Deep-water bivalve mollusks collected during the TALUD XV cruise off the west coast of the southern Baja California Peninsula, Mexico

Abstract Background During the TALUD XV research cruise off the southern part of the Baja California Peninsula, Mexico, samples of macro-invertebrates obtained in the deep-sea (296–2136 m) revealed a rich fauna of bivalves (17 species belonging to 10 families). The number of species per station varied from one to five. The richest families were Nuculidae, Nuculanidae, Neilonellidae, Limidae, and Cuspidariidae. Solemyidae, Lucinidae, Poromyidae, Verticordiidae, and Pectinidae were each represented by a single species. Some species groups need a thorough revision and were tentatively identified (Nuculana cf. hamata, Limatula cf. saturna). New information Significant new distribution information is provided for two species, both recorded for the first time from off western Mexico: Ennucula panamina with an extension of its known distribution over 20° of latitude north and Jupiteria callimene with an extension of 16° 42' of latitude to the north. One species (Ennucula taeniolata) is reported in shallower depth and one in deeper water (Acesta sphoni). New records are provided for an additional nine species. Environmental and habitat conditions are given for the first time for many of the bivalve species.


Introduction
An intensive survey of deep-water invertebrates in Pacific Mexico has long been overdue (see . Deep-water mollusks collected in the 19th and 20th centuries during the "Albatross" and the "Velero IV" cruises represent the largest collection available to date in this area (see Dall 1895, Emerson and Puffer 1957, Parker 1963. In her monumental monograph, Keen (1971) reported 792 + 11 = 803 species of "Pelecypoda" from tropical West America, corresponding to what the author called the "Panamic fauna." Keen (1971) defined the survey area as extending from Magdalena Bay, along the SW coast of the Baja California Peninsula, to Punta Aguja, in northern Peru. She included in this area the Galapagos Archipelago and other nearer, offshore islands. Since its publication, this monograph has remained the basic reference book for all species of bivalves and other marine mollusks occurring in the tropical West America. Many taxonomic changes, new species, and new records of bivalves have since been added to the Panamic fauna as described by Keen (1971), most of which were compiled in the contributions of Skoglund (1991), Skoglund (2001).
The recent monograph on marine bivalve mollusks of tropical West America by Coan and Valentich-Scott (2012) provided a new tool for the study of these organisms in the region. It details nearly 900 species, thus representing an increase in bivalve species of about 12% compared to Keen (1971) monograph, and includes the description of several new genera and species.
In 1989, an intensive survey of the deep-water fauna of the Mexican Pacific (the TALUD project) was initiated by the Laboratorio de Invertebrados Bentónicos, Instituto de Ciencias del Mar y Limnología (ICML), Universidad Nacional Autónoma de México (UNAM), in Mazatlán, Mexico. Starting in 2000, sampling was aimed at collecting specimens living below the Oxygen Minimum Zone (OMZ) core (see Hendrickx 2012). In this contribution we report on material collected off the west coast of Baja California during the TALUD XV cruise.

Materials and Methods
The material reported herein includes both living and empty shells and was collected during the TALUD XV research cruise (29 July to 6 August 2012) aboard the R/V "El Puma" of the UNAM, roughly between 23°05' N and 27°08' N off the west coast of southern Baja California. A total of 23 stations were sampled between 296 and 2123 m depth. Specimens of deep-water organisms were collected with a 2.35 m wide by 0.95 m high, standard benthic sledge (Hendrickx 2012) equipped with an outer collecting net of ca 5.5 cm (2 1/4") stretch mesh and an inner net of ca 2.0 cm (3/4") stretch mesh. Trawling generally lasted 30 minutes (some trawls were interrupted after 15 minutes) at an average speed of 1.75 knots. A total of 19 infaunal samples were also obtained using a 40 cm x 40 cm box core (USNEL) in depths from 338 to 2290 m. Sampling depths were estimated with a digital SIMRAD echo sounder. Near bottom environmental parameters were obtained with a Seabird-19 CTD (temperature, T; salinity, S) and dissolved oxygen concentrations (DO) were measured by the Winkler method using water collected with 10 liters Niskin bottles. Sediments (sed.) from an USNEL box core were used for granulometric analysis. For each species the following information is provided: 1) list of material examined; 2) type locality; 3) current geographic distribution; 4) environmental conditions near bottom; 5) remarks, if any. The taxonomic sequence follows Coan and Valentich-Scott (2012). New records from off the west coast of the Baja California Peninsula were based partly on the database of the SCRIPPS Institution of Oceanography mollusks collection and on a large data base containing records of species for this area referred to by Zamorano and Hendrickx (2011), and on information provided by Coan and Valentich-Scott (2012). All the specimens examined are deposited in the Regional Collection of Marine Invertebrates at the Mazatlán Marine Station, UNAM, in Mazatlán, Mexico (ICML-EMU), or at the Santa Barbara Museum of Natural History (SBMNH), Santa Barbara, California, USA. Abbreviations used herein are: sb, scale bar; St., sampling station; Sa, sand; Si, silt; Cl, clay.

