Joseph T. Thompson

Swimming dynamics and propulsive efficiency of squids throughout ontogeny

Squids encounter vastly different flow regimes throughout ontogeny as they undergo critical morphological changes to their two locomotive systems: the fins and jet. Squid hatchlings (paralarvae) operate at low and intermediate Reynolds numbers (Re) and typically have rounded bodies, small fins, and relatively large funnel apertures, whereas juveniles and adults operate at higher Re and generally have more streamlined bodies, larger fins, and relatively small funnel apertures. These morphological changes and varying flow conditions affect swimming performance in squids. To determine how swimming dynamics and propulsive efficiency change throughout ontogeny, digital particle image velocimetry (DPIV) and kinematic data were collected from an ontogenetic range of long-finned squid Doryteuthis pealeii and brief squid Lolliguncula brevis swimming in a holding chamber or water tunnel (Re = 20-20 000). Jet and fin wake bulk properties were quantified, and propulsive efficiency was computed based on measurements of impulse and excess kinetic energy in the wakes. Paralarvae relied predominantly on a vertically directed, high frequency, low velocity jet as they bobbed up and down in the water column. Although some spherical vortex rings were observed, most paralarval jets consisted of an elongated vortical region of variable length with no clear pinch-off of a vortex ring from the trailing tail component. Compared with paralarvae, juvenile and adult squid exhibited a more diverse range of swimming strategies, involving greater overall locomotive fin reliance and multiple fin and jet wake modes with better defined vortex rings. Despite greater locomotive flexibility, jet propulsive efficiency of juveniles/adults was significantly lower than that of paralarvae, even when juvenile/adults employed their highest efficiency jet mode involving the production of periodic isolated vortex rings with each jet pulse. When the fins were considered together with the jet for several juvenile/adult swimming sequences, overall propulsive efficiency increased, suggesting that fin contributions are important and should not be overlooked in analyses of the swimming performance of squids. The fins produced significant thrust and consistently had higher propulsive efficiency than did the jet. One particularly important area of future study is the determination of coordinated jet/fin wake modes that have the greatest impact on propulsive efficiency. Although such research would be technically challenging, requiring new, powerful, 3D approaches, it is necessary for a more comprehensive assessment of propulsive efficiency of the squid dual-mode locomotive system.

A Case-Based Approach Increases Student Learning Outcomes and Comprehension of Cellular Respiration Concepts.

This study investigated student learning outcomes using a case‐based approach focused on cellular respiration. Students who used the case study, relative to students who did not use the case study, exhibited a significantly greater learning gain, and demonstrated use of higher‐order thinking skills. Preliminary data indicate that after engaging with the case study, students were more likely to answer a question addressing misconceptions about cellular respiration correctly when compared with students who did not use the case study. More rigorous testing is needed to fully elucidate whether case‐based learning can effectively clarify student misconceptions related to biological processes.

Pulsed jet dynamics of squid hatchlings at intermediate Reynolds numbers

SUMMARY Squid paralarvae (hatchlings) rely predominantly on a pulsed jet for locomotion, distinguishing them from the majority of aquatic locomotors at low/intermediate Reynolds numbers (Re), which employ oscillatory/undulatory modes of propulsion. Although squid paralarvae may delineate the lower size limit of biological jet propulsion, surprisingly little is known about the hydrodynamics and propulsive efficiency of paralarval jetting within the intermediate Re realm. To better understand paralarval jet dynamics, we used digital particle image velocimetry (DPIV) and high-speed video to measure bulk vortex properties (e.g. circulation, impulse, kinetic energy) and other jet features [e.g. average and peak jet velocity along the jet centerline (Uj and Ujmax, respectively), jet angle, jet length based on the vorticity and velocity extents (Lω and LV, respectively), jet diameter based on the distance between vorticity peaks (Dω), maximum funnel diameter (DF), average and maximum swimming speed (U and Umax, respectively)] in free-swimming Doryteuthis pealeii paralarvae (1.8 mm dorsal mantle length) (Resquid=25–90). Squid paralarvae spent the majority of their time station holding in the water column, relying predominantly on a frequent, high-volume, vertically directed jet. During station holding, paralarvae produced a range of jet structures from spherical vortex rings (Lω/Dω=2.1, LV/DF=13.6) to more elongated vortex ring structures with no distinguishable pinch-off (Lω/Dω=4.6, LV/DF=36.0). To swim faster, paralarvae increased pulse duration and Lω/Dω, leading to higher impulse but kept jet velocity relatively constant. Paralarvae produced jets with low slip, i.e. ratio of jet velocity to swimming velocity (Uj/U or Ujmax/Umax), and exhibited propulsive efficiency [ηpd=74.9±8.83% (±s.d.) for deconvolved data] comparable with oscillatory/undulatory swimmers. As slip decreased with speed, propulsive efficiency increased. The detection of high propulsive efficiency in paralarvae is significant because it contradicts many studies that predict low propulsive efficiency at intermediate Re for inertial forms of locomotion.

