Bone Density Variation in Rattails (Macrouridae,Gadiformes): Buoyancy, Depth, Body Size, and Feeding

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author's publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.Extreme abiotic factors in deep-sea environments, such as near-freezing temperatures, low light, and high hydrostatic pressure, drive the evolution of adaptations that allow organisms to survive under these conditions. Pelagic and benthopelagic fishes that have invaded the deep sea face physiological challenges from increased compression of gasses at depth, which limits the use of gas cavities as a buoyancy aid. One adaptation observed in deep-sea fishes to increase buoyancy is a decrease of high-density tissues. In this study, we analyze mineralization of high-density skeletal tissue in rattails (family Macrouridae), a group of widespread benthopelagic fishes that occur from surface waters to greater than 7000 m depth. We test the hypothesis that rattail species decrease bone density with increasing habitat depth as an adaptation to maintaining buoyancy while living under high hydrostatic pressures. We performed micro-computed tomography (micro-CT) scans on 15 species and 20 specimens of rattails and included two standards of known hydroxyapatite concentration (phantoms) to approximate voxel brightness to bone density. Bone density was compared across four bones (eleventh vertebra, lower jaw, pelvic girdle, and first dorsal-fin pterygiophore). On average, the lower jaw was significantly denser than the other bones. We found no correlation between bone density and depth or between bone density and phylogenetic relationships. Instead, we observed that bone density increases with increasing specimen length within and between species. This study adds to the growing body of work that suggests bone density can increase with growth in fishes, and that bone density does not vary in a straightforward way with depth

Marine fish may be biochemically constrained from inhabiting the deepest ocean depths

No fish have been found in the deepest 25% of the ocean (8,400-11,000 m). This apparent absence has been attributed to hydrostatic pressure, although direct evidence is wanting because of the lack of deepest-living species to study. The common osmolyte trimethylamine N-oxide (TMAO) stabilizes proteins against pressure and increases with depth, going from 40 to 261 mmol/kg in teleost fishes from 0 to 4,850 m. TMAO accumulation with depth results in increasing internal osmolality (typically 350 mOsmol/kg in shallow species compared with seawater\u27s 1,100 mOsmol/kg). Preliminary extrapolation of osmolalities of predicted isosmotic state at 8,000-8,500 m may indicate a possible physiological limit, as greater depths would require reversal of osmotic gradients and, thus, osmoregulatory systems. We tested this prediction by capturing five of the second-deepest known fish, the hadal snailfish (Notoliparis kermadecensis; Liparidae), from 7,000 m in the Kermadec Trench. We found theirmuscles to have a TMAOcontent of 386 ± 18 mmol/kg and osmolality of 991 ± 22 mOsmol/kg. These data fit previous extrapolations and, combined with new osmolalities from bathyal and abyssal fishes, predict isosmotic state at 8,200 m. This is previously unidentified evidence that biochemistry could constrain the depth of a large, complex taxonomic group

Trophic interactions of megafauna in the Mariana and Kermadec trenches inferred from stable isotope analysis

Hadal trenches house distinct ecosystems but we know little about their sources of nutrition or trophic structures. We evaluated megafaunal food web structure and nutritional sources in the Kermadec and Mariana trenches using carbon and nitrogen stable isotope analysis (δ15N and δ13C values) of bulk tissues and proteinaceous individual amino acids (AAs). In the Kermadec Trench, bulk δ15N values ranged from 5.8‰ in trench sediment to 17.5‰ in tissues of the supergiant amphipod, Allicela gigantea. δ15N values of detritivores were much higher than those of sediments (by 7.5‰ more). The δ13C values ranged from −21.4‰ in sediments to −17.3‰ in the brittle star, Ophiolimna sp., and did not co-vary with δ15N values. In the Mariana Trench, only bait-attending fauna and surface sediments were available for analysis. Mariana Trench fishes, amphipods, and sediments had slightly lower δ15N values than those from the Kermadec Trench, possibly because the Mariana Trench lies under more oligotrophic surface waters. We found evidence for multiple food inputs to the system in each trench, namely substantially higher δ15N values in detritivores relative to sediment and high variability in δ13C values. Trophic levels determined from isotopic analysis of individual AAs in the Kermadec Trench ranged from three for detritivores to five for fishes. Source AA δ15N values were variable (range of ~7.0‰ in average δ15N source AA values), with much of this variation occurring in small amphipods. For the other fauna sampled, there was a significant increase in δ15N source AA values with increasing collection depth. This increase could reflect larger amounts of highly microbially reworked organic matter with increasing depth or sporadic input from turbidity flows. Although further sampling across a broader faunal diversity will be required to understand these food webs, our results provide new insights into hadal trophic interactions and suggest that trench food webs are very dynamic