Data resources
This study is based on material collected during the TALUD XV cruise kept in the holding of the Regional Collection of Marine Invertebrates, Mazatlán, Mexico, on pertinent literature and on comprative material available at the Santa Barbara Museum of Natural History, California, USA.

Results
Specimens of bivalves were found in 10 out of the 23 samples obtained during the survey, between 236 and 2136 m depth. In total, 76 live specimens and 8 empty specimens were collected. The collection contained 18 species in 14 genera belonging to 11 families (Figs 1,2,3,4  Deep-water bivalve mollusks collected during the TALUD XV cruise off the ...

Systematic section
In this contribution, we present the species collected during the TALUD XV cruise. The following sections were included: material examined, type locality, distribution of the material collected, general geographic distribution, environmental conditions and remarks. The taxonomic organization follows Coan and Valentich-Scott (2012).  Type locality. SW of Isla Coiba, Panama (Albatross St. 3360).

Remarks.
Ennucula panamina had previously been reported from its type locality (Hertlein and Strong 1940) and from off Punta Mancora (Coan and Valentich-Scott 2012). The record of Parker (1963), in a sample taken below 1000 m depth, was omitted by Coan and Valentich-Scott (2012) as the illustrated specimen was actually Ennucula cardara (Dall, 1916). This record is the first for E. panamina off western Mexico, represents a new locality for this species, and extends its known distribution over 20° of latitude north of previous reports. Remarks. This is the first record of Ennucula taeniolata from the outer coast of Baja California, and represents the shallowest record for this species.

Fig. 1c
Material examined.  (Dall, 1908), from Mexico to El Salvador, and J. callimene (Dall, 1908), from Costa Rica and Panama. In examining the type specimen of each species, we found our specimen had a heavy hinge plate, with wider, more numerous, and more closely packed teeth. This clearly indicates that it is aligned with J. callimene. This new record extends the distribution of J. callimene by about 16°42' of latitude to the north to western Mexico. The depth range of the Baja California specimens examined is within the known range of the species (see Table  1). ( (1)
Synthesis of the material of bivalves collected during the TALUD XV cruise, including species per station, station depth, number of specimens and depth previously reported for each species (see text for species depth range references). D, dead specimen; L, live specimen. See Fig. 5 for species distribution. Record extension to the north; first record off western Baja California; new localities. (1) (2) Distribution. Forrester Island, Alaska, USA into the Gulf of California as far north as Isla Angel de la Guarda, Baja California, Mexico. 20-1100 m (Coan and Valentich-Scott 2012).
Remarks. The collected shell specimen is badly damaged, hence the identification is tentative. The specimen falls into a large species group (see illustrations in Coan and Valentich-Scott 2012) and potentially several new species need to be described in this poorly studied complex.

Remarks.
One of the two species of this genus previously recorded from tropical West America. The other species being Neilonella atossa (Dall, 1908), known from California to the Gulf of California, and Punta Agua, Peru.
Remarks. The material of ICML-EMU-9978 is about 15 mm height and probably represents a juvenile of this species. Two species of Acesta have been reported for tropical West America by Coan and Valentich-Scott (2012): A. agassizii (Dall, 1902), from the Gulf of California to Panama and Islas Galápagos, and A. diomedae (Dall, 1908), from off the Islas Galápagos. The other species previously known in the area, A. sphoni and A. mori, both from northern Oregon to southern California, were recently reported by Walz et al. 2014) from the Gulf of California for the first time. Walz et al. 2014 also provided greatest depth records for both species. Acesta sphoni occurs at shallower depths than A. mori, in warmer water with less oxygen (Walz et al. 2014). The material examined herein, however, was collected in depths from 540 to 850 m, thus increasing the maximum known depth for this species by ca 300 m (see Table 1).  (Dall 1908), also from Alaska to the Gulf of California, but extending to Central America and also present in Galapagos Islands. The specimens examined are similar to the holotype of L. saturna. In comparison to the type our specimens are more inflated, wider, and have more reduced ears. The depth range of L. saturna is from 20-675 m (Table 1). Our specimens identified as L. cf. saturna were collected in much deeper water than previous reports. This, combined with the unusual morphology, reinforces the idea that it might represent a new species. Type locality. Off Santa Barbara Islands, California.

Order
Distribution. Santa Barbara Channel, California, USA, into the Gulf of California, as far north as northwest of Isla Santa Cruz, Mexico to Chile. 400-1310 m (Zamorano et al. 2007, Coan andValentich-Scott 2012).

