Bathybembix bairdii ( Mollusca : Gastropoda : Calliotropidae ) as a potential fishery resource off western Mexico Bathybembix bairdii ( Mollusca : Gastropoda : Calliotropidae ) como recurso pesquero potencial frente a las costas de México

Bathybembix bairdii, the Baird’s top shell, is reported for the first time from off the Baja California Peninsula west coast and the southwestern coast of Mexico, at depths of 710-2,093 m. Environmental conditions measured near bottom were: 2.10 to 5.81 °C, 34.40 to 34.63 (salinity), and <0.12-0.90 ml L-1 O2. The species was found mostly in muddy sediments dominated by silt (56.5-87.0%) (Baja California) or in sediments with a significant proportion of sand (63.5 to 88.5%) (southwestern Mexico). Shell height varied from 10.0 to 53.7 mm, with high proportion of large specimens in shallower water off Baja California. Densities varied from 1.75 to 207.45 org. ha-1 off Baja California and from 5.25 to 50.72 org. ha-1 in southwestern Mexico. Estimated maximum biomass occurred off southwestern Mexico (2.2 kg ha-1). Relationship between height and total weight (shell plus soft part) and between height and soft part weight were both highly correlated (R2: 0.933 and 0.928, respectively). Soft part weight varied from 29 to 62% of total weight and proportion increased with size. Mega invertebrate species associated with B. bairdii included 47% of decapod crustaceans, 35% of echinoderms, and 18% of mollusks. As a by-catch species regularly found in deep-water trawls, B. bairdii could represent a valuable resource for


INTRODUCTION
With eight recognized species, the genus Bathybembix Crosse, 1893, is one of the ten genera of the family Calliotropidae Hickman & McLean, 1990.It is exclusively found in water deeper than the continental shelf.The Baird's top shell, Bathybembix bairdii (Dall, 1889), is one of three species occurring in the eastern Pacific and is widely distributed from Alaska to Central America (Hendrickx & López 2006) and further south to Chile (Santhanam 2018).Records for deep-water (> 200 m depth) mollusks are usually scarce due to sampling difficulties and cost, but a large series of specimens of B. bairdii was recently made available from research cruises in the southern Gulf of California and off El Salvador, thus bringing new information on this species abundance, distribution and tolerance to hypoxic environment (Hendrickx & López 2006).These authors reported material from 25 localities, in depth from 778 to 2140 m and dissolved oxygen concentrations from 0.07 to 1.98 ml L -1 , and estimated densities of up to 25 kg ha -1 with higher values registered off El Salvador.
Due to recent interest for deep-water resources in the region, particularly fishes and shrimps (e.g., Kameya et al. 1997, Ramírez-Rodríguez et al. 2003, Wehrtmann & Nielsen-Muñoz 2009, Hendrickx 2012), B. bairdii could represent an attractive by-catch species if a deep-water fishery is developed on a regular basis.It is a locally abundant large species (up to 55 mm height), with a taste adequate for consumption, and it has been considered as a potential, yet unexploited resource (Hendrickx & López 2006).Additionally, this information on B. bairdii occurrence and abundance is very valuable to shell collectors.Price ranges for this species from 20 to 35 US$ (Rice 1994).
Species of Bathybembix are known to occur in areas with oxygen deficiency, known as the Oxygen Minimum Zone (OMZ) (Hendrickx & López 2006, Sellanes et al. 2008).The OMZ off the west coast of Mexico is the largest worldwide.It is remarkably wide and encompasses a depth range of up to 1200 m in some areas.Oxygen concentrations in the Mexican Pacific OMZ core are also often critically low (<0.2 ml L -1 ) and represent a physiological barrier for many benthic and pelagic species (Helly & Levin 2004;Hendrickx & Serrano 2010, 2014;Hendrickx 2015).Recent research dealing with deep-water species of mollusks and decapod crustaceans from off the west coast of the Baja California Peninsula (Suárez-Mozo & Hendrickx 2016, Hendrickx et al. 2016, Papiol et al. 2016) have emphasized the effect of the OMZ on composition, abundance and distribution of deep-water invertebrates communities.However, detailed information on the abundance and tolerance to hypoxia of many species living close to the OMZ is still lacking.A large series of specimens of B. bairdii was collected off the west coast of the Baja California Peninsula and southwestern Mexico, between Jalisco and Guerrero.This study is aimed at providing additional information on the distribution, abundance and ecology of this species in the eastern Pacific.This information will be useful for future investigations dealing with this potential fishery resource in the region and emphasizes the wide distribution of the target species.

