The Genomes of Two Billfishes Provide Insights into the Evolution of Endothermy in Teleosts

Endothermy is a typical convergent phenomenon which has evolved independently at least eight times in vertebrates, and is of significant advantage to organisms in extending their niches. However, how vertebrates other than mammals or birds, especially teleosts, achieve endothermy has not previously been fully understood. In this study, we sequenced the genomes of two billfishes (swordfish and sailfish), members of a representative lineage of endothermic teleosts. Convergent amino acid replacements were observed in proteins related to heat production and the visual system in two endothermic teleost lineages, billfishes and tunas. The billfish-specific genetic innovations were found to be associated with heat exchange, thermoregulation, and the specialized morphology, including elongated bill, enlarged dorsal fin in sailfish and loss of the pelvic fin in swordfish.     

Filter-feeding and cruising swimming speeds of basking sharks compared with optimal models: they filter-feed slower than predicted for their size

Movements of six basking sharks (4.0-6.5 m total body length, L(T)) swimming at the surface were tracked and horizontal velocities determined. Sharks were tracked for between 1.8 and 55 min with between 4 and 21 mean speed determinations per shark track. The mean filter-feeding swimming speed was 0.85 m s(-1) (+/-0.05 S.E., n=49 determinations) compared to the non-feeding (cruising) mean speed of 1.08 m s(-1) (+/-0.03 S.E., n=21 determinations). Both absolute (m s(-1)) and specific (L s(-1)) swimming speeds during filter-feeding were significantly lower than when cruise swimming with the mouth closed, indicating basking sharks select speeds approximately 24% lower when engaged in filter-feeding. This reduction in speed during filter-feeding could be a behavioural response to avoid increased drag-induced energy costs associated with feeding at higher speeds. Non-feeding basking sharks (4 m L(T)) cruised at speeds close to, but slightly faster ( approximately 18%) than the optimum speed predicted by the Weihs (1977) [Weihs, D., 1977. Effects of size on the sustained swimming speeds of aquatic organisms. In: Pedley, T.J. (Ed.), Scale Effects in Animal Locomotion. Academic Press, London, pp. 333-338.] optimal cruising speed model. In contrast, filter-feeding basking sharks swam between 29 and 39% slower than the speed predicted by the Weihs and Webb (1983) [Weihs, D., Webb, P.W., 1983. Optimization of locomotion. In: Webb, P.W., Weihs, D. (Eds.), Fish Biomechanics. Praeger, New York, pp. 339-371.] optimal filter-feeding model. This significant under-estimation in observed feeding speed compared to model predictions was most likely accounted for by surface drag effects reducing optimum speeds of tracked sharks, together with inaccurate parameter estimates used in the general model to predict optimal speeds of basking sharks from body size extrapolations.     

Power isn't everything: muscle function and energetic costs during steady swimming in Atlantic cod (Gadus morhua)

Power produced by red myotomal muscles of fish during cruise swimming appears seldom maximized, so we sought to investigate whether economy may impact or dominate muscle function. We measured cost of transport (COT) using oxygen consumption and the strain trajectories and electromyographic activity of red muscle measured at anterior (ANT) and posterior (POST) locations while Atlantic cod (Gadus morhua) swam steadily at speeds between 0.3 and 1.0 body lengths (BL) s(-1). We then measured the power produced by isolated segments of red muscle when activated either as in the swimming cod or such that maximal net power was produced. Patterns of activation during swimming were not optimal for power output and were highly variable between tail beats, particularly at the ANT location and at slow swim speeds. Muscle strain amplitude did not increase until swimming speed reached 0.9 (ANT) versus 0.5 (POST) BL s(-1). These limited power to only 53% (ANT) and 71% (POST) of maximum at slower swim speeds and to 70%-80% of maximum at high swim speeds. COT (resting metabolism subtracted) was minimal at the slowest swim speed, surprisingly, where power was most impaired by activation and strain. Thus, production of powered forces for maneuverability/stability appeared to greatly impact red muscle function during cruise swimming in cod, particularly at slow speeds and in ANT muscle.     

