis (13 Ind, 64%).

Distribution of amphipod species on Isla Pérez
The spatial species distribution around Isla Pérez matches the distribution of specific island habitats, and relates to the lifestyle of each species.The geomorphology of the Alacranes Reef is highly complex, with direct implications for species distribution.In particular, Isla Pérez forms part of the reef crest barrier on the eastern windward side, where the island resists, absorbs and dissipates wave energy, while on the leeward side there is an extensive area of flow and ebb to the interior lagoon (CONANP, 2006).Each geomorphological condition is associated with a characteristic amphipod species composition.
On the West (leeward) side of Isla Pérez, where the shoreline is protected and composed of sandy beaches, the most frequent and abundant species of amphipod in the intertidal zone was Melita planaterga; this species has previously been found in the intertidal zone on rock habitats with abundant algal growth (Lazo-Wasem and Gable, 1987;LeCroy, 2000).Although the SIMPER analysis did not identify Lysianopsis alba as a main species, it was the second most frequent and abundant species on the island's leeward side.In coastal areas this species is usually found on muddy or silty sand or shell hash bottoms, along protected or semiprotected shores (LeCroy, 2007).
On the other hand, on the East (windward) side of the island, where the shoreline is exposed and composed of sandy beaches with sea grass beds and rubble beaches with corals and broken shells, the species Cymadusa filosa was highly abundant on sea grass beds of Thalassia testudinum.In sea grass beds and among algae, C. filosa has been reported with high abundance, tube-building behavior and detritivory habit (Zimmerman et al., 1979;Appadoo and Myers, 2003).Other species, such as Parhyale hawaiensis (another species not identified by the SIMPER analysis) and Tethorchestia antillensis, were found in large numbers in rubble intertidal beaches.The former species usually inhabits the region from the intertidal zone to shallow water, among algae and other fouling growth on hard substrata (e.g.piers, jetties, oyster beds, mangroves, and coral rubbles) (LeCroy, 2007), whereas the latter species often inhabits the supratidal zone, under the leaf litter of mangrove (LeCroy, 2011); in the intertidal zone of Isla Pérez, it is found under the leaves of T. testudinum on rubble beaches along the shoreline.For highly mobile supratidal fringe species, such as talitrid amphipods (including T. antillensis), with a high tolerance of aerial conditions, mangrove leaves and sea grass beds potentially provide both food and shelter (Porri et al., 2011;terHorst, 2012).
Those species with low abundance in the intertidal zone, but greater abundance in the shallow water adjacent to Isla Pérez, were Eudevenopus honduranus and Metharpinia floridana.Both species were collected on sand bottoms from the shallow water on the West (leeward side) of the island, and are typical examples of the most widespread infaunal families (Platyischnopidae and Phoxocephalidae, respectively) in sandy sediments of tropical coastal areas (Bousfield, 1970;Thomas, 1993).

Amphipods of the Alacranes Reef
With 256 species, the amphipod fauna of the Great Barrier Reef, Australia, is the richest fauna yet known from any tropical reef area (Lowry and Myers, 2009).In contrast, amphipods on Gulf of Mexico coral reefs have not been the subject of detailed systematic study (Thomas, 1993;Baldinger, 2000).Nevertheless, there are independent summaries for two southern coral reef areas: Thomas (1993) for the Florida Key Reefs and Winfield et al. (2011) for the Veracruz Reef System.The first of these pointed out that the number of species identified at that time (52 spp.) represented approximately one-third of the total number of species in the Florida Key reefs; the second study reported an accumulated number of 63 amphipod species on the Veracruz Reef System.In the Alacranes Reef, there are 44 recorded species from 22 families, of which 31 are reported in the present study, with the 13 remaining species being recorded in a study of fouling species in the Reef 's navigation buoys (Paz-Ríos et al., 2013).
Comparing the faunal composition of the Alacranes Reef with other coral reefs in the Mexican Atlantic, it is apparent that the Alacranes Reef shares more species with coral reefs of the Mexican Caribbean than with coral reefs of the southwestern Gulf of Mexico.As expected, the Alacranes Reef shares an intermediate number of amphipod families (14 of 28 families, 50% similarity) with those identified in the coral reefs in the western sector of the Campeche Bank by Escobar-Briones and Jiménez-Guadarrama (2010).At the same taxonomic rank, the Alacranes Reef shares few amphipod families (11 of 27 families, 41% similarity) with those identified in the Veracruz Reef System by Winfield and Ortiz (2011); at the species rank, the Alacranes Reef shares a relatively low number of species (two of 68 spp., 3% similarity) with the Veracruz Reef System.It is also instructive to compare the Alacranes Reef with the Mexican Caribbean reef Banco Chinchorro, although this has been poorly sampled spatially, only recording 25 species of gammarideans sensu lato for the entire coral reef (Oliva-Rivera, 2003).Notwithstanding this qualification, using the same principles of comparison, there are relatively few amphipod families (11 of 27 families, 41% similarity) shared between the Alacranes Reef and the Banco Chinchorro; this was also reflected at the species rank, where the Alacranes Reef shares only a small number of species (six of 64 spp., 9% similarity) with those identified in the Banco Chinchorro.
In the above cases, despite the differences in habitats studied and sampling methods, a comparison of the faunal composition among coral reefs in the Mexican Atlantic could be useful as baseline for developing biogeographic studies, for instance, to assess endemism using presence/absence data or to identify discrete ecoregions.
Based on the species listed in this study, there is a remarkable number of new records for northern Yucatan Peninsula (15 spp.), accounting for about 48% of the recorded amphipod fauna in the region.As has been noted in other studies (Winfield et al., 2006;Cardoso et al., 2011), such new records emphasise the importance of a taxonomic survey in these poorly studied habitats; the intertidal zone and shallow water of the Alacranes Reef 's islands thus have great potential for the discovery of more new records and even new species, given that the present work only sampled on one of the Reef 's islands.
Species inhabiting the intertidal zone and shallow water can be used as bioindicators inasmuch as the beaches are ecosystems that are affected by human action, for instance recreation (Defeo et al., 2009), which in the near future could become the major threat to the Alacranes Reef (Jordán-Dahlgren and Rodríguez-Martínez, 2003).Furthermore, given that coral reef islands are low-lying accumulations of unconsolidated carbonate sand and gravel deposited on coral reef platforms by the focussing effect of waves and currents (Stoddart and Steers, 1977), they are considered physically vulnerable to a range of climate change impacts including a rise in sea-level, changing weather and oceanographic wave regimes, and increased cyclone frequency and intensity (Webb and Kench, 2010).Therefore, as well as increasing the understanding of regional marine biodiversity, the amphipod species described in the current study may also serve as a baseline for shoreline monitoring by assessment of temporal change in faunal composition.

Figure 1 .
Figure 1.Location maps of the study area.(A) Alacranes Reef, southern Gulf of Mexico.(B) Coral reef islands in Alacranes Reef.(C) Sampling sites on Isla Pérez.

Figure 3 .
Figure 3. Non-metric multidimensional scaling ordination analysis (MDS) among stations (n = 15) on the intertidal zone in Isla Pérez.Overlap of two groups of sampling stations due to a high similarity on the fauna identity.