STUDY SPECIES
Bathybembix bairdii is a medium size (maximum known size, 55 mm shell height) deep-water species of Calliotropidae recently reported as very abundant off El Salvador (Hendrickx & López 2006).As other species of this genus, and in other genera within the family Calliotropidae, it is a deposit feeder (Hickman 1981) in muddy environment with evidence of consumption of plant debris and occurrence in deep-water kelp and wood falls (Gage & Tyler 1991, Miller et al. 2000, Kiel & Goedert 2006).It has been reported from off Queen Charlotte Islands, BC, Canada (Austin 1985).There is also a series of 28 records available at Global Biodiversity Information Facility (GBIF 2016) for the eastern Pacific, from Canada and the U.S.A., from off the northern tip of Prince of Wales Island (55°44'N-135°22'W) to off San Diego (32°38'N-117°29'W), and one isolated record from off Costa Rica (9°09'N-84°49'W).It has been reported for Ecuador by Keen (1971).Ramírez et al. (2003) reported B. bairdii in Peru in a checklist of species occurring in this area and Santhanam (2018) included it for Chile.In addition, there are numerous records from the Gulf of California (Fig. 1) and off El Salvador (Hendrickx & López 2006).The mollusks collections holdings of SCRIPPS Institution of Oceanography (SIO), of the Los Angeles Museum of Natural History (LAMNH), and of the Santa Barbara Museum of Natural History (SBMNH) include several records for this species.SIO has two records, the first from off San Pedro Island, central Gulf of California (931 m depth), and the second from off the Bay of Chamela, southwestern (SW) Mexico (66 m depth).The first record fit well with the known geographic and depth distribution of B. bairdii as described by Hendrickx & López (2006); the second, however, is rather surprising in what concerns the recorded depth and is probably erroneous.Records in the SBMNH are all from off California, and include both catalogued and un-catalogued lots.Records in the LAMNH holdings are exclusively from the San Catalina Island area, thus fitting the known distribution of the species off northwestern America.

