First Description of Deep-Water Elasmobranch Assemblages in the Exuma Sound, the Bahamas

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Deep-Sea Research II

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First description of deep-water elasmobranch assemblages in the Exuma Sound, The Bahamas

Edward J. Brooks a,n, Annabelle M.L. Brooks a, Sean Williams a, Lance K.B. Jordan b, Debra Abercrombie c, Demian D. Chapman d, Lucy A. Howey-Jordan b, R. Dean Grubbs e a Shark Research and Conservation Program, Cape Eleuthera Institute, Eleuthera, The Bahamas b Microwave Telemetry, Inc., 8835 Columbia 100 Parkway, Suites K & L, Columbia, MD 21045, USA c Abercrombie and Fish, Miller Place, NY 11776, USA d School of Marine and Atmospheric Science & Institute for Ocean Conservation Science, Stony Brook University, Stony Brook, New York 11794, USA e Florida State University Coastal & Marine Laboratory, 3618 Coastal Highway 98, St. Teresa, FL 32358, USA article info abstract

Deep-sea chondrichthyans, like many deep-water fishes, are very poorly understood at the most fundamental fi Keywords: biological, ecological and taxonomic levels. Our study represents the rst ecological investigation of deep- Deep-sea fisheries water elasmobranch assemblages in The Bahamas, and the first assessment of species-specific resilience to Deep-water capture for all of the species captured. Standardised deep-water longline surveys (n¼69) were conducted Mortality September to December 2010 and 2011 between 472 m and 1024 m deep, resulting in the capture of 144 Deep-Sea sharks from 8 different species. These included the Cuban dogfish, Squalus cubensis, the bigeye sixgill shark, Elasmobranch Hexanchus nakamurai, the bluntnose sixgill shark, Hexanchus griseus,thesmoothdogfish, Mustelus canis The Bahamas insularis,theroughskindogfish, Centroscymnus owstoni, Springer's sawtail catshark, Galeus springeri and the Longline false catshark, Pseudotriakis microdon. Preliminary genetic analysis indicated two or more species of gulper Squalus cubensis Hexanchus nakamurai sharks, Centrophorus spp.; however, for the present study they were treated as a single species complex. Water Hexanchus griseus depth and distance from the rocky structure of the Exuma Sound wall were inversely correlated with species Mustelus canis insularis richness, whereas seabed temperature was directly correlated with species richness. These variables also had a Centroscymnus owstoni significant influence on the abundance and distribution of many species. Expanded depth ranges were Galeus springeri established for S. cubensis and H. nakamurai,which,inthecaseofS. cubensis, is thought to be driven by Pseudotriakis microdon thermal preferences. At-vessel mortality rates increased significantly with depth, and post-release mortality Centrophorus spp. was thought to be high for some species, in part due to high post-release predation. This study highlights the importance of utilising strategic geographic locations that provide easy access to deep water, in combination with traditional expedition-based deep-ocean science, to accelerate the acquisition of fundamental ecological and biological insights into deep-sea elasmobranchs. & 2015 Elsevier Ltd. All rights reserved.

1. Introduction (Last, 2007; Naylor et al., 2012; White et al., 2013). Estimates of species productivity and intrinsic rebound potential only exist for 2.2% of There is a fundamental lack of basic biological and ecological deep-ocean chondrichthyans (Kyne and Simpfendorfer, 2010), and information pertaining to the majority of deep-water species (Devine those that have been assessed have among the lowest values et al., 2006; Haedrich et al., 2001; Norse et al., 2012), largely due to the documented for any species of fish to date (Simpfendorfer and Kyne, logistical challenges and expense of sustained ecological investigation 2009). In areas where deep-water sharks have been actively targeted in this remote and challenging ecosystem (Ramirez-Llodra et al., 2011). by fisheries, dramatic population declines have been triggered Despite being home to 50% of all known chondrichthyan species (Anderson and Ahmed, 1993; Barbier et al., 2014; Daley et al., 2002, (Kyne and Simpfendorfer, 2007), the study of deep-water elasmo- this issue; Graham et al., 2001; Graham and Daley, 2011; Jones et al., branchs is very much in its infancy; indeed, many genera need further 2005; Koslow et al., 2000; Morato et al., 2006; White and Kyne, 2010), investigation on the most fundamental genetic and taxonomic level and it is likely that bycatch of elasmobranchs in deep-water trawl and longline fisheries is having similar negative effects (Graham et al., 2001). Given the slow rate of scientific advancement in the deep- n Correspondence to: Shark Research and Conservation Program, Cape Eleuthera ocean, it has been suggested that many fisheries may become Institute, PO Box EL-26029, Rock Sound, Eleuthera, The Bahamas. fi Tel.: þ1 242 334 8552. commercially extinct before scienti cstudycanbegin(Haedrich E-mail address: [email protected] (E.J. Brooks). et al., 2001). http://dx.doi.org/10.1016/j.dsr2.2015.01.015 0967-0645/& 2015 Elsevier Ltd. All rights reserved.

