Updated checklist and identification of areas of endemism of benthic amphipods ( Caprellidea and Gammaridea ) from offshore habitats in the SW Gulf of Mexico *

1 Laboratorio de Ecología de Crustáceos, Facultad de Estudios Superiores Iztacala. Posgrado en Ciencias del Mar y Limnología-UNAM, A. P. 314, Tlalnepantla, C.P.54090, Estado de México, México. E-mail ignacioc@servidor.unam.mx 2 Laboratorio de Biodiversidad y Macroecología, Instituto de Ciencias del Mar y Limnología-UNAM, A. P. 70-305, 04510, México, D.F., México. 3 Museo de Zoología “Alfonso L. Herrera”, Departamento de Biología Evolutiva, Facultad de Ciencias-UNAM, A. P. 70-379, 04510, México, D.F., México.


INTRODUCTION
The first reports of amphipods from offshore habitats were documented during the last decades of the 19 th century by Sars, Chevreux, and Stebbing (Thurston, 2000).A large number of amphipods have been recorded subsequently in diverse benthic habitats (Barnard, 1961(Barnard, , 1962(Barnard, , 1964)).Endemicity to the generic level was analyzed by Barnard and Karaman (1991) and Bellan-Santini (1990) within different biogeographic regions.At a worldwide scale, the surveys by Marquez and Bellan-Santini (1993), Cartes and Sorbe (1999), Bachelet et al. (2003), and Guerra-García (2003) have contributed with new species to the checklist, showing the restricted geographic distribution of species of this group.
Our knowledge of the amphipod fauna has significantly increased in the last years; however, it remains limited for offshore habitats in most of the ocean regions.The benthic amphipod fauna of the Gulf of Mexico has been extensively documented in the coastal ecosystems including the continental shelf (Myers, 1981;Ortiz, 1991;Thomas, 1993;LeCroy, 1995LeCroy, , 2000LeCroy, , 2001)).
Our objective was to update the checklist of benthic amphipod species (Caprellidea and Gammaridea) occurring between 25 and 3700 m depth, and to recognize areas of endemism of amphipod fauna in the offshore habitats of the south-western region of the Gulf of Mexico.