DATA COLLECTION
The material on which this study is based was collected by the Research Vessel 'El Puma' of the Universidad Nacional Autónoma de México (UNAM), in 2012 and 2014 (TALUD project).The TALUD project (named after the word 'TALUD', meaning 'slope' in Spanish) was implemented in order to sample deep-water communities off western Mexico.Specimens of Bathybembix bairdii were captured during sampling operations off the southwestern coast of Mexico (one cruise: Jalisco to Guerrero; TALUD XII, March-April 2008) and off the west coast of the Baja California Peninsula (BC) (two cruises: TALUD XV, July-August 2012; TALUD XVI-B, May-June 2014).During these three cruises, a total of 63 localities were sampled, from 304 to 2165 m depth (Fig. 1).Positional coordinates for each sampling station were obtained using a GPS navigation system.Depth was measured with a digital recorder.All the specimens were captured with a standard benthic sledge (2.35 m width, 0.9 m high) equipped with a modified shrimp net (ca., 5.5 cm stretched mesh size) with a ca., 2.0 cm (3/4") internal lining net.The material collected during this survey was deposited in the Regional Collection of Marine Invertebrates (ICML-EMU), at UNAM in Mazatlán, Mexico.Shell height (standard measure used for all specimens) was measured to the nearest 0.1 mm and specimens weight (whole specimens and soft parts) to the nearest 0.1 g (Sartorius M-power balance).Abundance was estimated as density of organisms per hectare (org.ha -1 ) using the swept area method (width of the sledge * distance of the haul).Biomass (kg ha -1 ) was estimated using the total weight of each sample and the values from the swept area method.Environmental data were obtained from measurements at ~20 m above bottom using a CTD-O 2 (Seabird 19 with oxygen probe) and rosette-mounted 10 L Niskin bottles.Near-bottom temperature (T) and salinity (S) data were obtained directly from the CTD records and dissolved oxygen was estimated from water samples using the Winkler titration method (Strickland & Parsons 1972).Sediments were collected with a modified USNEL box core at each sampling station, and samples of the top 3 cm were stored at 4-8 °C.Grain size distribution was determined by laser dispersion (Malvern Mastersizer 2000E) or by traditional method of sieving and sedimentation (Folk 1968).with silt proportion >70% (Table 2).However, off SW Mexico, 3 out of 4 samples were associated with sediments containing a significant larger proportion of sand (63.5 to 88.5% sand content), and in one case with mixed sediments.All captures from off southwestern Mexico (TALUD XII) were associated with very low (0.22, 0.26 and 0.27 ml L -1 ) or low (0.51 ml L -1 ) oxygen concentrations.Off Baja California, a sizable number of large specimens (24) were associated with hypoxic environment (O 2 concentrations <0.12-0.90ml L -1 ), in depths near the lower boundary of the OMZ.Smaller specimens of B. bairdii were almost invariably (97 specimens) found in deeper water, with much higher oxygen concentrations (>1.4 ml L -1 ) (Table 2).
Minimum and maximum sizes (shell height) of the material examined were 10.0 and 53.7 mm, respectively.Off Baja California, size distribution of the examined material varied according to depth (Fig. 2), with a high proportion of large specimens found in shallower water and of small specimens found in deeper water.Off southwestern Mexico, all samples of B. bairdii came from a narrow depth range (1,058 to 1,299 m), thus making comparative depth-distribution impossible.

DISTRIBUTION
In southwestern Mexico (TALUD XII), Bathybembix bairdii was caught in 4 out of 18 sampling stations.Off Baja California, it was found in only one sample out of 22 during the TALUD XV cruise and in 11 out of 23 samples during the TALUD XVI-B cruise (Fig. 1, Table 1).The distribution of B. bairdii in western Mexico also includes the series of stations reported by Hendrickx & López (2006) in the Gulf of California (Fig. 1).

RELATIONSHIP WITH ENVIRONMENTAL PARAMETERS
Due to scarcity of records, strong variation in densities among sampling stations and heterogeneous distribution of samples, no significant relationship was detected when comparing densities of organisms and environmental parameters associated with each sampling station.According to Papiol et al. (2016), parameters that partly explained the occurrence and density of decapod crustaceans collected in the same area during the same cruises were depth and oxygen concentration.In the case of B. bairdii, however, simple correlations between density and these two parameters were very weak, with R 2 values lower than 0.01 in both cases.This is due to the heterogeneous dispersion of the species and very variable abundance of specimens.