The effective management and conservation of deep-sea shark Bahamas (24.541N, 76.121W). The Exuma Sound is a deep-water stocks is dependent on access to pertinent life history, community inlet of the Atlantic Ocean 200 km in length and 50–75 km in structure and species resilience data; information which at present width, orientated approximately NW/SE on its long axis. The is largely absent. Virtually no fisheries-dependent or independent Exuma Sound is surrounded by the shallow waters of the Great research has been conducted in the Western Central Atlantic Bahama Bank and is characterised by steep walls dropping from Fishing (WECAF) region, which incorporates the tropical and 30 m to over 500 m along its margin, slowly increasing to a sub-tropical western Atlantic, the Caribbean Sea and the Gulf of maximum depth of 1600–2000 m approximately 25 km from the Mexico. The Food and Agriculture Organisation of the United wall (Buchan, 2000). The steep walls at the edge of the Exuma Nations estimate that a total of 101 chondrichthyan species inhabit Sound are characterised by rugose limestone outcroppings provid- the WECAF region based on limited fisheries data (Kyne and ing a complex benthic structure (Ball et al., 1969). As gradients Simpfendorfer, 2007). A recent WECAFC workshop on deep-sea become shallower on the floor of the sound, the benthos transi- fisheries (October 2014) concluded that there were no commercial tions to muddy silt dominated by clastic turbidites (Crevello and deep-sea fisheries in the region operated by member states, Schlager, 1980) which provide very little benthic structure. The however, there are many foreign vessels operating in the region northeast corner of the Exuma Sound is 2.5 km from Powell and a request for fisheries data has been made to the relevant flag Point, on the southeastern tip of the island of Eleuthera, with states (R. VanAnrooy, personal communication). The only two water depths in excess of 1000 m accessible in less than 4 km published fisheries independent studies in the region are the work from shore. of McLaughlin and Morrissey (2004) who undertook a series of All research was conducted in collaboration with the Cape deep-water longline surveys of various types off the coast of Eleuthera Institute's sister organisation The Island School (www. Jamaica, and the work of Russell et al. (1988) who undertook islandschool.org). One of the tenants of The Island School pro- some bottom longline surveys off the coast of Puerto Rico. Other gramme is the immersion of students in ongoing primary research than these relatively limited studies, there has been no further conducted at the Cape Eleuthera Institute. Students are guided structured investigation into deep-water elasmobranch assem- through the research process from posing a question, gathering blages within the WECAF region. and analysing data, and finally communicating their results via In addition to understanding the basic structure of deep-water scientific posters and presentations. Both the 2010 and 2011 field elasmobranch assemblages, one of the most important areas of seasons were run as Island School research projects, thus this research from a management point of view is species-specific study performed a dual research and educational purpose. resilience to capture. The capture of an animal in commercial fishing gear imposes both physiological and physical insults, which 2.2. Demersal longline sampling can lead to either immediate (at-vessel), or post-release mortality (Brooks et al., 2012; Skomal and Mandelman, 2012). In deep-water Standardised demersal longline surveys consisted of a mainline sharks the stress of capture is potentially compounded by the anchored to the seabed by a single grapnel anchor. Thirty gangions additional thermal, barometric and photic stress associated with terminating in one of four different sizes of circle hook (5 16/0, an ascent from the deep-ocean. Consequently, it is likely that 5 14/0, 10 12/0, 10 10/0) were spaced approximately 10 m deep-water sharks have higher rates of both at-vessel and post- apart originating 5 m from the anchor. This wide range of hook release mortality than shallow water species; however, this has yet sizes was designed to capture a wide range of jaw morphologies to to be investigated. The quantification of post-release mortality is ensure that the gear would sample the entire species assemblage more challenging given the extreme conditions of the deep-water and all demographics within a species. The 300 m section of environment. In recent years pop-up archival satellite transmitters mainline to which the hooks were attached fished at prescribed (PSAT) have been used to quantify the post-release mortality and depths throughout the survey. Hooks were baited with a mixture behaviour of a number of shallow water species of shark (e.g. Atlantic bonito (Sarda sarda) and opportunistically sourced fish Campana et al., 2009; Hoolihan et al., 2011), however, the use of carcasses. To ensure all hooks were on the seabed, mainline length PSATs to monitor post-release survivorship and behaviour in deep- was a minimum of 1.5 times the water depth resulting in lengths water species has seen limited application. between 1000 and 2000 m. An archival temperature and depth Given this acute lack of fundamental data pertaining to deep- recorder (TDR) (Lotek LAT-1400, Newfoundland, Canada), pro- water elasmobranchs, there were two objectives to this study. grammed to record temperature and depth every second, was First, we investigate the diversity, distribution and demographic affixed to the mainline 10 m from the last hook. Depth and seabed structure of deep-water elasmobranch assemblages in the north- temperature for each set were taken as the deepest and coldest east Exuma Sound, The Bahamas; and second, we provide pre- record from the entire dataset. Soak time was 4 h based on liminary estimations of the resilience of the species encountered deployment and retrieval times, however, more accurate soak to longline capture. times were calculated post-hoc from TDR data, based on time at maximum depth. A maximum of two lines were deployed each field day, and never more than one at a time. Sets were conducted 2. Methods during both the day and night. For each survey, the straight line distance between the survey location and the vertical wall, Research was carried out under the Cape Eleuthera Institute marking the edge of the Exuma Sound, was measured using Arc research permit numbers MAF/FIS/17 and MAF/FIS/34 issued by GIS (Version 9.1, ESRI, Redlands, California, USA). Based on these the Bahamian Department of Marine Resources and in accordance measurements, surveys were assigned to six, 500-m wide geo- with CEI animal care protocols developed within the guidelines of graphic zones (Fig. 1). Since no surveys were conducted within the Association for the Study of Animal Behaviour and the Animal 500 m of the wall to minimise entanglement and gear loss in the Behaviour Society (Rollin and Kessel, 1998). rocky structure, Zone 1 was defined as 500–1000 m from the wall of the Exuma Sound, Zone 2 1000–1500 m, and so on through to 2.1. Study area Zone 6 which was 3000–3500 m from the wall (Fig. 1).

All sharks captured were identiﬁed to species and pre-caudal (LPC), This study was conducted September to December 2010 and fork (LF)andtotal(LT) lengths recorded. Sex was determined based on 2011 in the waters adjacent to Cape Eleuthera, Eleuthera, The presence/absence of claspers. Maturity estimates for males were based

Analyser (Applied Biosystems). Resulting sequences were validated by eye and then entered into the searchable Fish Barcode of Life Initiative (FISH-BOL) online database (http://boldsystems.org/)foridentiﬁcation to the lowest taxon possible. At the time, this database contained 297 shark species (of 4500 spp.).