MATERIAL AND METHODS
The Gulf of Mexico is characterized by a complex geomorphology (Roberts et al., 1999) with various canyons, escarpments, salt diapirs and massive carbonated deposits (Bryant et al., 1991).The semienclosed basin is linked with the Caribbean Sea by the Yucatan Channel and with the Western Tropical Atlantic Ocean through the Straits of Florida and the different straits and sills through the Caribbean Sea.The seafloor is an accumulation of terrigenous clastic sediments, the sedimentary regime is the result of the influence of the Mississippi, Panuco, Papaloapan and Grijalva-Usumacinta rivers (McKee and Baskaran, 1999).
The continental shelf represents approximately 30% of the total area (Rabalais et al., 1999) with a variable extension (Bouma, 1972).The continental slope is characterized by the Mexican ridges in the western sector of the Gulf, a canyon and knolls in the Bay of Campeche, and an escarpment along the northern edge of the Campeche Bank.The Sigsbee abyssal plain occupies most of the central portion of the basin and is characterized by thin turbidite layers (Bryant et al., 1991).The surface circulation is dominated by the Loop Current and interaction with eddies (Welsh and Inoue, 2000), in general the water column is thermally stratified and displays space and time variability along the continental shelf (Monreal-Gómez and Salas de León, 1997).
The amphipod species were sorted out by sieving, with a 250 µm sieve, superficial sediment samples that were collected with GOMEX (0.06 m 2 ) and USNEL (0.25 m 2 ) boxcorers on six cruises: SIGSBEE.1 (SBI), SIGSBEE.2 (SBII), ENOS.1 (ENI), ENOS.2 (ENII), OGMEX.12 (OGXII), and OGMEX.16(OGXVI).These cruises were in the south-western (SW) region of the GM in the polygon delimited by 18º38.0'and 25º27.0'N-92º19.0'and 97º12.0'W on board the 100 I. WINFIELD et al.R/V Justo Sierra-UNAM from 1994 to 1999.The bathymetric range (25 to 3700 m) encompassed soft bottom habitats of the continental shelf, continental slope and abyssal plain.Sampling sites were graphically posted with the SURFER V.7 software.Caprellidea and Gammaridea amphipods were preserved in ethanol solution, and identified according to McCain (1968), Myers (1981), Lowry (1984), Barnard and Karaman (1991), Ortiz (1994), Bousfield and Hoover (1997), Lowry and Stoddart (1997), LeCroy (2000LeCroy ( , 2001)), and Ortiz et al. (2002).The classification and the superfamily arrangement followed Bousfield and Shih (1994) and Bousfield (2001).Incomplete or damaged amphipods were identified to the lowest taxonomic level possible.Each species herein reported includes the geographical occurrence, the information for depth and sediment type and the cruises on which they were collected.The specimens were characterized by their frequency and abundance of occurrence in the samples and herein named as dominant, common and rare faunal components.The specimens are deposited at the Colección Nacional de Crustáceos (CNCR-UNAM) and counted with a reference number to the database and collection.
Endemicity in this study was defined as local areas with high survival of species (allochthonous endemics) (Pielou, 1992).The Parsimony Analysis of Endemicity (PAE) was used to identify the areas of endemism in the SW region of GM.This method classifies the study sites according to their shared taxa, following the parsimony criterion (Rosen, 1988;Morrone, 2004).To obtain the cladograms and the strict consensus cladogram WINCLADA V 0.9.99 beta (Nixon, 1999) cladistic software was used.The data matrix (which can be requested from the first author) included 40 species (columns) that were identified as 0 to 39, collected in 15 sites (rows) that were identified as S1 to S15 (between 25 and 3635 m depth).The amphipods used in the data matrix included six caprellids and 34 gammarids.The amphipod information was coded as binary characters; presence of the amphipod was equal to 1 and its absence equal to 0 (Morrone, 1994).A hypothetic area was added (0 in all columns) to root the cladograms.The effects of sampling intensity and spatial autocorrelation were not considered in the findings.The areas of endemism identified were overlapped on the locations sampled.
This species is a common component, it occurs in soft bottoms of the Mexican ridges (SBI cruise) and the Bay of Campeche (OGXVI cruise) within a depth range of 550 to 2120 m.Czerniavski, 1868 This species is a dominant component, it occurs in muddy sediments of the Mexican ridges (SBI cruise) within a depth range of 550 to 2120 m.

Caprella equilibra Say, 1818
This species is a dominant component, it occurs in muddy sediments of the Mexican ridges and Sigsbee abyssal plain (SBI cruise) within a depth range of 1231 to 3700 m.Leach, 1814 This species is a dominant component, it occurs in muddy sediments of the Sigsbee abyssal plain (SBI cruise) within a depth range of 2200 to 3700 m.
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXVI cruise) at 897 m depth.(Mayer, 1903) This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXVI and ENII cruises) within a depth range of 116 to 1470 m.

Hemiaegina minuta Mayer, 1890
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXVI cruise) at 354 m depth.

Paracaprella pusilla Mayer, 1890
This species is a rare component, it occurs in muddy sediments of the Mexican ridges (SBI cruise) at 498 m depth.
Family PHTISICIDAE Vassilenko, 1968 9. Hemiproto wigleyi McCain, 1968 This species is a rare component, it occurs in soft bottoms of the Veracruz continental shelf (SBII cruise) and the Bay of Campeche (OGXVI cruise) within a depth range of 25 to 76 m. 10.Phtisica sp.
This species is a rare component, it occurs in soft bottoms of the Veracruz continental shelf (SBII cruise) at 76 m depth.