Remarks.
The genus Lucinoma is represented in the tropical West Pacific by three species: L. aequizonatum, from California to the Gulf of California, L. annulatum (Reeve, 1850), reported from a very wide latitudinal range, from Japan and Alaska south to the Gulf of California and Costa Rica, and L. heroica (Dall, 1901), known from the Gulf of California and off Pisco, Peru. The material reported by as L. heroica belongs to L. aequizonatum (see depth range for this species in Table 1, partly obtained from . Lucinoma aequizonatum is an extremophile and is characteristic of the most sulfide-rich, methane-rich, and oxygen-poor environments of modern continental margins (Moffitt et al. 2015). The material examined, although very similar to L. aequizonatum in shell morphology, might represent an undescribed species (John Taylor, pers. comm., December, 2013).
Remarks. This genus is represented by five species in the region. This new sampling confirms the presence of this species further south along the Baja California Peninsula (ca 2 degrees of latitude).
Remarks. This is the only species of this genus collected in the region. The material examined represents a new sampling locality and the first record from off the west coast of Baja California, Mexico, thus filling the distributional gap between southern California and the Gulf of California records.

Discussion
The material collected during the TALUD XV brings interesting information on the very rich deep-water mollusk fauna occurring off the west coast of the peninsula of Baja California. Specimens obtained also came from a wide latitudinal range (Fig. 5). Two species were recorded for the first time off western Mexico, with a distributional range increase of 16-20 degrees to the north (i.e., Ennucula panamina and Jupiteria callimene). In addition, five species have been collected for the first time off the west coast of Baja California Peninsula (i.e., Ennucula taeniolata, Neilonella ritteri, Lucinoma aequizonatum, Luzonia chilensis, and Dermatomya mactroides). New localities significantly filling the gap of their previously known distribution range were presented for four species (Table 1). As in the case of other invertebrates, diversity and distribution of deep-water mollusks is under the influence of many factors. Temperature, dissolved oxygen, sediment types and organic matter content in sediments are among the most important (Levin et al. 2001). In an area where the Oxygen Minimum Zone (ZMO) is particularly extended (Serrano 2012), dissolved oxygen values are critical for the survival of sedentary species. Some species of mollusks (e.g., Lucinoma spp.) are known to tolerate extremely low oxygen concentrations and are able to survive in severe hypoxic conditions Vaquer-Sunyer and Duarte 2008). Except for two samples (i.e., Jupiteria pontonia and Limatula cf. saturna), the material collected during the TALUD XV cruise was obtained in a very narrow oxygen range: 0.05 to 0.15 ml O /l. Both A. sphoni and L. aequizonatum have been previously reported as occurring repeatedly in very low oxygen conditions Taylor and Glover 2010).
Although the general depth range sampled during the TALUD XV cruise was 296 to 2285 m, it is surprising that samples of bivalves were generally obtained in a very narrow range, i.e., from 528 and 850 m: 83% of the species and 92% or the total number of specimens. Number of species found in each station was low (1 to 6). Although the numbers of species and specimens obtained were few, five and four species were collected in stations 23 and 20, respectively (Table 1). This is an interesting find considering that so little is known about deep-water mollusks communities composition below the OMZ in hypoxic conditions and about their adaptations and tolerance to oxygen deficiency.
Due to a general lack of information and of comparative material of deep-water bivalves in this region of the world, several species could not be properly identified and some might represent new species. This demonstrates that this fauna is poorly known and further surveys will without any doubts bring much needed data on deep-water bivalves of the Mexican Pacific.

Conclusions
A total of 17 species of deep-water bivalves were collected during the survey. The collection allows for the addition of new information related to the bathymetric and geographic distribution of these species. Some specific taxonomic issues remained to be 2 Figure 5.
Distribution of sampling stations where specimens of bivalves were collected during the TALUD XV survey off the western coast of the Baja California Peninsula.
solved, in particular in what concerns the identity of Ennucula panamina and E. taeniolata. Other material in need of a thorough review are Nuculana cf. hamata and Limatula cf. saturna. Besides, important ecological information was available for all species reported, including data on dissolved oxygen, temperature, salinity and sediments composition which are usually lacking for deep-water mollusks fauna. The studied bivalvia fauna is specifically associated with the lower boundary of the Oxygen Minimum Zone which is one of the major oceanographic characteristics in the eastern Pacific.

Ethics and security
Ethics have been followed during the field study and in the manuscript. Security aspects were respected under the rules and internal controls of the Universidad Nacional Autónoma de México.

Author contributions
MEH Head scientist of the TALUD project, redaction of first draft of the manuscript, revision and edition of succesive drafts. PVS Identification of specimens, revision of drafts and final edition of the manuscript. NYSM Revision of critical specimens, preparation of plates, revision of succesive drafts of the manuscript.

Conflicts of interest
The authors declare that they have no conflicts of interest.