2.4. Estimating mortality

At-vessel mortality was quantified upon retrieval of the gear and expressed as a percentage of the total catch of a specific species. Animals were considered moribund if there was (1) no movement, (2) no ‘blink’ reflect from the nictitating membrane or movement of the eye, (3) the presence of rigor mortis, or (4) the presence of scavenger damage. In the present study, X-Tags (Microwave Telemetry, Inc., Columbia, MD) 12 cm in length, 43 g weight in air, and rated to a crush depth of 2500 m, were attached to selected specimens of Centrophorus spp., Hexanchus griseus, and Fig. 1. Sampling zones, stratified by distance from the wall of the Exuma Sound, off Cape Eleuthera, The Bahamas. Dotted lines indicate sampling zones and points Hexanchus nakamurai. These PSATs were pre-programmed to demarcate the geographic location of each longline station. Total area sampled over detach after a set period of time (30 days–6 months), whereupon the course of the study was 10.5 km2 at depths ranging from 473–1024 m. they floated to the surface and transmitted archived temperature, depth and light levels through the Argos satellite system. on gross external morphological examination whereby the claspers were assessed for (1) the degree of calcification, (2) the length, (3) free rotation at the base, and (4) the ability to spread the distal end of the 2.5. Data analysis clasper. If the clasper rotated, was calcified and the distal end could be spread, then the animal was considered mature. We acknowledge that Abundance data relating to sparsely distributed animals is typically external examination alone is not sufficient to assess maturity in some characterised by large numbers of zeros leading to a heavily skewed species (e.g. Prionace glauca; Pratt, 1979), however, it remains the best distribution (Martin et al., 2005), and as a result, fails the assumptions non-lethal methodology, and is commonly used in contemporary of the majority of traditional parametric statistical techniques. In the literature (e.g. Brooks et al., 2013; Chapman et al., 2007; Pikitch et al., present study, Contingency Analysis was used to model species- 2005). Maturity was assigned to females based on published size-at- specific presence/absence against capture location (Zones 1–6) and maturity data when available. For all animals a small finclipwas the time of day (Day/Night). Following contingency analysis, Pearson's collected for genetic analysis and for those that were released, an Chi Squared tests were used to test the null hypothesis that the individually numbered dart tag was inserted in basolateral dorsal distribution of presence and absence was equal across categories. musculature (Hallprint, Victoria Harbour, Australia). Between category differences were identified by serial contingency analysis comparisons between levels and subsequent Chi Squared 2.3. Genetic identification of species tests. The effects of water depth and seabed temperature on the presence/absence of each species were modelled using logistic The taxonomy of some deep-water elasmobranch taxa is not fully regression. Elasmobranch species richness, defined as the number of resolved. We used DNA barcoding of the cytochrome oxidase I gene species captured on a single longline, was analysed with respect to (mtCOI) to identify to the lowest taxonomic level for each specimen water depth, seabed temperature and sampling location using non- captured. Polymerase chain reaction (PCR) of the mtCOI PCR was parametric Spearman Rank Correlation. Male size at maturity esti- carried out using genomic DNA template isolated from ethanol mates were generated using logistic regression when sufficient preserved fin clips taken from live or dead sharks. Genomic DNA numbers of both mature and immature male animals were captured. were extracted from 10–25 mg of tissue using a modified protocol Inverse prediction based on the logistic function was used to predict with the DNeasy (Qiagen, Valencia, California) commercial kit. PCR the length (LT) at which 50% (M50) of the male population reached was performed in a volume of 50 μL, which included 1 μLofthe maturity (Papastamatiou et al., 2009). All the above analyses were extracted genomic DNA, 10 pmol of each forward and reverse primer, performed using JMP 7.0.1 (SAS Institute, Cary, NC, USA) and the level 1X PCR buffer, 40 μM dNTPs, and 1 unit of HotStar© Taq Polymerase of significance (α) for all tests was 0.05. (Qiagen, Valencia, California). We used mtCOI primers previously To test the effectiveness of longline sampling in describing the published by Ward et al. (2005), obtaining 550 bp of sequence for species richness of deep-water shark assemblages, a species- each specimen. All reactions were run with a positive (i.e., shark DNA accumulation plot was constructed. However, given that species previously confirmed to amplify with other primers) and negative (i.e., richness (S), defined as the number of unique species, is a non- no DNA). Thermal cycling conditions consisted of a 5 min activation of linear function of sampling effort absolute values of species thepolymeraseat951C, followed by 35 cycles of 1 min at 94 1C, 1 min richness are rarely reached (Southwood and Henderson, 2000). at 52 1C, and 2 min at 72 1C, followed by a final extension step of 72 1C Several absolute species richness extrapolators were incorporated for 5 min. Amplicons were resolved on a 1.2% agarose gel and in an attempt to predict the diversity of deep-water elasmobranch visualised using ethidium bromide dye. PCR products were purified species that exists in the study area, given an infinite number of with ExoSAP-IT (Affymetrix, Inc., Santa Clara, CA, USA) and sequenced samples. Sample order was entered randomly (999 permutations) using the Big Dye Terminator v3.1 cycle sequencing kit (Applied and five nonparametric extrapolation models used were, in order Biosystems, Foster City, CA, USA) with a Bio-Rad DYAD thermal cycler of conservative to least conservative: Bootstrap, Chao1, Chao2, (Bio-Rad Laboratories, Hercules, CA, USA). The M13 forward primer Jacknife1, and Jacknife2 (Clarke and Gorley, 2006). These analyses was used for sequencing. The resulting products were precipitated were conducted using PRIMER v6.0 (Plymouth Marine Labora- with 125 mM EDTA and 100% ethanol and run on an ABI 3730 DNA tories, Devon, UK).

