Christopher P. Kenaley

Additional Records of Deep-sea Fishes from off Greater New England

Abstract A recent review of deep-sea fishes captured deeper than 200 m off greater New England, from the Scotian Shelf at 44°N to the southern New England Shelf at about 38°N, documented 591 species. Subsequent trawling activity and reviews of deep-sea taxa occurring in the area have revealed that an additional 40 species inhabit the deep sea off New England. Thirty-two of these new records were captured in the course of 44 bottom trawls and 94 mid-water trawls over or in the proximity of Bear Seamount (39°55′N, 67°30′W). Five of the 40 species have been described as new to science, at least in part from material taken in the study area. In addition to describing such information as specimen size and position, depth, and date of capture, errors made in the previous study of deep-sea fishes in the area are identified and corrected.

THE COMPLEX EVOLUTIONARY HISTORY OF SEEING RED: MOLECULAR PHYLOGENY AND THE EVOLUTION OF AN ADAPTIVE VISUAL SYSTEM IN DEEP-SEA DRAGONFISHES (STOMIIFORMES: STOMIIDAE)

The vast majority of deep‐sea fishes have retinas composed of only rod cells sensitive to only shortwave blue light, approximately 480–490 nm. A group of deep‐sea dragonfishes, the loosejaws (family Stomiidae), possesses far‐red emitting photophores and rhodopsins sensitive to long‐wave emissions greater than 650 nm. In this study, the rhodopsin diversity within the Stomiidae is surveyed based on an analysis of rod opsin‐coding sequences from representatives of 23 of the 28 genera. Using phylogenetic inference, fossil‐calibrated estimates of divergence times, and a comparative approach scanning the stomiid phylogeny for shared genotypes and substitution histories, we explore the evolution and timing of spectral tuning in the family. Our results challenge both the monophyly of the family Stomiidae and the loosejaws. Despite paraphyly of the loosejaws, we infer for the first time that far‐red visual systems have a single evolutionary origin within the family and that this shift in phenotype occurred at approximately 15.4 Ma. In addition, we found strong evidence that at approximately 11.2 Ma the most recent common ancestor of two dragonfish genera reverted to a primitive shortwave visual system during its evolution from a far‐red sensitive dragonfish. According to branch‐site tests for adaptive evolution, we hypothesize that positive selection may be driving spectral tuning in the Stomiidae. These results indicate that the evolutionary history of visual systems in deep‐sea species is complex and a more thorough understanding of this system requires an integrative comparative approach.

A revision of Atlantic species of Photostomias (Teleostei: Stomiidae: Malacosteinae), with a description of a new species

While one or possibly two species of the genus Photostomias have been recognized, an unpublished revision of the Malacosteinae suggested that there may be as many as six species worldwide. Our review of museum material revealed three taxa in the Atlantic alone: Photostomias atrox Alcock, 1890; Photostomias guernei Collett, 1889; and a new species described herein. Because of a paucity of Indo-Pacific material and a need to better document Atlantic biodiversity, we treat only the Atlantic species at this time. A key to the identification of Atlantic Photostomias is given.

A biorobotic adhesive disc for underwater hitchhiking inspired by the remora suckerfish

A multimaterial biomimetic remora disc attaches to a variety of surfaces and enables underwater hitchhiking. Remoras of the ray-finned fish family Echeneidae have the remarkable ability to attach to diverse marine animals using a highly modified dorsal fin that forms an adhesive disc, which enables hitchhiking on fast-swimming hosts despite high magnitudes of fluid shear. We present the design of a biologically analogous, multimaterial biomimetic remora disc based on detailed morphological and kinematic investigations of the slender sharksucker (Echeneis naucrates). We used multimaterial three-dimensional printing techniques to fabricate the main disc structure whose stiffness spans three orders of magnitude. To incorporate structures that mimic the functionality of the remora lamellae, we fabricated carbon fiber spinules (270 μm base diameter) using laser machining techniques and attached them to soft actuator–controlled lamellae. Our biomimetic prototype can attach to different surfaces and generate considerable pull-off force—up to 340 times the weight of the disc prototype. The rigid spinules and soft material overlaying the lamellae engage with the surface when rotated, just like the discs of live remoras. The biomimetic kinematics result in significantly enhanced frictional forces across the disc on substrates of different roughness. Using our prototype, we have designed an underwater robot capable of strong adhesion and hitchhiking on a variety of surfaces (including smooth, rough, and compliant surfaces, as well as shark skin). Our results demonstrate that there is promise for the development of high-performance bioinspired robotic systems that may be used in a number of applications based on an understanding of the adhesive mechanisms used by remoras.