ABUNDANCE AND FISHERY
Only one specimen in one sample was collected during the TALUD XV cruise, off Baja California Sur, in the northern limit of the area covered during this cruise (Fig. 1; solid).On the contrary, a total of 149 specimens were obtained in 11 samples during the Baja California northern cruise (TALUD XVI-B); in the southernmost sampling area, off southwestern Mexico, 87 specimens were caught in 4 samples (TALUD XII) (Table 2).In the later cruise, one station (XII-23) contained 62% (54 specimens) of the total catch for this area.In this southernmost area, density varied from 5.25 to 50.72 org.ha -1 , with an average of 26.48 org.ha -1 (Table 2).Biomass per hectare of the two largest samples (TALUD XII, 23 and 27) was estimated at 2.2 and 0.4 kg ha -1 , respectively.Off the Baja California Peninsula, density varied from a low 1.75 to a maximum of 207.45 org.ha -1 .Biomass per hectare of the two largest samples (XVI-B 7 and 15) (Table 2) was estimated at 0.79 and 0.24 kg ha -1 , respectively.Relationship between height and total weight (shell plus soft part) and between height and soft part weight were both highly correlated (R 2 : 0.9332 y 0.9281 respectively) (Fig. 3a y b).For B. bairdii, shell (not including the operculum) represents 38 to 71% of total weight, generally according to size of the individuals.The body (or soft part) weight of examined specimens (including the operculum) varied from 29 to 62% of total weight (Fig. 3b).several species of deep-water mollusks (Williams et al. 2004, Vaquer-Sunyer & Duarte 2008, Zamorano & Hendrickx 2012).The absence of specimens (either small or large) of B. bairdii in deeper water off southwestern Mexico (i.e., in depths >1299 m), where there is a significant increase of dissolved oxygen with increasing depth (Hendrickx & Serrano 2010, Serrano 2012), is rather puzzling and other factors (e.g., food availability, recruitment patterns) might affect species distribution in that area.Absence of specimens might also be related to patchy distribution patterns that characterize deep-water invertebrate fauna below the OMZ (Jumars & Eckman 1983, Levin et al. 2000, Papiol & Hendrickx 2016).
Size segregation by depth observed off Baja California might be due to the presence of two separate populations with distinct growing rhythm or to ontogenic migrations with larger, mature specimens migrating to shallower water.Changes in ontogenetic niche has been documented for shallow water species (e.g., Peel & Aldana-Aranda 2013) but is virtually undocumented for deep-water species.The narrow depth range at which B. bairdii was observed off southwestern Mexico (1,058 to 1,299 m), however, seems contradictory with the Baja California observations and further sampling is needed to establish the bathymetric distribution of this species, particularly trying to define where smaller specimens occur.
Size range of the material reported by Hendrickx & López (2006) was 10-54 mm (mostly >30 mm) for the Gulf of California and 32-44 mm for El Salvador, values that are similar to what was observed during this survey (i.e., 10.0 to 53.7 mm).Biomass data observed during this survey are far from the captures reported from off El Salvador (average of 25 kg ha -1 ) (Hendrickx & López 2006).Smith & Hamilton (1983) reported an average density of 0.024 org.m -2 off southern California, equivalent to about 240 org.ha -1 , very close to the maximum density registered in this study (i.e., 207.45 org.ha -1 ) off Baja California.Densities ranging from 14 to 769 kg trawl hour were recorded off El Salvador (Hendrickx & López 2006) which would represent an estimate of up to 71.2•10 3 specimens per hour of trawl considering individual weight between 18.0 g (large) and 3.6 g (medium-sized) for this species (10.8 on the average) (individual weight obtained from Mexican material).In this study, B. bairdii exhibited a meat (or soft part) content from 29 to 62% of total weight.Comparatively, meat content of Hexaplex trunculus (Linnaeus, 1758), represents about 38% of total weight (Vasconcelos et al. 2009).In other species of Gastropoda, however, meat content can be as high as 67-85% of total ASSOCIATED FAUNA Sampling data available for stations where B. bairdii was collected indicated a rich by-catch invertebrate fauna including 110 macrobenthic species: 52 decapod crustaceans (47% of total), 38 echinoderms (35%), and 20 mollusks (18%); data for fish are not available.