3. Results Squalus cubensis (Contingency Analysis – χ2¼0.906, p¼0.341), Centrophorus spp. (Contingency Analysis χ2 ¼2.193, p¼0.139), A total of 69 deep-water longline surveys resulted in the capture of H. griseus (Contingency Analysis χ2 ¼0.027, p¼0.872), Mustelus 144 individual sharks from 8 different species (Table 1 and canis insularis (Contingency Analysis χ2 ¼0.277, p¼0.599), Cen- Supplementary Table 1). Survey depths were between 472.6 m and troscymnus owstoni (Contingency Analysis χ2 ¼0.012, p¼0.911) 1024.1 m (weighted mean ¼700.0m),andseabedtemperaturesof or Galeus springeri (Contingency Analysis χ2 ¼1.945, p¼0.163). 5.9–15.6 1C(weightedmean¼10.4 1C). Over two thirds of the surveys Time of day did have a significant effect on the presence/absence were conducted during daylight hours (Day: n¼48,69.6%.Night: of H. nakamurai (Contingency Analysis χ2 ¼5.117, p¼0.024) n¼21, 30.4%). Surveys were conducted between 462 m and 3588 m whereby all fourteen individuals were captured during the day. from the shelf edge of the Exuma Sound, although sampling density Given the lack of significant variation in diurnal catch rates for the washigherincloserproximitytothewall(Fig. 1). Significant, non- majority of species, no distinction was made between day/night linear relationships were established between water depth (r2¼0.895, sets was made for all further analysis. p¼ o0.001) and temperature (r2¼0.906, p¼o0.001) and distance from the ‘drop-off’ of the Exuma Sound (Fig. 2). A poorly defined thermocline appears at 100–150mclosertotheedgeoftheExuma 3.2. Distribution and demographic structure of elasmobranchs Sound, and becomes less defined further offshore, deepening to approximately 200 m (Fig. 3). A small thermal inflection is also The Cuban dogfish (S. cubensis) was the most abundant species apparent at 450–500 m (Fig. 3). Descriptive environmental data for captured over the course of the study (n¼55). We found that mtCOI each zone are presented in Table 2. sequences obtained from all individuals tentatively identified as being this species in the field were matched with 100% certainty to reference sequences of S. cubensis in the Barcode of Life Database 3.1. Diurnal variation in catch rates (BOLD). Cuban dogfish were one of the shallowest dwelling species, captured at a mean depth of 581.1 m (79.4 S.E.), a mean seabed The time of day (Day/Night) during which the surveys were temperature of 13.0 1C(70.25 S.E.), and were significantly high conducted had no significant effect on the presence/absence of er in abundance less than 1000 m from the drop-off of the Exuma

Table 1 Catch composition of deep-water elasmobranchs sampled over the course of the present study.

Latin name Total Mean LT Range LT Mean depth (m) Depth range Mean temp. Temp range catch Males Female Unsexed (cm) (cm) (m) (1C) (1C)

Squalus cubensis 55 23 32 0 61.0 45–80 581.8 (79.45 S.E.) 472.6–730.6 13.0 (70.25 S. 9.2–15.6 E.) Centrophorus spp. 51 9 38 4 95.1 52–156 731.4 (78.1 S.E.) 580.5–829.6 9.5 (70.2 S.E.) 7.9–12.9 Hexanchus nakamurai 14 11 3 0 148.4 111–171 639.5 (717.3 S.E.) 504.1–701.5 11.5 ( 70.4 S.E.) 10.0–14.5 Hexanchus griseus 8 4 4 0 287.4 108–389 665.4 (733.5 S.E.) 564.9–791.0 11.1 ( 70.9 S.E.) 8.2–13.8 Mustelus canis 7 1 6 0 92.1 74–113 549.7 (720.95 S. 504.1–651.1 14.1 (70.6 S.E.) 11.5–15.6 insularis E.) Centroscymnus 5 1 3 1 79.7 72–102 888.3 (739.6 S.E.) 841.4–1024.1 7.3 (70.5 S.E.) 5.9–8.0 owstoni Galeus springeri 3 1 2 0 42.2 31–53 706.8 (764.0 S.E.) 630.6–806.9 10.4 (71.5 S.E.) 8.2–12.3 Pseudotriakis 1 1 0 0 227.0 227 790.1 n/a 8.7 n/a microdon

Fig. 2. Species richness was found to decrease signiﬁcantly with increasing distance from the wall of the Exuma Sound (ρ¼0.295, p¼0.014), increasing depth (ρ¼0.242, p¼0.045), and decreasing seabed temperature (ρ¼0.288, p¼0.016). Signiﬁcant non‐linear relationships were established between distance from the wall of the Exuma Sound, depth (r2¼0.895, p¼ o0.001), and temperature (r2 ¼0.906, p¼ o0.001).

Fig. 3. Example depth and temperature proﬁles from each of the six sampling zones illustrated in Fig. 1. Data presented represent mean temperature every 20 m during the descent phase for a single longline deployment in the centre of each zone in the Autumn (September–December).

Table 2 Environmental data derived from the temperature depth recorders deployed on each set stratiﬁed by sampling zone. Approximate values for the wall are provided as reference.

Wall Zone 1 Zone 2 Zone 3 Zone 4 Zone 5 Zone 6

Distance from The Wall (m) 0500–1000 1000–1500 1500–2000 2000–2500 2500–3000 3000–3500 Depth mean (m) 25 554.3 (713.0 S.E.) 678.9 (76.7 S.E.) 741.20 (710.7 S.E.) 811.1 (710.3 S.E.) 842.6 (751.3 S.E.) 922.6 (728.7 S.E.) Depth range (m) n/a 472.6–662.1 604.1–730.6 620.6–841.4 789.1–840.1 791.0–893.5 856.5–1024.1 Temperature mean (1C) 28 13.7 (70.35 S.E.) 10.6 (70.2 S.E.) 9.2 (70.2 S.E.) 8.3 (70.2 S.E.) 7.4 (70.78 S.E.) 6.6 (70.3 S.E.) Temperature range (1C) n/a 10.7–15.6 9.2–12.3 7.9–11.7 7.7–8.7 6.7–8.2 5.9–7.5