Ontogenetic changes in mantle kinematics during escape-jet locomotion in the oval squid, Sepioteuthis lessoniana Lesson, 1830

We investigated the kinematics of mantle movement during escape jet behavior in an ontogenetic series of Sepioteuthis lessoniana, the oval squid. Changes in mantle diameter during the jet were measured from digitized S-VHS video fields of tethered animals that ranged in age from hatchlings to 9 weeks. The amplitude of both mantle contraction and mantle hyperinflation (expressed as percent change from the resting mantle diameter) during an escape jet was significantly greater in hatchlings than in older, larger squid (P < 0.05). The maximum amplitude of mantle contraction during the escape jet decreased from an average of −40% in hatchlings to −30% in the largest animals studied. The maximum amplitude of mantle hyperinflation decreased from an average of 18% in hatchlings to 9% in the largest squid examined. In addition, the maximum rate of mantle contraction decreased significantly during ontogeny (P < 0.05), from a maximum of 8.6 mantle circumference lengths per second (L/s) in hatchlings to 3.8 L/s in the largest animals studied. The ontogenetic changes in the mantle kinematics of the escape jet occurred concomitantly with changes in the organization of collagenous connective tissue fiber networks in the mantle. The alteration in mantle kinematics during growth may result in proportionately greater mass flux during the escape jet in newly hatched squid than in larger animals.

Ontogenetic Changes in Fibrous Connective Tissue Organization in the Oval Squid, Sepioteuthis lessoniana Lesson, 1830

Ontogenetic changes in the organization and volume fraction of collagenous connective tissues were examined in the mantle of Sepioteuthis lessoniana, the oval squid. Outer tunic fiber angle (the angle of a tunic collagen fiber relative to the long axis of the squid) decreased from 33.5° in newly hatched animals to 17.7° in the largest animals studied. The arrangement of intramuscular collagen fiber systems 1 (IM-1) and 2 (IM-2) also changed significantly during ontogeny. Because of the oblique trajectory of the IM-1 collagen fibers, two fiber angles were needed to describe their organization: (1) IM-1SAG, the angle of an IM-1 collagen fiber relative to the squid’s long axis when viewed from a sagittal plane and (2) IM-1TAN, the angle of an IM-1 collagen fiber relative to the squid’s long axis when viewed from a plane tangential to the outer curvature of the mantle. The sagittal component (IM-1SAG) of the IM-1 collagen fiber angle was lowest in hatchling squid (32.7°) and increased exponentially during growth to 43° in squid with a dorsal mantle length (DML) of 15 mm. In squid larger than 15 mm DML, IM-1SAG fiber angle did not change. The tangential component (IM-1TAN) of IM-1 collagen fiber angle was highest in hatchling squid (39°) and decreased to 32° in the largest squid examined. IM-2 collagen fiber angle (the angle of an IM-2 collagen fiber relative to the outer surface of the mantle) was lowest in hatchling squid (34.6°) and increased exponentially to about 50° in 15-mm DML animals. In squid larger than 15 mm DML, IM-2 fiber angle increased slightly with size. The volume fraction of collagen in IM-1 and IM-2 increased 68 and 36 times, respectively, during growth. The ontogenetic changes in the organization of collagen fibers in the outer tunic, IM-1, and IM-2 may lead to ontogenetic differences in the kinematics of mantle movement and in elastic energy storage during jet locomotion.