DISCUSSION
Although B. bairdii is widely distributed in the eastern Pacific, we were not able to trace any previously published record of this species from off the west coast of the Baja California Peninsula or from off southwestern Mexico.Therefore, all records of B. bairdii in these areas represent first reports and partly fill the distribution gap between California and Costa Rica.As in the case of Cardiomya planetica (Dall, 1908) and Astyris permodesta (Dall, 1890) (Levin et al. 2000, Gracia & Valentich-Scott 2014), B. bairdii could be even more commonly distributed to the south in the eastern Pacific but there is a significant lack of information for deep-water mollusks off western Colombia, Ecuador, Peru and Chile.
In this survey, a strong patchiness tendency was detected, with isolated captures of B. bairdii and absence of records in localities where environmental conditions were essentially similar.It is noteworthy, for example, that during this survey no specimens were found in three other stations with a similar depth range (i.e., 865-1,100 m) and similar environmental conditions (i.e., oxygen concentration, temperature), or in the 11 deeper stations (depth range, 1,380-2,165 m) where oxygen concentration were higher (see Papiol et al. 2016).Bathybembix bairdii might therefore belong to a group of macrobenthic species that show a preference for low oxygen environment with high supply of detritus in the sediments, conditions that are typically found below the OMZ in the study area (see Papiol et al. 2016).
Bathybembix species are mostly deposit feeders in muddy sediments (Gage & Tyler 1991).Throughout the study area food supply (i.e., deposits of organic detritus originating from the euphotic zone) is abundant (Papiol et al. 2016) and benefit deposit feeders.Our material was essentially found associated with muddy bottoms, except off southwestern Mexico.Feeding habits of these two sub-populations, off Baja California and off southwestern Mexico, might therefore be different but we have no information on this.Tolerance to mild (<0.5 ml L -1 O 2 ) to severe (<0.2 ml L -1 O 2 ) hypoxia is remarkable but not surprising, as similar tolerance has been documented for weight (Price et al. 1976).Although there is a clear relationship between size-total weight-age and meat weight in gastropods (Borulya & Bregman 2002), proportion of meat may vary according to reproductive cycle, stomach content and degree of erosion of the shell (Vasconcelos et al. 2009).As far as we know, there is no study on the nutritive value of B. bairdii.Kesavan et al. (2013) provided information related to the amino and fatty acids, the vitamins and minerals content of Babylonia zeylanica (Bruguière, 1789), noting that this abundant commercial species might provide an alternative source of meat in human diet; a similar study with B. bardii would be highly desirable.Associated fauna collected with B. bairdii was rather diverse (i.e., 110 species).The only comparative data available are those provided by Hendrickx & López (2006) from off El Salvador: decapod crustaceans (42.5%) and fishes (16%) largely dominated the by-catch, made of 33.0% of B. bairdii.
Gastropods have long been considered an emerging resource in the shrimp by-catch (Appukkutan & Babu-Philip 1994).Bathybembix bairdii has been recorded as a by-catch product of the 'Tanner' crab, Chionoecetes tanneri Rathbun, 1893, fishery by Phillips & Lauzier (1997) in British Columbia.These authors emphasized the dependence of the ecosystem where C. tanneri and the associated fauna live directly or indirectly from transfer of energy generated by near-surface primary production, a trend which has also been detected off the west coast of the Baja California Peninsula and in the Gulf of California, where B. bairdii is also known to occur (Papiol & Hendrickx 2016, Papiol et al. 2016).The presence of another species, Bathybembix humboldti has been reported from deep-water (200-1,480 m) by-catch off Chile, associated to Heterocarpus reedi Bahamonde, 1955, the 'chilean nylon shrimp' (Veliz & Vasquez 2000, Pérez et al. 2005) but no additional data were provided by these authors.Up to 2015, however, exploitation rate of species of Bathybembix occurring off Chile was not defined (Reyes & Hüne 2015).
Fishery potential of deep-water mollusks in the Mexican pacific is hard to evaluate due to their habitat (often below 500 m depth) and the time-consuming, costly fishing operations and need for specific gear (Hendrickx 2012).In addition, population dynamics and reproductive patterns of deep-water resources need to be thoroughly studied before regular fishery operations are to be considered and stocks should be adequately estimated (Phillips & Lauzier 1997, Koslow et al. 2000).

Figure 3 .
Figure 3. Relationship between a) shell height and total weight and b) shell height and soft parts weight of Bathybembix bairdii (n= 20) / Relación entre a) la altura de la concha y el peso total y b) la altura de la concha y el peso de las partes blandas en Bathybembix bairdii (n= 20)