Fishes of the hadal zone including new species, in situ observations and depth records of Liparidae

AbstractObservations and records for fish exceeding 6000m deep are few and often spurious. Recent developments in accessing and sampling the hadal zone 6000–11,000m) have led to an acceleration in new findings in the deep subduction trenches, particularly in the Pacific Ocean. This study describes the discovery of two new species of snailfish (Liparidae) from the Mariana Trench; the ‘Mariana snailfish’ (6198–8076m) and the ‘Ethereal snailfish’ (7939–8145m). These new findings represent respectively the deepest known specimen caught with corroborating depth data, and the deepest fish seen alive. Further specimens and observations of the Kermadec Trench snailfish, Notoliparis kermadecensis, are also presented, as well as the first hadal records of Synaphobranchidae and Zoarcidae (6068 and 6145m respectively) and a depth extension for the Macrouridae (maximum depth now 7012m). Details of these new snailfish specimens caught by baited trap and behaviour observations filmed by baited cameras are presented. An updated assessment of fishes from hadal depths is also reported

Distribution, composition and functions of gelatinous tissues in deep-sea fishes

Many deep-sea fishes have a gelatinous layer, or subdermal extracellular matrix, below the skin or around the spine. We document the distribution of gelatinous tissues across fish families (approx. 200 species in ten orders), then review and investigate their composition and function. Gelatinous tissues from nine species were analysed for water content (96.53 ± 1.78% s.d.), ionic composition, osmolality, protein (0.39 ± 0.23%), lipid (0.69 ± 0.56%) and carbohydrate (0.61 ± 0.28%). Results suggest that gelatinous tissues are mostly extracellular fluid, which may allow animals to grow inexpensively. Further, almost all gelatinous tissues floated in cold seawater, thus their lower density than seawater may contribute to buoyancy in some species. We also propose a new hypothesis: gelatinous tissues, which are inexpensive to grow, may sometimes be a method to increase swimming efficiency by fairing the transition from trunk to tail. Such a layer is particularly prominent in hadal snailfishes (Liparidae); therefore, a robotic snailfish model was designed and constructed to analyse the influence of gelatinous tissues on locomotory performance. The model swam faster with a watery layer, representing gelatinous tissue, around the tail than without. Results suggest that the tissues may, in addition to providing buoyancy and low-cost growth, aid deep-sea fish locomotion. © 2017 The Authors

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Pseudoliparis swirei sp. nov.: A newly-discovered hadal snailfish (Scorpaeniformes: Liparidae) from the Mariana Trench

Gerringer, Mackenzie E., Linley, Thomas D., Jamieson, Alan J., Goetze, Erica, Drazen, Jeffrey C. (2017): Pseudoliparis swirei sp. nov.: A newly-discovered hadal snailfish (Scorpaeniformes: Liparidae) from the Mariana Trench. Zootaxa 4358 (1): 161-177, DOI: https://doi.org/10.11646/zootaxa.4358.1.

Pseudoliparis swirei Gerringer & Linley & Jamieson & Goetze & Drazen 2017, sp. nov.