Sound (Contingency Analysis χ2¼23.61, p¼ o0.001; Fig. 4a). Depth Thebigeyesixgillshark(H. nakamurai)wasthethirdmost (Logistic Regression r2¼0.42, χ2¼36.52, p¼ o0.001) and tempera- abundant species (n¼14). All field identifications of this species were ture (Logistic Regression r2¼0.39, χ2¼33.94, p¼ o0.001) both had confirmed with mtCOI sequences in the BOLD database. They were asignificant effect on the presence/absence of S. cubensis.Sexratios significantly more abundant less than 1500 m from the wall of the were slightly skewed but did not significantly diverge from an Exuma Sound (Contingency Analysis χ2¼7.23, p¼0.007; Fig. 4c), at expected 1:1 ratio (Chi Squared Test χ2¼1.47, p¼0.225) with a mean depth of 639.5 m (716.7 S.E.), and at a mean seabed females 1.4 times more abundant than males. Mature sharks were temperature of 11.5 1C(70.38 S.E.). Depth had a significant effect 2.6 times more abundant than immature sharks (Chi Squared Test on the presence/absence of H. nakamurai (Logistic Regression χ2¼10.67, p¼0.001). A significant logistic relationship (Logistic χ2¼4.94, p¼0.026), however, temperature did not (Logistic Regres- 2 2 Regression χ ¼16.36, p¼ o0.001) was established between LT sion χ ¼3.27, p¼0.070).Maleswere3.7timesmoreabundantthan and maturity for 13 mature and 9 immature male S. cubensis.Based females (Chi Squared Test χ2¼4.57, p¼0.033). Of the 11 males on this logistic function, 50% (M50) of the male population were captured, only one was immature which precluded the mathematical predicted to be mature at 54.4 cm LT (Range 49.1–57.9 cm LT). Two calculation of size-at-maturity, however, the smallest mature male female Cuban dogfish were recaptured after 30 and 579 days at captured was 131 cm LT, and the immature male measured 148 cm LT, liberty. No growth was detected for the animal at liberty for the suggesting the onset of male maturity occurs at approximately 130– shorter duration; however, the recapture point was 1373.5 m away 150 cm LT. from the initial capture location suggesting limited short term move- The presence/absence of the bluntnose sixgill shark (H. griseus) ments. The second animal, a 72 cm LT mature female when tagged, (n¼8, all genetically confirmed in the BOLD database), exhibited was recaptured by a sport fisherman and grew 1.8 cm LF yielding a no significant relationship with distance from the Exuma Sound 1 growth rate of 1.13 cm yr LF. There was no location data provided (Fig. 4d), or with temperature and depth. The mean capture depth for this recapture so linear dispersal could not be calculated. was 665.4 m (733.52 S.E.), and the mean seabed temperature was None of the Centrophorus species we collected were identifiable to 11.1 1C(70.86 S.E.), however, the range of these values were wide, the species level in the BOLD database. All of the sequences obtained 565–791 m and 8.2–13.8 1C. H. griseus exhibited an even sex ratio; were matched with certainty to the genus Centrophorus but all of however, immature animals outnumbered mature animals 3:1 them were very similar (9997% sequence match) to a range of although this was not a statistically significant difference (Chi reference specimens in the BOLD database. Not all of the mtCOI Squared Test χ2¼2.00, p¼0.157). sequences we obtained were identical, exhibiting from 0–1.1% pair- The insular subspecies of the smooth dogfish (M. canis insularis) wise sequence divergence. This suggests Exuma Sound may contain a (n¼7, all genetically confirmed in the BOLD database) was most complex of 2–3 weakly differentiated gulper shark species. A taxo- commonly encountered within 1000 m of the edge of the Exuma nomic revision is currently underway for the genus Centrophorus and Sound (Contingency Analysis χ2 ¼11.09, p¼0.049; Fig. 4e), at a is subsequently beyond the scope of this study (see White et al., 2013 mean depth of 549.7 (720.9 S.E.) m and at a mean seabed and Veríssimo et al., 2014). Consequently, for all further analysis all temperature of 14.1 1C(70.6 S.E.). Depth (Logistic Regression gulper shark specimens were grouped into a single species complex. r2 ¼0.30, χ2 ¼10.72, p¼0.001) and temperature (Logistic Regres- Centrophorus spp. (n¼51) were the second most commonly encoun- sion r2¼0.33, χ2 ¼11.75, p¼ o0.001) contributed significantly to tered group. Centrophorus spp. were significantly more abundant the presence/absence of M. canis insularis. This species exhibited 1000–2500 m from the wall of the Exuma Sound (Contingency an apparently skewed sex ratio with only one of the seven sharks Analysis χ2¼15.94, p¼0.007; Fig. 4b), in a mean water depth of captured being male but given the small sample size this was not 730.6 m (77.9 S.E.), and at a mean seabed temperature of 9.5 1C statistically significant (Chi Squared Test χ2 ¼3.57, p¼0.059). (70.17 S.E.). As Centrophorus spp. were most common at the inter- There was a roughly equal ratio of mature and immature animals mediate depths of our sampling distribution, the presence/absence (Chi Squared Test χ2¼0.14, p¼0.705). A single immature female dataset was bisected at the mean depth (730.6 m) and seabed (82 cm LT) M. canis insularis was recaptured after 62 days at temperature (9.5 1C) of capture. Separate logistic functions were fitted liberty; however, no growth was identified over this short dura- to the respective datasets which indicated that for values shallower tion. The distance between the capture and recapture locations and warmer than the mean, there was no significant relationship was 680 m, suggesting a degree of short term site fidelity. between presence/absence and depth (Logistic Regression r2¼0.07, The roughskin dogfish (C. owstoni)(n¼5, all genetically verified), χ2¼3.78, p¼0.052) or temperature (Logistic Regression r2¼0.07, was the deepest dwelling shark encountered during this project, χ2¼3.70, p¼0.054). However, for values deeper and colder than the captured at a mean depth of 888.3 m (739.6 S.E.) and a mean mean, there were significant relationships between depth (Logistic temperature of 7.3 1C(70.5S.E.).Thisspecieswascapturedalmost Regression r2¼0.33, χ2¼10.91, p¼0.001) and temperature (Logistic exclusively 3000–3500 m away from the wall of the Exuma Sound in Regression r2¼0.15, χ2¼5.47, p¼ o0.019). Sex ratios were signifi- the deepest portion of the study site (Contingency Analysis cantly skewed (Chi Squared Test χ2¼16.80, p¼ o0.001) whereby χ2¼17.44, p¼0.004; Fig. 4f). Depth (Logistic Regression females were 4.2 times more common than males. Maturity was not r2¼0.52, χ2¼12.87, p¼ o0.001) and temperature (Logistic Regres- assessed in this species complex given the multiple Centrophorus sion r2¼0.45, χ2¼11.19, p¼ o0.001) contributed significantly to the species encountered. presence/absence of C. owstoni. Three males and one female were