Is tilting behaviour at low swimming speeds unique to negatively buoyant fish? Observations on steelhead trout,Oncorhynchus mykiss,and bluegill,Lepomis macrochirus

When swimming at low speeds, steelhead trout and bluegill sunfish tilted the body at an angle to the mean swimming direction. Trout swam using continuous body/caudal fin undulation, with a positive (head-up) tilt angle ( 0 , degrees) that decreased with swimming speed ( u , cm s⁻¹) according to: 0 =(164±96).u^{(−1.14±0.41)} (regression coefficients; mean±2 s.e. ). Bluegill swimming gaits were more diverse and negative (head down) tilt angles were usual. Tilt angle was −3·0 ± 0.9° in pectoral fin swimming at speeds of approximately 0.2–1.7 body length s⁻¹ (Ls⁻¹; 3–24 cm s⁻¹), −4.5 ±2.6° during pectoral fin plus body/caudal fin swimming at 1·2–1·7 L s⁻¹ (17–24cm s⁻¹), and −5.0± 1.0° during continuous body/caudal fin swimming at 1.6 and 2.5 L s⁻¹ (22 and 35cm s⁻¹). At higher speeds, bluegill used burst-and-coast swimming for which the tilt angle was 0.1±0.6°. These observations suggest that tilting is a general phenomenon of low speed swimming at which stabilizers lose their effectiveness. Tilting is interpreted as an active compensatory mechanism associated with increased drag and concomitant increased propulsor velocities to provide better stabilizing forces. Increased drag associated with trimming also explains the well-known observation that the relationship between tail-beat frequency and swimming speed does not pass through the origin. Energy dissipated because of the drag increases at low swimming speeds is presumably smaller than that which would occur with unstable swimming.     

Toothless predators: feeding performance and techniques among the piscivores within Lake Tana's endemic barbus species flock (Pisces:Cyprinidae)

With more than 2000 fish species the Cyprinidae is the largest family of vertebrates. Lake Tana, a large lake (3050 km²) situated in the NW‐ highlands of Ethiopia, harbours, as far as we know the only remaining intact species flock of large (max. 100 cm FL) cyprinid fishes (15 Barbus spp.). One of the most intriguing aspects of this endemic Barbus species flock is the large number of piscivores (8). Cyprinid fishes seem not well designed for piscivory, they lack teeth in the oral jaw, have a small slit‐shaped pharyngeal cavity and all lack a stomach with low pH for digesting large prey. Many barbs are benthivorous species, like the ancestral barb in Lake Tana's isolated system. Why then is piscivory, which is rare among cyprinids, so common in Lake Tana Barbus? The aim of present study was to compare the performance and techniques of these piscivorous Barbus with known piscivores from other fish families. We studied prey handling times over prey size, prey capture using high‐speed movies, and assessed the effect of prey size on performance and prey selection in the field. Performances were explained by functional morphology of their feeding system. Overall, Lake Tana's piscivorous Barbus perform relatively 'poor', compared to piscivores from other fish families. For example, Lake Tana's piscivores are only able to handle prey fish smaller than 16% of their own body length. However, Lake Tana lacks potential piscivorous competitors, rendering the piscivorous Barbus by far the 'best' and apparently highly successful. They have adapted to all available macro‐habitats (littoral, offshore pelagic and offshore benthic), using different techniques (ambush, pursuit and cruising), a unique scenario for barbs.     

Critical swimming speed: its ecological relevance.

Critical swimming speed (U(crit)) is a standard measurement to assess swimming capabilities of fishes. To conduct this measurement a fish is introduced into a water tunnel in which the current velocity can be controlled by the investigator. At the beginning of the measurement water velocity is low, approximately 1 body length (BL) s(-1), and is then incrementally increased at prescribed intervals. Fishes tend to maintain their position in the water tunnel against the current until fatigue sets in. The time and velocity at which the fish fatigue are used to calculate the critical swimming speed. This procedure is widely used to assess the effects of environmental conditions and pollutants on fish performance. Since the procedure is conducted in conditions that are far from representing most natural environment experienced by fishes, doubts have been raised about its ecological and ecophysiological relevance. Few studies examined correlations between critical swimming speed and traits that seem to be more ecologically relevant. Positive correlations were found between U(crit) and routine activity, metabolic rates and body size of open water, planktivorous fishes, metabolic rates and body size. These data indirectly suggest ecological relevancy of U(crit), but direct measurements relating U(crit) to reproductive success or survival are required to assess such relevancy.     