Pseudoliparis swirei Gerringer & Linley sp. nov. Figures 2, 3, 4, 5; Tables 2, 3 Mariana snailfish: Linley et al. 2016 (page 105, Figure 4a) Mariana snailfish: Linley et al. 2017 (page 42, Figure 6.43) Mariana snailfish/Mariana liparid: Gerringer et al. 2017a (page 111) Mariana liparid/ Liparidae sp. nov: Gerringer et al. 2017b (page 137) Diagnosis. Andriashev and Pitruk (1993) define the genus Pseudoliparis as having a well-developed disk and one pair of nostrils and lacking pseudobranchia and pleural ribs, with four radials in the pectoral girdle, which has neither notches nor fenestrae. In this genus, the hypural plate is divided by a distal slit (Andriashev and Pitruk, 1993). Like the other in this genus, Pseudoliparis swirei sp. nov. (Figures 2, 3) displays these characters, including a moderately well-developed disk, although this is easily damaged in collection. Pseudoliparis swirei sp. nov. can be distinguished from the two other known Pseudoliparis species with the following characters. Pseudoliparis swirei sp. nov. differs from P. belyaevi in the presence of a distinct lower pectoral-fin lobe, similar to that seen in P. amblystomopsis (Andriashev, 1955). Pseudoliparis swirei has more dorsal-fin rays 55 (51–58) than P. amblystomopsis 49 (49–52), more anal-fin rays 48 (43–49) compared to 43 (42–45), and more vertebrae 61 (56– 62), compared to 55–57, although these ranges somewhat overlap. Head length is shorter in P. swirei sp. nov. (17.0–21.7 %SL) than P. amblystomopsis (21.6–24.0 %SL). Comparisons were made according to ranges presented by Andriashev & Pitruk (1993). Pseudoliparis belyaevi is known only from the Japan Trench, P. amblystomopsis from the Japan and Kurile-Kamchatka trenches, P. swirei only from the Mariana Trench. Description. Vertebrae 61 (56–62), dorsal-fin rays 55 (51–58), anal-fin rays 48 (43–49), caudal-fin rays 13 (11–14), pectoral-fin rays 30 (28–32), pectoral radials 4, pyloric caeca 7 (5–9). Ranges of measurements and counts are presented in Table 2. Ratios are presented in Table 3. All individual measurements and counts are available in Supplementary Table 1. Micro-CT scans and a 3D rotatable model of the holotype are available in the Supplementary Material. Head small, low, and wide, lateral profile anteriorly rounded and rising slowly to occiput, where the angle increases. Head depth about equal to body depth or lower, depending on abdominal fullness. Snout blunt, nostrils single, nares on horizontal with center of eye. Mouth broad, horizontal, subterminal, moderately large; upper jaw reaching to below middle of orbit, oral cleft reaching to below anterior edge of orbit. Teeth simple, sharp canines, innermost largest, arranged in approximately 9 (6–11 maxilla, 7–13 mandible) oblique, irregular rows of up to 20 (6–17 maxilla, 8–20 mandible) teeth each, forming a moderately wide band (2–4 teeth wide) in each jaw (Figure 4). Larger individuals had more teeth per row and more rows of teeth. Maxilla with prominent symphyseal gap, slight gap present in mandible. Pharyngeal teeth well developed, long, sharp, strongly fixed on globular tooth plates. Eye very small, about 10% head length. Orbit large, its dorsal margin well below that of head. Gill opening small, located completely above pectoral fin, width 5% SL. Opercular flap fleshy, broadly triangular, opercle terminates in two small spines below the flesh. Cephalic pores small, easily damaged; few remaining. Eight widely separated infraorbital and mandibular pores, lacking raised rims. In fresh specimens, the infraorbital and mandibular pores appear sunken and anteriorly orientated within the gelatinous tissue of the head (Figure 4). Pectoral fin divided into lobes by a moderately deep notch, rudimentary rays absent. Notch rays 5 (3–6), clearly more widely spaced than those of upper and lower lobes, more so in larger individuals. Upper and lower lobe rays closely spaced. Dorsal-most pectoral-fin ray on horizontal between level of upper jaw and lower margin of orbit. Symphysis of pectoral fins and anteriormost ray below rear of orbit. Upper lobe about 15.2% SL (12.6– 19.8), lower about 7.8% SL (6.3–12.1). Upper lobe almost extending to anal-fin origin, lower lobe distinct, reaching well behind disk to below middle of upper lobe base. Pectoral radials four, fenestra absent; of four specimens examined (USNM 438996/ HADES 200024, USNM 438994/ HADES 200027, USNM 438997/ HADES 200033, USNM 438989/ HADES 200096); one (USNM 438996 HADES 200024) had (1+1+1+1), and three (USNM 438994/ HADES 200027, USNM 438997/ HADES 200033, USNM 438989/ HADES 200096) had (3+1) radials, generally round, notches and foramina absent (Figure 5). Radials gradually and irregularly decreasing in size from R1 (largest) to R4 (smallest). Distal radials present under the base of all rays, with the exception of the two most ventral rays (Supplementary Figure 1). Scapula double-headed, posterior head larger and broader than anterior head, coracoid with broad head