Phtisica marina Slabber, 1769
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXVI and ENII cruises) within a depth range of 76 to 1470 m.Suborder GAMMARIDEA Latreille, 1803 Superfamily AMPELISCOIDEA Bousfield, 1979 Family AMPELISCIDAE Costa, 1857 12. Ampelisca sp.
This species is a dominant component, it occurs in muddy sediments and sandy bottoms of the Veracruz continental shelf (SBII cruise) and Bay of Campeche (OGXII and OGXVI cruises) within a depth range of 25 to 203 m.
13. Ampelisca agassizi (Judd, 1896) This species is a common component, it occurs in sandy bottoms of the Bay of Campeche (OGXVI cruise) at 25 m depth.Goeke and Heard, 1983 This species is a common component, it occurs in muddy sediments and sandy bottoms of Tamaulipas continental shelf (SBI cruise) and the Bay of Campeche (OGXII and OGXVI cruises) within a depth range of 47 to 203 m.

Ampelisca bicarinata
15. Ampelisca lobata Holmes, 1908 This species is a common component, it occurs in soft bottoms of the Tamaulipas continental shelf (OGXVI cruise) within a depth range of 169 to 203 m. 16.Ampelisca parapacifica Goeke and Heard, 1984 This species is a common component, it occurs in muddy sediments and sandy bottoms of the Bay of Campeche (OGXII and OGXVI cruises) within a depth range of 26 to 169 m. 17.Ampelisca vadorum Mills, 1963 This species is a common component, it occurs in sandy bottoms of the Bay of Campeche (OGXVI cruise) at 25 m depth.Mills, 1967 This species is a common component, it occurs in muddy sediments and sandy bottoms of the Bay of Campeche (OGXVI cruise) within a depth range of 25 to 200 m.(Chevreux, 1908) This species is a rare component, it occurs in soft bottoms of the Sigsbee abyssal plain (SBI cruise) at 3600 m depth.

Ampelisca verrilli
22. Apocorophium simile (Shoemaker, 1934) This species is a rare component, it occurs in soft bottoms of the Mexican ridges (SBI cruise) at 1231 m depth.

Corophium sp.
This species is a dominant component, it occurs in soft bottoms of the Tamaulipas continental shelf, the Mexican ridges and the Sigsbee abyssal plain (SBI cruise) and sandy sediments of the Bay of Campeche (OGXVI cruise) within a depth range of 25 to 3700 m. (Costa, 1851) This species is a rare component, it occurs in soft bottoms of the Sigsbee abyssal plain (SBI cruise) at 2620 m depth.(Crawford, 1937) This species is a rare component, it occurs in soft bottoms of the Mexican ridges (SBI cruise) at 1231 m depth.This species is a rare component, it occurs in soft bottoms of the Mexican ridges (SBI cruise) at 498 m depth.(Shoemaker, 1933) This species is a rare component, it occurs in soft BENTHIC AMPHIPODS AND AREAS OF ENDEMISM 103 bottoms of the Bay of Campeche (ENII cruise) at 256 m depth.
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXII and OGXVI cruises) within a depth range of 26 to 203 m.Superfamily OEDICEROTOIDEA Bousfield, 1979 Family OEDICEROTIDAE Lilljeborg, 1865 38.Americhelidium sp.
This species is a rare component, it occurs in sandy sediments soft bottoms of the Bay of Campeche (OGXVI cruise) at 25 m depth.39.Americhelidium americanum (Bousfield, 1973) This species is a rare component, it occurs in soft bottoms of the Veracruz continental shelf (SBII cruise) at 76 m depth.

Hartmanodes sp.
This species is a rare component, it occurs in sandy sediments of the Bay of Campeche (OGXII cruise) at 25 m depth.

Perioculodes sp.
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (OGXVI cruise) at 61 m depth.
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (ENII cruise) at 878 m depth.
This species is a common component, it occurs in soft bottoms of the Bay of Campeche (OGXVI, ENI and ENII cruises) within a depth range of 25 to 1800 m. (Holmes, 1905) This species is a common component, it occurs in soft bottoms of the Bay of Campeche (OGXII and ENII cruises) within a depth range of 200 to 1290 m.