Body Fineness Ratio as a Predictor of Maximum Prolonged-Swimming Speed in Coral Reef Fishes

The ability to sustain high swimming speeds is believed to be an important factor affecting resource acquisition in fishes. While we have gained insights into how fin morphology and motion influences swimming performance in coral reef fishes, the role of other traits, such as body shape, remains poorly understood. We explore the ability of two mechanistic models of the causal relationship between body fineness ratio and endurance swimming-performance to predict maximum prolonged-swimming speed (U_max) among 84 fish species from the Great Barrier Reef, Australia. A drag model, based on semi-empirical data on the drag of rigid, submerged bodies of revolution, was applied to species that employ pectoral-fin propulsion with a rigid body at U _max. An alternative model, based on the results of computer simulations of optimal shape in self-propelled undulating bodies, was applied to the species that swim by body-caudal-fin propulsion at U_max. For pectoral-fin swimmers, U_max increased with fineness, and the rate of increase decreased with fineness, as predicted by the drag model. While the mechanistic and statistical models of the relationship between fineness and U_max were very similar, the mechanistic (and statistical) model explained only a small fraction of the variance in U_max. For body-caudal-fin swimmers, we found a non-linear relationship between fineness and U_max, which was largely negative over most of the range of fineness. This pattern fails to support either predictions from the computational models or standard functional interpretations of body shape variation in fishes. Our results suggest that the widespread hypothesis that a more optimal fineness increases endurance-swimming performance via reduced drag should be limited to fishes that swim with rigid bodies.     

The behavior in flow of the morphologically variable seaweed Hedophyllum sessile (C. Ag.) Setchell

Drag force was measured on individual specimens of Hedophyllum sessile in a variable-speed flow tank. Those from sheltered localities, which are broad, bullate blades, experience greater drag at a given water velocity than ones from localities more exposed to the action of waves, which have smooth, deeply dissected blades. All specimens rearranged their blades as water velocity increased, resulting in a decrease in effective drag at higher water speeds, but individuals with smooth, dissected blades assumed a more compact shape at high current speeds and thus reduced their effective drag over that of broad-bladed individuals at the same speed. In habitats chronically exposed to strong wave action, drag reduction may be an important survival mechanism; in calm habitats the turbulence induced by lack of such streamlining may enhance mixing of the water in the immediate vicinity of a plant.     

Drag reduction in wave-swept macroalgae: Alternative strategies and new predictions

? Premise of the study: Intertidal macroalgae must resist extreme hydrodynamic forces imposed by crashing waves. How does frond flexibility mitigate drag, and how does flexibility affect predictions of drag and dislodgement in the field? ? Methods: We characterized flexible reconfiguration of six seaweed species in a recirculating water flume, documenting both shape change and area reduction as fronds reorient. We then used a high-speed gravity-accelerated water flume to test our ability to predict drag under waves based on extrapolations of drag recorded at slower speeds. We compared dislodgement forces to drag forces predicted from slow- and high-speed data to generate new predictions of survivorship and maximum sustainable frond size along wave-swept shores. ? Key results: Bladed algae were generally "shape changers", limiting drag by reducing drag coefficients, whereas the branched alga Calliarthron was an "area reducer", limiting drag by reducing projected area in flow. Drag predictions often underestimated actual drag measurements at high speeds, suggesting that slow-speed data may not reflect the performance of flexible seaweeds under breaking waves. Several seaweeds were predicted to dislodge at similar combinations of velocity and frond size, suggesting common scaling factors of dislodgement strength and drag. ? Conclusions: Changing shape and reducing projected area in flow are two distinct strategies employed by flexible seaweeds to resist drag. Flexible reconfiguration contributes to the uncertainty of drag extrapolation, and researchers should use caution when predicting drag and dislodgement of seaweeds in the field.     