Fig. 4. Presence/absence mosaic plots of (A) S. cubensis, (B) Centrophorus spp., (C) H. nakamurai, (D) H. griseus, (E) M. canis insularis, and (F) C. owstoni in six 500 m wide zones, spatially stratiﬁed by distance from the wall of the Exuma Sound. Dissimilar letters above the bars indicate statistical signiﬁcance between levels derived from serial contingency analyses.

captured, however, given the small sample size statistical comparisons 3.3. Species diversity estimates were not made and ratios should be interpreted cautiously. The springer's sawtail catshark (G. springeri)(n¼3) was cap- Spearman Rank Correlation indicated that species richness tured at a mean depth of 706.8 m (764.03 S.E.) and a mean tem- declined signiﬁcantly with increasing depth (ρ¼0.242, p¼0.045), perature of 10.4 1C(71.46 S.E.). Two females and one male were and decreasing temperature (ρ¼0.288, p¼0.016) and increasing captured and all three specimens of G. springeri were thought to be distance from the wall of the Exuma Sound (ρ¼0.295, p¼0.014) mature. A single immature male false catshark (Pseudotriakis (Fig. 2). Examination of the species-accumulation plot revealed that microdon) was captured in 790.1 m of water at a seabed tempera- observed species richness, based on data from all deep-water longline ture of 8.7 1C. stations, was approaching an asymptote (Fig. 5).

3.4. Resilience to longline capture deep-water elasmobranchs. We captured 144 sharks from at least eight species in a relatively small area (10.5 km2) over 69 sets; Species-speciﬁcat-vesselmortalityratesacrossallspeciescom- however, the paucity of information pertaining to typical catch bined increased with mean capture depth (Spearman Rank Correlation rates in the region makes comparison with other areas challen- ρ¼0.77, p¼0.04; Table 2). The recapture of two S. cubensis and a ging. A comparison of coarse CPUE estimates for all species single M. canis insularis, two of the shallowest dwelling species, suggest combined suggests that catch rates in the Exuma Sound (0.027 that both are able to survive the combined insults of capture and sharks hook1 h1 70.003 S.E.) were 3.28 times greater than ascent, but exactly what proportion of those released survive is capture rates in Jamaica (0.008 sharks hook1 h1 70.002 S.E.) unknown. Post-release survivorship was estimated via satellite tele- where similar gear was used (McLaughlin and Morrissey, 2004;J. metry for Centrophorus spp. (n¼11), H. griseus (n¼3), and H. nakamurai Morrissey, unpublished data). Russell et al. (1988) described two (n¼2) (Table 3). Of the 16 PSATs deployed, only two reported via the research cruises off Puerto Rico during which bottom longlines Argos system, one deployed on H. griseus transmitted 88% of its dataset, were deployed. The number of deployments was not given and one PSAT on Centrophorus spp. transmitted a partial dataset prior however, catch rates in number of sharks per set, and the numbers to washing ashore. The latter PSAT was not recovered. In addition to of sharks per 100 hooks (irrespective of soak time) were provided. the partially transmitted Centrophorus spp. dataset, two further Cen- The two cruises captured a mean of 3 and 2 sharks per set, and a trophorus spp. PSATs were recovered after they washed ashore allowing mean of 6.4 and 4.2 sharks per 100 hooks respectively. The present the retrieval of the entire dataset. The data from all three Centrophorus study captured a mean of 2.84 (70.32 S.E.) sharks per set, spp. PSATs indicated that the sharks had been preyed upon almost comparable to the Puerto Rico cruises, and 9.51 sharks per 100 immediately post-release. This conclusion was based on (1) the hooks (71.07 S.E.), a much greater catch rate than Puerto Rico. instantaneous loss of light data in o200 m of water; (2) clear diurnal The two cruises yielded species richness estimates of 6.0 and vertical migrations and surfacing behaviour that is considered unchar- 8.0 respectively, similar to the estimates of the present study. In acteristic of a deep-water shark; and (3) the physical deterioration of the present study, the models used to extrapolate maximum the recovered PSATs as by a strong acid, thought to be stomach acid. species richness suggest that given an inﬁnite number of samples, The data transmitted by the PSAT deployed on H. griseus indicated that no more than one additional species would be recorded. This this individual survived and returned to normal diurnal vertical implies that the assemblages described by sampling efforts to date migrations approximately 60 h post-release. No PSATs deployed on H. are representative of the deep-water elasmobranch assemblage nakamurai either transmitted or were recovered. Table 4 present within the study area. The present study has yielded abundance and diversity estimates in the upper bounds of those generated by contemporary 4. Discussion studies in the region. It is possible that the north east of the Exuma Sound in particular might have a greater carrying capacity for The results of the present study suggest that the northeast Exuma Sound supports an abundant and diverse assemblage of Table 4 Summary of post-release survivorship in Centrophorus spp., Hexanchus griseus and H. nakamurai determined by pop-off satellite transmitters. DNR indicates that the tag did not report.