and long slender helve. %SL %HL Holotype Holotype and Paratypes n Holotype Holotype and Paratypes n Fresh Head Length 20.6 14.5–21.9 (18.7±1.8) 33 Snout Length 7.2 4.3–9.3 (6.4±1.0) 33 35.0 26.3–45.5 (33.8±5.3) 37 Eye Width 2.1 0.9–2.9 (1.8±0.5) 33 10.0 5.3–15.4 (9.9±2.4) 37 Body Depth 18.6 18.6–31.2 (24.5±3.1) 18 90.0 90.0–156.8 (128.7±17.9) 18 Preanal Fin Length 37.1 36.5–49.5 (42.0±3.5) 33 180.0 180.0–295.8 (228.0±26.1) 37 Disk present, oval, longer than wide, below cheek and gill cavity between pectoral fin notches; well behind pectoral symphysis. Bones fully developed but weakly calcified; all elements present. Disk and pectoral girdle supported by a pair of clearly visible and strongly developed muscles extending anteriorly to pectoral symphysis, probably infracarinalis anterior (D.L. Stein, personal communication). Disk structure supporting a thin layer of tissue, often damaged or missing entirely; disk margin only slightly thicker than more central tissue. In cross section, disk rays clearly flattened as if to support disk margin. Body depth dependent on reproductive state and fullness of stomach, usually much deeper than head depth, but shallow above vertebral column. Abdominal cavity long; peritoneum and body cavity extending to about 40% standard length. Total vertebrae 61 (56–62); anterior 13 (11–14), caudal 46 (44–49). In the 19 individuals in good enough condition to be radiographed, a double ray is present at or near anal fin first ray, usually between the second and third haemal spines of the caudal vertebrae. Pre-dorsal length about 27% SL (18.6–32.6), dorsal fin origin between fourth and fifth vertebrae (origin after vertebrae 3–5). Pre-anal-fin length about 42% SL (36.3–49.5)*. Anus far posterior to disk, roughly 2/3 of distance from disk to anal fin origin. Pyloric caeca usually 7 (5–9), located left ventrally in body cavity; thick, digitate, usually separated into two distinct size classes, most commonly 4 short and 3 long, longest about 8.7% SL (5.9–11.7), shortest 3.7% SL (2.4–5.3). Longer caeca generally grouped together. Hypural with obvious suture; caudal fin most commonly of 13 (11–14) rays, ventral one or two often rudimentary. Skin thin, transparent; subdermal extracellular matrix (SECM; Eastman et al. 1994) thick below skin and between muscle bands. Total and standard lengths were approximately 10% shorter after preservation. The subdermal extracellular matrix is also lost after capture and preservation, resulting in changes to shape and proportion (Gerringer et al. unpublished data). With increased use of visual in situ techniques, reporting of both fresh and preserved specimen features will become increasingly useful. The 37 individuals used for description varied in size from 89–235 mm SL, apparently covering a wide developmental range for the species. Some characters correlated significantly with ontogeny, explaining much of the variation in ratios. Both the upper and lower pectoral-fin lobe lengths as a percentage of SL decreased significantly with increasing SL (upper: F1,25=11.88, p74% ML bootstrap support,>0.96 Bayesian posterior probability), with highly concordant topology. Genetic distances between the two species of Pseudoliparis are 0.6% at Cyt- b and 0.7% at 16S rRNA (Table 4), with distances of 1– 1.4% (Cyt- b) and 0.8–1% (16S rRNA) to the Notoliparis species. COI lacked sufficient polymorphism to resolve the relevant nodes, with low bootstrap support observed for the placement of P. swirei sp. nov. relative to P. belyaevi and N. kermadecensis (Figure 6). Genetic distances among species also were the lowest at COI, at 5 mm) and up to 851 small eggs of less than half the diameter of the larger size class. There were rarely intermediate stages (Figure 7). Individuals with only small eggs had maximum egg sizes ranging from 0.7 to 1.4 mm. Genital papilla visible in freshly collected males, oriented anteriorly. Distribution. Known only from the Mariana Trench at capture depths from 6,898–7,966 m, individuals likely this species were recognized in video at depths 6,198–8,098 m (Linley et al. 2016; Jamieson & Linley, unpublished data). Etymology. The Mariana Trench famously houses the ocean’s deepest point, at Challenger Deep, named for the HMS Challenger expedition which discovered the trench in 1875. Their deepest sounding of 8,184 m, then the greatest known ocean depth, was christened Swire Deep after Herbert Swire, the ship’s First Navigating Sublieutenant (Corfield 2003). We name this fish in his honor, in acknowledgment and gratitude of the crew members that have supported oceanographic research throughout history.Published as part of Gerringer, Mackenzie E., Linley, Thomas D., Jamieson, Alan J., Goetze, Erica & Drazen, Jeffrey C., 2017, Pseudoliparis swirei sp. nov.: A newly-discovered hadal snailfish (Scorpaeniformes: Liparidae) from the Mariana Trench, pp. 161-177 in Zootaxa 4358 (1) on pages 164-170, DOI: 10.11646/zootaxa.4358.1.7, http://zenodo.org/record/106755