Ontogeny of form and function: locomotor morphology and drag in zebrafish (Danio rerio)

Many fish species transform in body shape during growth, but it remains unclear how this influences the mechanics of locomotion. Therefore, the present study focused on understanding how drag generation during coasting is affected by ontogenetic changes in the morphology of zebrafish (Danio rerio). The shapes of the body and fins were measured from photographs of fish ranging in size from small larvae to mature adults and these morphometrics were compared to drag coefficients calculated from high-speed video recordings of routine swimming. We found that the viscous drag coefficient of larval and juvenile fish increased by more than an order of magnitude during growth and the inertial drag coefficient decreased at a comparable rate in adults. These hydrodynamic changes occurred as zebrafish disproportionately increased the span of their fins and their body changed shape from elongated to streamlined, as reflected by the logistic growth of a newly defined streamlining index, SL. These results suggest that morphological changes incur a performance cost by generating greater drag when larvae and juveniles operate in the viscous regime, but later provide a performance benefit by reducing pressure drag in the inertial regime of the adult stage.     

Shape variation in a benthic stream fish across flow regimes

Evolution of fish body shapes in flowing and non-flowing waters have been examined for several species. Flowing water can select for fish body shapes that increase steady swimming efficiency, whereas non-flowing water can favor shapes that increase unsteady swimming efficiency. Benthic stream fishes often use areas near the substrate that exhibit reduced or turbulent flow, thus it is unclear which swimming forms would be favored in such environments, and how shape might change across flow regimes. To test the relationship between fish body shape and flow regime in a benthic stream fish, we used geometric morphometric techniques to characterize lateral body shape in mountain sucker (Catostomus platyrhynchus) across flow rates, using stream gradient as an indicator of stream flow. Mountain suckers from low-flow environments were more streamlined, consistent with steady swimming body shapes, whereas mountain suckers from high flows had deeper bodies, consistent with unsteady swimming body shapes. In addition, smaller individuals tended to have more robust body shapes. These patterns are opposite to those predicted for stream fishes in the mid-water column. The benthic stream environment represents a distinct selective environment for fish shape that does not appear to conform to the simple dichotomy of flowing versus non-flowing water.     

Distribution and habitat associations of billfish and swordfish larvae across mesoscale features in the Gulf of Mexico

Ichthyoplankton surveys were conducted in surface waters of the northern Gulf of Mexico (NGoM) over a three-year period (2006-2008) to determine the relative value of this region as early life habitat of sailfish (Istiophorus platypterus), blue marlin (Makaira nigricans), white marlin (Kajikia albida), and swordfish (Xiphias gladius). Sailfish were the dominant billfish collected in summer surveys, and larvae were present at 37.5% of the stations sampled. Blue marlin and white marlin larvae were present at 25.0% and 4.6% of the stations sampled, respectively, while swordfish occurred at 17.2% of the stations. Areas of peak production were detected and maximum density estimates for sailfish (22.09 larvae 1000 m(-2)) were significantly higher than the three other species: blue marlin (9.62 larvae 1000 m(-2)), white marlin (5.44 larvae 1000 m(-2)), and swordfish (4.67 larvae 1000 m(-2)). The distribution and abundance of billfish and swordfish larvae varied spatially and temporally, and several environmental variables (sea surface temperature, salinity, sea surface height, distance to the Loop Current, current velocity, water depth, and Sargassum biomass) were deemed to be influential variables in generalized additive models (GAMs). Mesoscale features in the NGoM affected the distribution and abundance of billfish and swordfish larvae, with densities typically higher in frontal zones or areas proximal to the Loop Current. Habitat suitability of all four species was strongly linked to physicochemical attributes of the water masses they inhabited, and observed abundance was higher in slope waters with lower sea surface temperature and higher salinity. Our results highlight the value of the NGoM as early life habitat of billfishes and swordfish, and represent valuable baseline data for evaluating anthropogenic effects (i.e., Deepwater Horizon oil spill) on the Atlantic billfish and swordfish populations.     