Ontogeny of mantle musculature and implications for jet locomotion in oval squid Sepioteuthis lessoniana

SUMMARY We examined the relationship between mantle muscle structure and mantle kinematics in an ontogenetic series (5-85 mm dorsal mantle length) of oval squid, Sepioteuthis lessoniana. Thick filament length increased during growth in the mantle muscle fibres that power jet locomotion (i.e. the circular muscles). The thick filament length of both the superficial mitochondria-rich (SMR; analogous to vertebrate red muscle fibres) and central mitochondria-poor (CMP; analogous to vertebrate white muscle fibres) circular muscles increased significantly during ontogeny. Thick filaments in the SMR circular muscle fibres of newly hatched squid (N=5) ranged from 0.7 to 1.4 μm and averaged 1.0 μm, while the thick filaments of the SMR fibres of the largest squids (N=4) studied ranged from 1.2 to 3.4μ m and averaged 1.9 μm. The ontogeny of thick filament length in the CMP circular muscle fibres showed a similar trend. The range for hatchling CMP circular muscles was 0.7-1.4 μm, with an average of 1.0 μm, whereas the range and average for the largest squids studied were 0.9-2.2 μm and 1.5μ m, respectively. Within an individual hatchling, we noted no significant differences between the thick filament lengths of the SMR and CMP fibres. Within an individual juvenile, the thick filaments of the SMR fibres were∼ 25% longer than the CMP fibres. The change in thick filament length may alter the contractile properties of the circular muscles and may also result in a decrease in the rate of mantle contraction during jetting. In escape-jet locomotion, the maximum rate of mantle contraction was highest in newly hatched squid and declined during ontogeny. The maximum rate of mantle contraction varied from 7-13 muscle lengths per second in newly hatched squid (N=14) and from 3-5 muscle lengths per second in the largest squids (N=35) studied.

Mechanical specialization of the obliquely striated circular mantle muscle fibres of the long-finned squid Doryteuthis pealeii.

SUMMARY The centrally located, mitochondria-poor (CMP) and superficially located, mitochondria-rich (SMR) circular muscle fibres in the mantles of some squids provide one of the few known examples of specialization in an obliquely striated muscle. Little is known of the mechanical properties or of the mechanisms and performance consequences of specialization in these fibres. We combined morphological and physiological approaches to study specialization in the SMR and CMP fibres of the long-finned squid Doryteuthis pealeii. The mean thick filament length was 3.12±0.56 μm and 1.78±0.27μ m for the SMR and CMP fibres, respectively. The cross-sectional areas of the whole fibre and the core of mitochondria were significantly higher in the SMR fibres, but the area occupied by the myofilaments did not differ between the two fibre types. The area of sarcoplasmic reticulum visible in cross sections was significantly higher in CMP fibres than in SMR fibres. In live bundles of muscle fibres partially isolated from the mantle, mean peak isometric stress during tetanus was significantly greater in SMR [335 mN mm–2 physiological cross section (pcs)] than in CMP (216 mN mm–2 pcs) fibres. SMR fibres had a lower average twitch:tetanus ratio (SMR=0.073; CMP=0.18) and a twofold lower unloaded maximum shortening velocity at 20°C (SMR=2.4 L0 s–1; CMP=5.1 L0 s–1), where L0 was the preparation length that yielded the highest tetanic force. The structural differences in the two muscle fibre types play a primary role in determining their mechanical properties, and the significant differences in mechanical properties indicate that squid have two muscle gears. A simple model of the mantle shows that a gradient of strain and strain rate exists across the mantle wall, with fibres adjacent to the outer edge of the mantle experiencing 1.3- to 1.4-fold lower strain and strain rate than fibres adjacent to the inner edge of the mantle. The model also predicts that the CMP fibres generate virtually no power for slow jetting while the SMR fibres are too slow to generate power for the escape jets. The transmural differences in strain and strain rate predicted by the model apply to any cylindrical animal that has circumferentially oriented muscle fibres and an internal body cavity.