Skating by: low energetic costs of swimming in a batoid fish

ABSTRACT We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s−1, we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT–speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances. Summary: The little skate exhibits decreasing mass-adjusted swimming metabolic rates with increasing speed, which are the lowest values among elasmobranchs. However, its cost of transport is one of the highest measured for fishes.

Revision of the Manefish Genus Paracaristius (Teleostei: Percomorpha: Caristiidae), with Descriptions of a New Genus and Three New Species

Abstract The family Caristiidae, commonly known as manefishes or veilfins, includes seven species of mesopelagic, oceanic fishes found throughout the major ocean basins of the world. We present a partial revision of the family, including all of the “small mouth” species, which are distinguished from other species of the family by having an upper jaw that extends approximately to midorbit and is almost completely covered by the thin bones of the suborbital series, a broad suborbital space, and by the lack of palatine teeth. This group, previously thought to include only the genus Paracaristius, is described in full, including the establishment of a new genus and three new species. The new genus Neocaristius includes only Neocaristius heemstrai, a distinctive species that is distinguished from all other species in this group by dentition, lateral-line morphology, dorsal-fin origin, and orbit size, as well as other meristic and morphometric characters. Neocaristius heemstrai is a circumaustral species, known from the South Atlantic, South Pacific, and southern Indian Ocean. The genus Paracaristius includes four species, P. maderensis and three species newly described herein. Species of Paracaristius are distinguished from each other on the basis of meristics, dentition, presence or absence of papillae on the hyoid arch, and placement of the dorsal fin. Two species of Paracaristius, P. nemorosus, new species, and P. aquilus, new species, are apparently resticted to the eastern tropical Atlantic, while the other two, P. nudarcus, new species, and P. maderensis are more widespread.

Comparative Innervation of Cephalic Photophores of the Loosejaw Dragonfishes (Teleostei: Stomiiformes: Stomiidae): Evidence for Parallel Evolution of Long-Wave Bioluminescence

Four genera of the teleost family Stomiidae, the loosejaw dragonfishes, possess accessory cephalic photophores (AOs). Species of three genera, Aristostomias, Malacosteus, and Pachystomias, are capable of producing far‐red, long‐wave emissions (>650nm) from their AOs, a character unique among vertebrates. Aristostomias and Malacosteus posses a single far‐red AO, while Pachystomias possesses anterior and posterior far‐red AOs, each with smaller separate photophores positioned in their ventral margins. The purpose of this study was to establish the primary homology of the loosejaw AOs based on topological similarity of cranial nerve innervation, and subject these homology conjectures to tests of congruence under a phylogenetic hypothesis for the loosejaw dragonfishes. On the basis of whole‐mount, triple‐stained specimens, innervation of the loosejaw AOs is described. The AO of Aristostomias and the anterior AO of Pachystomias are innervated by the profundal ramus of the trigeminal (Tpr), while the far‐red AO of Malacosteus and a small ventral AO of Pachystomias are innervated by the maxillary ramus of the trigeminal (Tmx). The largest far‐red AO of Pachystomias, positioned directly below the orbit, and the short‐wave AO of Photostomias are innervated by a branch of the mandibular ramus of the trigeminal nerve. Conjectures of primary homology drawn from these neuroanatomical similarities were subjected to tests of congruence on a phylogeny of the loosejaws inferred from a reanalysis of a previously published morphological dataset. Optimized for accelerated transformation, the AO innervated by the Tpr appears as a single transformation on the new topology, thereby establishing secondary homology. The AOs innervated by the Tmd found in Pachystomias and Photostomias appear as two transformations in a reconstruction on the new topology, a result that rejects secondary homology of this structure. The secondary homology of AOs innervated by the Tmx found in Malacosteus and Pachystomias is rejected on the same grounds. Two short‐wave cephalic photophores present in all four genera, the suborbital (SO) and the postorbital (PO), positioned in the posteroventral margin of the orbit and directly posterior to the orbit, respectively, are innervated by separate divisions of the Tmd. The primary homologies of the loosejaw PO and SO across loosejaw taxa are proposed on the basis of similar innervation patterns. Because of dissimilar innervation of the loosejaw SO and SO of basal stomiiforms, primary homology of these photophores cannot be established. Because of similar function and position, the PO of all other stomiid taxa is likely homologous with the loosejaw PO. Nonhomology of loosejaw long‐wave photophores is corroborated by previously published histological evidence. The totality of evidence suggests that the only known far‐red bioluminescent system in vertebrates has evolved as many as three times in a closely related group of deep‐sea fishes. J. Morphol., 2010.