Species Length LT Sex Pop-off Transmission Fate (cm) duration

Centrophorus 102 F 5 Month DNR Unknown spp. Centrophorus 156 F 30 Day DNR Unknown spp. Centrophorus 152 F 30 Day Partial Predated spp. Centrophorus 80 F 30 Day Recovered Predated spp. (Full) Centrophorus 146 F 30 Day DNR Unknown spp. Centrophorus 96 F 30 Day DNR Unknown Fig. 5. Species accumulation curves which contain both the observed species spp. richness (Sobs) and five (Bootstrap, Chao1, Chao2, Jacknife1, and Jacknife2) species Centrophorus 85 M 4 Month DNR Unknown richness extrapolators used to predict diversity given an infinite number of samples spp. (Clarke and Gorley, 2006). Centrophorus 101 F 30 Day DNR Unknown spp. Centrophorus 149 F 30 Day DNR Unknown Table 3 spp. Rank order of species-specific at-vessel mortality rates. Mortality increased Centrophorus 100 F 6 Month Recovered Predated significantly with mean capture depth (Spearman Rank Correlation ρ¼0.77, spp. (Full) p¼0.04). Centrophorus 94 F 4 Month DNR Unknown spp. Rank Species nM% Mortality Mean capture depth (m) Hexanchus 340 M 30 Day Full Survived griseus 1 Centroscymnus owstoni 5 4 80.00 888.3 Hexanchus 389 F 5 Month DNR Unknown 2 Galeus springeri 3 2 66.67 706.8 griseus 3 Centrophorus spp. 51 15 29.41 731.4 Hexanchus 306 F 5 Month DNR Unknown 4 Squalus cubensis 55 5 9.09 581.8 griseus 5 Hexanchus nakamurai 14 1 7.14 639.5 Hexanchus 155 M 4 Month DNR Unknown 6 Hexanchus griseus 8 0 0.00 665.4 nakamurai 7 Mustelus canis insularis 7 0 0.00 549.7 Hexanchus 144 M 6 Month DNR Unknown 8 Pseudotriakis microdon 1 0 0.00 790.1 nakamurai

Please cite this article as: Brooks, E.J., et al., First description of deep-water elasmobranch assemblages in the Exuma Sound, The Bahamas. Deep-Sea Res. II (2015), http://dx.doi.org/10.1016/j.dsr2.2015.01.015i E.J. Brooks et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎ 9 deep-water organisms given the strong (90 cm s1), highly taxonomy remains unresolved and may include some endemic species directional surface current that flows on and off the shelf in the with limited ranges, as well as, circumglobal species complexes area (Rankey and Reeder, 2011), that likely delivers greater food composed of described and undescribed species. A complete morpho- fall from the shallow water and terrestrial ecosystems than in metric and genetic taxonomic revision of this genus is currently other parts of the sound. The importance of shallow water and underway (see White et al., 2013 and Veríssimo et al., 2014). terrestrial primary production for deep-water ecosystems, in areas Unfortunately this study was undertaken prior to robust morpho- where the continental shelf is very narrow has yet to be investi- metric and genetic markers being available, and it was impossible to gated. Further investigation by comparative sampling in areas assign identifications to the species level for each of our specimens. where similar surface currents do not exist, and/or through the Thefewsampleswewereabletocontributetotheongoingworkof use of stable isotope analysis (e.g. Pethybridge et al., 2012; Hussey Veríssimo and colleagues indicates that Centrophorus cf. uyato, Cen- et al., 2012), is recommended. trophorus granulosus and a new species of Centrophorus yet to be The distribution of some species encountered during the present described are present within the Exuma Sound assemblage (C. Cotton, study diverged from temperature and depth ranges established in the personal communication). The unfortunate consequence of this lack of literature. S. cubensis is reported to inhabit the waters of the western species-specificidentification is the limited inferences that can be Atlantic, greater Caribbean and Gulf of Mexico from North Carolina to drawn from the current dataset about this poorly understood group. southern Brazil, Argentina and Venezuela (Castro, 2011; Compagno, All depth and temperature ranges, sex ratios presented herein should 1984; McLaughlin and Morrissey, 2004; Russell et al., 1988). Capture be treated cautiously. depths for S. cubensis rangedfrom472.6mto730.6m,fargreaterthan One interesting component of the Centrophorus spp. complex the 60–380 m previously reported by Compagno (1984), the slightly and H. nakamurai were the significantly skewed sex ratios. Demo- increased range of 110–500 m reported by Castro (2011) or the 50– graphic segregation is considered normal for many populations of 459 m reported by Jones et al. (2013). This variation in depth shallow water elasmobranchs (Mucientes et al., 2009; Springer, association is likely attributable to geographical variation in thermal 1967; Speed et al., 2012), and has also been reported in many profiles of the water column. Menni et al. (2010) report a depth range deep-water species (Girard and Du Buit, 1999; Moura et al., 2014). of 30–350 m and a thermal range of 4.83–21.6 1CforS. cubensis from Segregation within Centrophorus spp. is unsurprising as female- the temperate waters off the south east coast of South America. This dominated populations of Centrophorus cf. uyato in the Cayman depth range does not overlap at all with the ranges reported in the Trench (McLaughlin and Morrissey, 2004), and a male-dominated present study, however, the thermal ranges match relatively closely. population of Centrophorus squamosus off the northwest coast of The mid-point of the thermal range reported by Menni et al. (2010) is Spain (Bañón et al., 2006) have previously been reported, suggest- 13.2 1C which is close to the mean capture temperature in the present ing that this is a normal occurrence within this genus. This is study of 12.99 1C. Furthermore the thermal range in the Exuma Sound supported by the apparent consistent segregation across multiple also falls within the larger range reported in the south western Centrophorus species in the present study. This is the first instance Atlantic. This suggests that S. cubensis select vertical habitat based that sexual segregation has been reported in populations of H. on thermal rather than barometric or photic preferences leading to nakamurai. Marginal sexual segregation was identified in S. cuben- the disparate depth ranges in different latitudes, and may account for sis, however, it was not statistically significant. S. cubensis has the divergent reporting in the literature. previously been reported to form large schools stratified by size Expanded depth ranges were also found for H. nakamurai,aspecies and sex (Castro, 2011), and it is interesting to note that Daly-Engel thought to inhabit the deep continental slope and have a circumglobal et al. (2010) reported strong sexual segregation in a congener, distribution (Ebert et al., 2013). Originally described in 1969, it was Squalus cf. mitsukurii. noted to occur from 90 m to 350 m with the possibility of being Significantly skewed ratios of mature and immature animals were present at deeper depths that were undersampled (Springer and identified in S. cubensis and H. nakamurai.InS. cubensis, this could be Waller, 1969). More recently, twenty-two H. nakamurai were captured due to the ontogenetic shift in habitat use reported by Sadowsky and off Puerto Rico between depths of 69 and 589 m (Russell et al., 1988), Moreira (1981), whereby immature animals inhabit shallower waters and a single H. nakamurai from 430 m off the coast of Jamaica than their mature conspecifics; S. cubensis is thought to be 25–27 cm