How sailfish use their bills to capture schooling prey

The istiophorid family of billfishes is characterized by an extended rostrum or ‘bill’. While various functions (e.g. foraging and hydrodynamic benefits) have been proposed for this structure, until now no study has directly investigated the mechanisms by which billfishes use their rostrum to feed on prey. Here, we present the first unequivocal evidence of how the bill is used by Atlantic sailfish (Istiophorus albicans) to attack schooling sardines in the open ocean. Using high-speed video-analysis, we show that (i) sailfish manage to insert their bill into sardine schools without eliciting an evasive response and (ii) subsequently use their bill to either tap on individual prey targets or to slash through the school with powerful lateral motions characterized by one of the highest accelerations ever recorded in an aquatic vertebrate. Our results demonstrate that the combination of stealth and rapid motion make the sailfish bill an extremely effective feeding adaptation for capturing schooling prey.     

Swimming behavior in relation to buoyancy in an open swimbladder fish, the Chinese sturgeon

The swimbladder of fishes is readily compressed by hydrostatic pressure with depth, causing changes in buoyancy. While modern fishes can regulate buoyancy by secreting gases from the blood into the swimbladder, primitive fishes, such as sturgeons, lack this secretion mechanism and rely entirely on air gulped at the surface to inflate the swimbladder. Therefore, sturgeons may experience changes in buoyancy that will affect their behavior at different depths. To test this prediction, we attached data loggers to seven free-ranging Chinese sturgeons Acipenser sinensis in the Yangtze River, China, to monitor their depth utilization, tail-beating activity, swim speed and body inclination. Two distinct, individual-specific, behavioral patterns were observed. Four fish swam at shallow depths (7–31 m), at speeds of 0.5–0.6 m s⁻¹, with ascending and descending movements of 1.0–2.4 m in amplitude. They beat their tails continuously, indicating that their buoyancy was close to neutral with their inflated swimbladders. In addition, their occasional visits to the surface suggest that they gulped air to inflate their swimbladders. The other three fish spent most of their time (88–94%) on the river bottom at a depth of 106–122 m with minimum activity. They occasionally swam upwards at speeds of 0.6–0.8 m s⁻¹ with intense tailbeats before gliding back passively to the bottom, in a manner similar to fishes that lack a swimbladder. Their bladders were probably collapsed by hydrostatic pressure, resulting in negative buoyancy. We conclude that Chinese sturgeons behave according to their buoyancy, which varies with depth due to hydrostatic compression of the swimbladder.     

Computational fluid dynamics of flow regime and hydrodynamic forces generated by a gliding North Atlantic right whale (Eubalaena glacialis)

Accurate estimates of drag on marine animals are required to investigate the locomotive cost, propulsive efficiency, and the impacts of entanglement if the animal is carrying fishing gear. In this study, we performed computational fluid dynamics analysis of a 10 m (length over all) right whale to obtain baseline measurements of drag on the animal. Swimming speeds covering known right whale speed range (0.125 m/s to 8 m/s) were tested. We found a weak dependence between drag coefficient and Reynolds number. At a swimming speed of 2 m/s, we analyzed the boundary layer thicknesses, the flow regimes, and drag components. We found the thickest boundary layer at the lateral sides of the peduncle, whereas the boundary layer thickness over the outer part of the flukes was less than 1.7 cm. Laminar flow occurred over the anterior ~0.6 LoA and turbulent flow from ~0.8 LoA to the fluke notch. On the surfaces of the flukes outside of the body wake region, flow was laminar. Our most significant finding is that the drag coefficient (0.0071–0.0059) of a right whale for swimming speeds ranging from 0.25 m/s to 2 m/s is approximately twice that of many previous estimates for cetaceans.     