Metharpinia floridana
This species is a rare component, it occurs in sandy sediments of the Bay of Campeche (OGXII cruise) at 25 m depth.Bousfield, 1965 This species is a rare component, it occurs in sandy sediments of the Bay of Campeche (OGXVI cruise) at 25 m depth.Superfamily STENOTHOIDEA Bousfield, 2001 Family AMPHILOCHIDAE Boeck, 1871 Subfamily AMPHILOCHINAE Barnard and Karaman, 1991 52.Hourstonius tortugae (Shoemaker, 1933) This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (ENII cruise) at 879 m depth.
This species is a dominant component, it occurs in soft bottoms of the Mexican ridges and Sigsbee abyssal plain (SBI cruise) within a depth range of 498 to 3700 m.Walker, 1904 This species is a rare component, it occurs in soft bottoms of the Sigsbee abyssal plain (SBI cruise) at 3635 m depth.
This species is a rare component, it occurs in soft bottoms of the Veracruz continental shelf (SBII cruise) at 76 m depth.

Syrrhoe sp.
This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (ENI cruise) at 1800 m depth.
According to PAE and SCC, about 60 % of the difference between groups is accounted for by most species occurring at nine localities.Most of the ben-BENTHIC AMPHIPODS AND AREAS OF ENDEMISM 105 thic amphipod species are endemic to the continental slope and abyssal plain (25 %) and in overall, the Gulf of Mexico has 32 % endemism (or 18 species) of the 56 benthic amphipods reported in this study, and 6.5 % of endemic species of the Atlantic Ocean (279 species) (Thurston, 2000).

New records and geographical extension
This study contributes with 56 species that are grouped into 21 families and 13 superfamilies of the suborders Caprellidea and Gammaridea in the SW of GM.Ampelisca sp., Corophium sp., Cerapus sp., Concarnes sp., Harpinia sp., Maxillipius sp. and Stenothoe sp. will require a future taxonomic analysis once this larger collection of specimens is accounted for.The distribution of 13 amphipod species originally recorded for the northern GM is geographically and bathymetrically extended into the Bay of Campeche (Table 1).The occurrence of Caprella danilevskii, C. penantis and Stenothoe gallensis on the continental slope and the abyssal plain can be explained by sediment transport and turbidity currents.Other species (Hemiproto wigleyi, Carinobatea cuspidata, Parahaustorius holmesi, and Americhelidium americanum) extend their geographic distribution southwards.Other coastal species have also been recorded on the continental shelf (Ampelisca lobata, Hourstonius tortugae, and Concarnes concavus) and the continental slope (Phtisica marina).The family Corophiidae is one of the cases previously known from coastal habitats (Bousfield, 2000) and extending into the continental slope (Apocorophium simile and Monocorophium insidiosum), and abyssal plain (Apocorophium acutum, Corophium sp. and Monocorophium acherusicum).
New records of genera not previously recorded in the GM included Maxillipius sp. on the continental shelf with sister species M. rectitelson Ledoyer, 1973 in Madagascar andM. commensalis Lowry, 1984 in Papua New Guinea (Lowry, 1984), Halice sp. on the continental slope with 15 sister species (Barnard and Karaman, 1991) in the western sector.The presence of Syrrhoe sp. on the continental slope of the Bay of Campeche with 13 sister species, a close relative being S. papyracea Stebbing, 1888 from the Caribbean Sea (Barnard and Karaman, 1991) and Pseudharpinia sp. on the continental slope as well as the other two records of genera in the GM.
A total number of 101 species of caprellid and gammaridean amphipods, grouped into 26 families, were recorded by Escobar-Briones and Winfield (2003) on the continental shelf and upper continental slope and they recognized that the greatest species richness (ca.70%) occurred in the N and E Gulf of Mexico regions.These new records, which extend into the lower continental slope and abyssal plain, have increased by 41 species the known number of species and by six the number of known families.A larger effort has been made since 1997 solely in the abyssal plain habitats and may provide in the coming years new unexpected records.