An Intact Retroviral Gene Conserved in Spiny-Rayed Fishes for over 100 My

We have identified a retroviral envelope gene with a complete, intact open reading frame (ORF) in 20 species of spiny-rayed fishes (Acanthomorpha). The taxonomic distribution of the gene, “percomORF”, indicates insertion into the ancestral lineage >110 Ma, making it the oldest known conserved gene of viral origin in a vertebrate genome. Underscoring its ancient provenence, percomORF exists as an isolated ORF within the intron of a widely conserved host gene, with no discernible proviral sequence nearby. Despite its remarkable age, percomORF retains canonical features of a retroviral glycoprotein, and tests for selection strongly suggest cooption for a host function. Retroviral envelope genes have been coopted for a role in placentogenesis by numerous lineages of mammals, including eutherians and marsupials, representing a variety of placental structures. Therefore percomORF’s presence within the group Percomorpha—unique among spiny-finned fishes in having evolved placentation and live birth—is especially intriguing.

High postural costs and anaerobic metabolism during swimming support the hypothesis of a U-shaped metabolism–speed curve in fishes

Significance Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds. Empirical studies to date do not support this view. Here we report a complete dataset on a swimming batoid fish that shows a clear energetic minimum at intermediate swimming speeds. We also demonstrate that this species uses a combination of aerobic and anaerobic metabolism to fuel steady swimming at each speed, including the slowest speeds tested. This contradicts the widespread assumption that fish use only aerobic metabolism at low speeds. Kinematic data support this nonlinear relationship by also showing a U-shaped pattern to body angle during steady swimming. Swimming performance is considered a key trait determining the ability of fish to survive. Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds and increasing expenditure at low and high speeds. However, to date no complete datasets have shown an energetic minimum for swimming fish at intermediate speeds rather than low speeds. To address this knowledge gap, we used a negatively buoyant fish, the clearnose skate Raja eglanteria, and took two approaches: a classic critical swimming speed protocol and a single-speed exercise and recovery procedure. We found an anaerobic component at each velocity tested. The two approaches showed U-shaped, though significantly different, speed–metabolic relationships. These results suggest that (i) postural costs, especially at low speeds, may result in J- or U-shaped metabolism–speed curves; (ii) anaerobic metabolism is involved at all swimming speeds in the clearnose skate; and (iii) critical swimming protocols might misrepresent the true costs of locomotion across speeds, at least in negatively buoyant fish.

A biorobotic model of the suction-feeding system in largemouth bass: the roles of motor program speed and hyoid kinematics

ABSTRACT The vast majority of ray-finned fishes capture prey through suction feeding. The basis of this behavior is the generation of subambient pressure through rapid expansion of a highly kinetic skull. Over the last four decades, results from in vivo experiments have elucidated the general relationships between morphological parameters and subambient pressure generation. Until now, however, researchers have been unable to tease apart the discrete contributions of, and complex relationships among, the musculoskeletal elements that support buccal expansion. Fortunately, over the last decade, biorobotic models have gained a foothold in comparative research and show great promise in addressing long-standing questions in vertebrate biomechanics. In this paper, we present BassBot, a biorobotic model of the head of the largemouth bass (Micropterus salmoides). BassBot incorporates a 3D acrylic plastic armature of the neurocranium, maxillary apparatus, lower jaw, hyoid, suspensorium and opercular apparatus. Programming of linear motors permits precise reproduction of live kinematic behaviors including hyoid depression and rotation, premaxillary protrusion, and lateral expansion of the suspensoria. BassBot reproduced faithful kinematic and pressure dynamics relative to live bass. We show that motor program speed has a direct relationship to subambient pressure generation. Like vertebrate muscle, the linear motors that powered kinematics were able to produce larger magnitudes of force at slower velocities and, thus, were able to accelerate linkages more quickly and generate larger magnitudes of subambient pressure. In addition, we demonstrate that disrupting the kinematic behavior of the hyoid interferes with the anterior-to-posterior expansion gradient. This resulted in a significant reduction in subambient pressure generation and pressure impulse of 51% and 64%, respectively. These results reveal the promise biorobotic models have for isolating individual parameters and assessing their role in suction feeding. Summary: Experiments using a biorobotic model of the suction feeding system of ray-finned fishes reveal that motor program speed and kinematic timing of key musculoskeletal components affect subambient pressure generation.