(J. Morrissey, unpublished data). Castro (2011) expanded the depth LT at birth (Castro, 2011), and the smallest specimen captured in the range to 200–500 m, however, all of these published depth ranges are present study was 45 cm LT, which could support these observations, shallower than the capture records in the present study which ranged but could also be a function of susceptibility to capture on longlines from504.1mto701.5m.Itispossiblethat H. nakamurai follow a for smaller animals. The smallest animal captured across all species similar thermally-driven vertical distribution as S. cubensis, however, was G. springeri at 31 cm LT which might be an indication that there are no temperature data from other geographic regions within individuals smaller than this cannot easily ingest the smallest (10/0) the literature to which comparisons can be made. H. nakamurai is the hook, or could simply be due to lack of animals smaller than this in only species which exhibited diurnal variation in catch rates. Diel the study area. In contrast, H. nakamurai are born at 40–43 cm LT,well vertical migration is well established in H. griseus (Andrews et al., within the range of longline catchability which may indicate ontoge- 2009; Comfort and Weng, this issue),anditispossiblethatsimilar netic segregation given that the smallest individual captured was behaviours exist in H. nakamurai which could account for these 111 cm LT, over double the size at birth. The segregation of populations differences. by size and sex has important management and conservation It should be noted that depth and/or temperature ranges estab- considerations, as the imposition of fisheries mortality on a specific lished in the present study did not depart from those already demographic can skew sex ratios, which disproportionally affects the established in the literature for H. griseus (Andrews et al., 2009; reproductive capacity of the entire stock (Mucientes et al., 2009; Field Castro, 2011), M. canis insularis (Heemstra, 1997), C. owstoni (Yano and et al., 2009). Tanaka, 1983; Yano and Tanaka, 1988), G. springeri (Konsta- The present study estimated size-at-maturity estimates for male ntinou and Cozzi, 1998; McLaughlin and Morrissey, 2004)or S. cubensis (M50 ¼54.4 cm; Range 49.1–57.9 cm LT), and H. nakamurai P. microdon (Castro, 2011). (130–150cm).Thisconformstothesinglerecordofmaturityfora Robust identification of gulper sharks (Centrophorus spp.) repre- male H. nakamurai by Castro (2011) who examined a 144 cm mature sented a significant challenge in this study. Species within the genus male, however, it is not stated if this measurement is LT or LF.Thesize- Centrophorus are found in tropical and temperate oceans throughout at-maturity estimate for S. cubensis does not conform to the most the world (Kyne and Simpfendorfer, 2010). However, the alpha recent and comprehensive study into their reproductive biology

to-date. Jones et al. (2013) reported M50 for male S. cubensis of 37.9 cm individuals survive the combined threats of capture, ascent, decent LSTL (Stretched Total Length which corresponds to LT in the present and post-release predation, it is unknown if they can survive the study), 16.5 cm smaller than our estimates. Our estimates corre- long-term effects of extreme physiological stress of capture. Based sponded better with estimates of Castro (2011) who suggested on these low chances of survival, traditional ﬁsheries management

45 cm LT and Compagno (1984) who indicated 50 cm LT,however, techniques (e.g. mandated release of prohibited species), are all of these estimates were based on a single citation (Bigelow and unlikely to be effective in reducing population mortality in many Schroeder, 1948), which used a single mature male to generate this species of deep-water shark. estimate (Jones et al., 2013). Other than the disparate size at maturity Our results illustrate the benefits of conducting deep-ocean res- estimates, the striking differencebetweenthepresentstudyandthe earch in areas where bathymetric structure results in narrow con- work of Jones et al. (2013) is the size ranges of the males they tinental shelves and research that can be undertaken over wider examined (20.4–46.6 cm LSTL) compared to the much larger males temporal scales at comparatively low cost. Targeted investigation in found in the Exuma Sound (45–64 cm LT). These substantial disparities these specific areas, in combination with traditional ocean-going res- seem to indicate massive regional variation in the growth and maturity earch which can encompass the spatial scale of these widely dis- patterns of S. cubensis which warrant further investigation. tributed species, may accelerate the acquisition of data and facilitate In general, survivorship in this study was low, but varied consider- effective management and conservation of deep-sea sharks. ably by species. The correlation of at-vessel mortality rates with mean capture depth is likely a combination of two scenarios. Firstly, the magnitude of thermal, barometric and photic stress, which increases Acknowledgments with depth, is a major contributor to at-vessel mortality; and secondly, that deeper dwelling species are inherently more sensitive to the We thank the numerous hard working volunteers including, physiological and physical trauma of capture. The instances of scavenger but not limited to Stephanie Liss, Alexandra Pickard, Gabe Wofford, damage in moribund animals was high amongst the deeper dwelling Aaron Shultz and Ian Hamilton. Thanks must also go to the hard species, in particular C. owstoni (75%), suggesting that these indivi- working Island School shark research students of Fall 2010 and Fall duals succumbed to the stress of capture alone, though depth-mediated 2011 including Taylor Schendel, Liam Donavan, Aubrey Faggen, differences in scavenger abundance may also affect this. In addition to Clay Bales, Dorothy Long, Aly Boyce, Devin Caccavaro, Jane Drin- fi the correlation between depth and mortality, the recaptures of a single kard, Anna Belk, Erik Can eld, James Murray, and Carter Wight, fi M. canis insularis and two S. cubensis, the two shallowest dwelling who also provided invaluable eld support. This work would not species, further suggest that shallower species are more resilient to the have been possible without the support of the Cape Eleuthera combined insults of capture and ascent from depth. It is thought that Foundation. post-release survivorship in Centrophorus spp. was low based on the almost immediate predation (o200 m from the surface) of all three Appendix A. Supplementary Information individuals fitted with a PSAT where data were recovered, and the high (30%) at-vessel-mortality rates. However, it is at present unknown if Supplementary data associated with this article can be found in this high post-release predation rate is consistent across individuals the online version at http://dx.doi.org/10.1016/j.dsr2.2015.01.015. without PSATs attached, or across the different species within the species complex. 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