Aerial Jumping in the Trinidadian Guppy (Poecilia reticulata)

Many fishes are able to jump out of the water and launch themselves into the air. Such behavior has been connected with prey capture, migration and predator avoidance. We found that jumping behavior of the guppy Poecilia reticulata is not associated with any of the above. The fish jump spontaneously, without being triggered by overt sensory cues, is not migratory and does not attempt to capture aerial food items. Here, we use high speed video imaging to analyze the kinematics of the jumping behavior P. reticulata. Fish jump from a still position by slowly backing up while using its pectoral fins, followed by strong body trusts which lead to launching into the air several body lengths. The liftoff phase of the jump is fast and fish will continue with whole body thrusts and tail beats, even when out of the water. This behavior occurs when fish are in a group or in isolation. Geography has had substantial effects on guppy evolution, with waterfalls reducing gene flow and constraining dispersal. We suggest that jumping has evolved in guppies as a behavioral phenotype for dispersal.     

Gait transition speed, pectoral fin-beat frequency and amplitude in Cymatogaster aggregata, Embiotoca lateralis and Damalichthys vacca

Surfperches are labriform swimmers and swim primarily with their pectoral fins, using the tail to assist only at higher speeds. The transition, from pectoral to pectoral and caudal fins, occurs at a threshold speed that has been termed physiologically and biomechanically 'equivalent' for fishes of different size. The gait transition ( U _P-C) of Cymatogaster aggregata occurred at a higher speed (measured in bodylengths s⁻¹) for smaller fish than larger fish. At U _P-C, pectoral fin-beat frequency was size-dependent: smaller fish have a higher pectoral fin-beat frequency than larger fish. In contrast, at low speeds (i.e. <60% of U _P-C) the pectoral fin-beat frequency was independent of the size of the fish. Inter-specific comparisons of U _P-C, pectoral fin-beat frequency and amplitude among C. aggregata, Embiotoca lateralis and Damalichthys vacca showed that C. aggregata had a higher U _P-C than E. lateralis and D. vacca . The pectoral fin-beat frequency at U _P-C showed no significant differences among species. Cymatogaster aggregata achieved higher U _P-C, in part, through increased fin beat amplitude rather than frequency. These differences in performance may be related to the different habitats in which these species live.     

Tilting behaviour of the Atlantic mackerel, Scomber scombrus, at low swimming speeds

Negatively-buoyant Atlantic mackerel, Scomber scombrus L., (fork length 30–39 cm) tilt their bodies with the head up while swimming at speeds below 0.8 body length per second (B.L. s⁻¹). This behaviour is quantitatively described by the body attack angle and swimming speed measured from film records. The maximum recorded body attack angle was 27° in a 32 cm-long fish swimming at 0.45 B.L. s⁻¹ while its nose followed a course close to the horizontal. In general, larger body attack angles were shown at lower swimming speeds and were associated with denser bodies at each speed. We consider that this behaviour pattern allows the fish to maintain a chosen swimming depth while its body creates lift by acting as a hydrofoil. Lift from the fins is insufficient at low swimming speeds.     

Whole-body lift and ground effect during pectoral fin locomotion in the northern spearnose poacher (Agonopsis vulsa)

The northern spearnose poacher, Agonopsis vulsa, is a benthic, heavily armored fish that swims primarily using pectoral fins. High-speed kinematics, whole-body lift measurements, and flow visualization were used to study how A. vulsa overcomes substantial negative buoyancy while generating forward thrust. Kinematics for five freely swimming poachers indicate that individuals tend to swim near the bottom (within 1 cm) with a consistently small (less than 1°) pitch angle of the body. When the poachers swam more than 1 cm above the bottom, however, body pitch angles were higher and varied inversely with speed, suggesting that lift may help overcome negative buoyancy. To determine the contribution of the body to total lift, fins were removed from euthanized fish (n=3) and the lift and drag from the body were measured in a flume. Lift and drag were found to increase with increasing flow velocity and angle of attack (ANCOVA, p<0.0001 for both effects). Lift force from the body was found to supply approximately half of the force necessary to overcome negative buoyancy when the fish were swimming more than 1 cm above the bottom. Lastly, flow visualization experiments were performed to examine the mechanism of lift generation for near-bottom swimming. A vortex in the wake of the pectoral fins was observed to interact strongly with the substratum when the animals approached the bottom. These flow patterns suggest that, when swimming within 1 cm of the bottom, poachers may use hydrodynamic ground effect to augment lift, thereby counteracting negative buoyancy.