Ontogeny of Squid Mantle Function: Changes in the Mechanics of Escape-Jet Locomotion in the Oval Squid, Sepioteuthis lessoniana Lesson, 1830

In Sepioteuthis lessoniana, the oval squid, ontogenetic changes in the kinematics of the mantle during escape-jet locomotion imply a decline in the relative mass flux of the escape jet and may affect the peak weight-specific thrust of the escape jet. To examine the relationship between ontogenetic changes in the kinematics of the mantle and the thrust generated during the escape jet, we simultaneously measured the peak thrust and the kinematics of the mantle of squid tethered to a force transducer. We tested an ontogenetic series of S. lessoniana that ranged in size from 5 to 40 mm dorsal mantle length (DML). In newly hatched squids, thrust peaked 40 ms after the start of the escape jet and reached a maximum of between 0.10 mN and 0.80 mN. In the largest animals, thrust peaked 70 ms after the start of the escape jet and reached a maximum of between 18 mN and 110 mN. Peak thrust was normalized by the wet weight of the squid and also by the cross-sectional area of the circumferential muscle that provides power for the escape jet. The weight-specific peak thrust of the escape jet averaged 0.36 in newly hatched squid and increased significantly to an average of 1.5 in the largest squids measured (P < 0.01). The thrust per unit area of circumferential muscle averaged 0.25 mN/mm2 in hatchlings and increased significantly to an average of 1.4 mN/mm2 in the largest animals tested (P < 0.01). The impulse of the escape jet was also lowest in newly hatched individuals (1.3 mN · s) and increased significantly to 1000 mN · s in the largest squids measured (P < 0.01). These ontogenetic changes in the mechanics of the escape jet suggest (1) that propulsion efficiency of the exhalant phase of the jet is highest in hatchlings, and (2) that the mechanics of the circumferential muscles of the mantle change during growth.

Volumetric Flow Imaging Reveals the Importance of Vortex Ring Formation in Squid Swimming Tail-First and Arms-First

ABSTRACT Squids use a pulsed jet and fin movements to swim both arms-first (forward) and tail-first (backward). Given the complexity of the squid multi-propulsor system, 3D velocimetry techniques are required for the comprehensive study of wake dynamics. Defocusing digital particle tracking velocimetry, a volumetric velocimetry technique, and high-speed videography were used to study arms-first and tail-first swimming of brief squid Lolliguncula brevis over a broad range of speeds [0–10 dorsal mantle lengths (DML) s−1] in a swim tunnel. Although there was considerable complexity in the wakes of these multi-propulsor swimmers, 3D vortex rings and their derivatives were prominent reoccurring features during both tail-first and arms-first swimming, with the greatest jet and fin flow complexity occurring at intermediate speeds (1.5–3.0 DML s−1). The jet generally produced the majority of thrust during rectilinear swimming, increasing in relative importance with speed, and the fins provided no thrust at speeds >4.5 DML s−1. For both swimming orientations, the fins sometimes acted as stabilizers, producing negative thrust (drag), and consistently provided lift at low/intermediate speeds (<2.0 DML s−1) to counteract negative buoyancy. Propulsive efficiency (η) increased with speed irrespective of swimming orientation, and η for swimming sequences with clear isolated jet vortex rings was significantly greater (η=78.6±7.6%, mean±s.d.) than that for swimming sequences with clear elongated regions of concentrated jet vorticity (η=67.9±19.2%). This study reveals the complexity of 3D vortex wake flows produced by nekton with hydrodynamically distinct propulsors. Summary: Multi-propulsor squids produce complex 3D vortex wake flows while swimming arms-first and tail-first, as revealed by 3D jet/fin force and propulsive efficiency measurements.

Erectile tissue in an invertebrate animal: the Octopus copulatory organ

The most familiar examples of erectile tissue are the genitalia of mammals, notably the penis and clitoris. Among the soft-bodied invertebrates, erectile tissue is virtually unknown, even in sex organs. Here we report that the ligula, the copulatory organ that is a modification of an arm tip of male octopuses, is erectile in Octopus bimaculoides. The normally minute ligula was observed during an unsuccessful mating attempt to be engorged. Histological sections of the ligula reveal striking structural convergences with mammalian erectile tissue: large, well-vascularized internal cavities subdivided by networks of collagen fibres and enclosed by an array of collagen fibres. This internal structure differs markedly from the dense, three-dimensional array of muscles and connective tissues seen in the other octopodid ligulae examined. Erectile tissue may represent an evolutionary compromise between opposing selective forces. Small ligulae may be advantageous because O. bimaculoides hunts in daylight and the white-faced ligula may be conspicuous to predators. Large ligulae, however, may be advantageous if the intense sexual selection thought to occur among octopodids selects for large ligulae, which can transfer larger spermatophores that carry more sperm. An erectile ligula may minimize the impact of these opposing selective forces.