Areas of endemism
Area A is considered controversial in this study owing to its small size and the exclusion of other sampling sites also located on the shelf of the Bay of Campeche.The marked seasonal influence of rivers and the resulting sedimentary texture would suggest that the distribution of the amphipod components could fluctuate from widespread to local over the long term.
The family Phoxocephalidae occurs frequently and in high abundance in area B in the continental slope of the Bay of Campeche, where species of the slope genera Halice sp., Syrrhoe sp., Pseudharpinia sp., Harpinia sp.occur.
Phoxocephalids (a primitive group) radiated successfully in shallower waters and colonized bathyal and abyssal depths before continental drift took place (Bousfield, 1982).Dispersion and speciation models for phoxocephalid amphipods are controversial and widely debated (Barnard and Drummond, 1978;Jarret and Bousfield, 1994); however, there is a coincidence between allopatrid speciation (vicariance) and the dispersion of this group towards the Western Atlantic.The incursion of Harpinia and Metharpinia into the Western Atlantic and the GM has been explained by the "post-Pangea" general model, with a centre of diversity in bathyal depths of the north-eastern Pacific (Jarret and Bousfield, 1994).Additionally, the presence of Halice sp., Byblis sp., Syrrhoe sp., Pseudharpinia sp.(primitive swimming forms), and Lembos sp.s.s.(primitive non-swimming aorid form), characteristic of bathyal and abyssal depths (Myers, 1981;Barnard and Karaman, 1991), fosters a new supposition about the GM and reinforces the hypothesis that the Bay of Campeche is an area with a high degree of endemism and greater biodiversity of natantia forms.Moreover, the broad protection in the marsupium, the fossorial condition, small body size, and direct development might represent endemicity evolutionary advantages for benthic amphipods.The patterns of origination and extinction that determine the current results are not biased by possible sampling artifacts (Miller, 2000), as we measured within-habitat rather than cumulative regional species richness and endemicity.
Area C has been recognized by the changes in sediment grain size that varies from inshore sandier substrates to offshore silt and clay sediments (Escobar-Briones et al., 1999).In addition to all the species and families (Caprellidae, Corophiidae and Stenothoidae) occurring in the Mexican ridge area there were frequent and abundant components.Variability (> 90%) in amphipod richness may be explained by habitat heterogeneity with secondary contributions from the net primary productivity exported as biogenic carbon to the seafloor in the area.Habitat heterogeneity relates to the total species richness at the regional level through species turnover.The exported biogenic carbon contribution represents a resource and can be important to species when its main role has an influence on the habitat characteristics e.g.minimum oxygen zone on the slope and high export rates on the continental margin.
Corophids and caprellids have been documented in coastal ecosystems in the northern GM (McCain, 1968;Myers, 1981;Bousfield, 2000;LeCroy, 2000).The distribution of these amphipods in deeper habitats of the northern GM suggests a later incursion of the reptantia species by sediment dumping during the Tertiary (Bouma and Roberts, 1990), or by continuous transport events from shallower waters caused by turbidity currents (Roberts et al., 1999).Similar sediment transport can occur in the Mexican Ridges promoting continuous transport of shallower species to deeper waters.Thomas(1993)

FIG. 1
FIG. 1. -Markers show the location of sampling stations of the six cruises where amphipods were sorted for this study.Abbreviations used: SBI: Sigsbee I, SBII: Sigsbee II, ENI-II: ENOS I and II, OGXII-XVI: OGMEX XII and XVI.

51.
Protohaustorius sp.This species is a rare component, it occurs in soft bottoms of the Bay of Campeche (ENII cruise) at 1140 m.
This species is a common component, it occurs in soft bottoms of the Mexican ridges and the Sigsbee abyssal plain (SBI cruise) within a depth range of 1231 to 3700 m.

TABLE 1 .
-Species of benthic amphipods that extend their geographical range within and into the Gulf of Mexico.Information includes the sector of previous record, the sector of new occurrence, the reported depth range, the new depth interval and the reference.