Phase shift between joint rotation and actuation reflects dominant forces and predicts muscle activation patterns.

During behavior, the work done by actuators on the body can be resisted by the body's inertia, elastic forces, gravity, or viscosity. The dominant forces that resist actuation have major consequences on the control of that behavior. In the literature, features and actuation of locomotion, for example, have been successfully predicted by nondimensional numbers (e.g. Froude number and Reynolds number) that generally express the ratio between two of these forces (gravitational, inertial, elastic, and viscous). However, animals of different sizes or motions at different speeds may not share the same dominant forces within a behavior, making ratios of just two of these forces less useful. Thus, for a broad comparison of behavior across many orders of magnitude of limb length and cycle period, a dimensionless number that includes gravitational, inertial, elastic, and viscous forces is needed. This study proposes a nondimensional number that relates these four forces: the phase shift (ϕ) between the displacement of the limb and the actuator force that moves it. Using allometric scaling laws, ϕ for terrestrial walking is expressed as a function of the limb length and the cycle period at which the limb steps. Scale-dependent values of ϕ are used to explain and predict the electromyographic (EMG) patterns employed by different animals as they walk.

Spring and latch dynamics can act as control pathways in ultrafast systems.

Ultrafast movements propelled by springs and released by latches are thought limited to energetic adjustments prior to movement, and seemingly cannot adjust once movement begins. Even so, across the tree of life, ultrafast organisms navigate dynamic environments and generate a range of movements, suggesting unrecognized capabilities for control. We develop a framework of control pathways leveraging the non-linear dynamics of spring-propelled, latch-released systems. We analytically model spring dynamics and develop reduced-parameter models of latch dynamics to quantify how they can be tuned internally or through changing external environments. Using Lagrangian mechanics, we test feedforward and feedback control implementation via spring and latch dynamics. We establish through empirically-informed modeling that ultrafast movement can be controllably varied during latch release and spring propulsion. A deeper understanding of the interconnection between multiple control pathways, and the tunability of each control pathway, in ultrafast biomechanical systems presented here has the potential to expand the capabilities of synthetic ultra-fast systems and provides a new framework to understand the behaviors of fast organisms subject to perturbations and environmental non-idealities.

Biomechanics: Passive forces set the stage for stick insects.

For small animals like insects, passive elastic forces within their joints are extremely important to control of limb motion. A new study shows that these passive forces are tuned to the needs of individual joints.

Jumping in lantern bugs (Hemiptera, Fulgoridae).

Lantern bugs are amongst the largest of the jumping hemipteran bugs, with body lengths reaching 44 mm and masses reaching 0.7 g. They are up to 600 times heavier than smaller hemipterans that jump powerfully using catapult mechanisms to store energy. Does a similar mechanism also propel jumping in these much larger insects? The jumping performance of two species of lantern bugs (Hemiptera, Auchenorrhyncha, family Fulgoridae) from India and Malaysia was therefore analysed from high-speed videos. The kinematics showed that jumps were propelled by rapid and synchronous movements of both hind legs, with their trochantera moving first. The hind legs were 20-40% longer than the front legs, which was attributable to longer tibiae. It took 5-6 ms to accelerate to take-off velocities reaching 4.65 m s-1 in the best jumps by female Kalidasa lanata. During these jumps, adults experienced an acceleration of 77 g, required an energy expenditure of 4800 µJ and a power output of 900 mW, and exerted a force of 400 mN. The required power output of the thoracic jumping muscles was 21,000 W kg-1, 40 times greater than the maximum active contractile limit of muscle. Such a jumping performance therefore required a power amplification mechanism with energy storage in advance of the movement, as in their smaller relatives. These large lantern bugs are near isometrically scaled-up versions of their smaller relatives, still achieve comparable, if not higher, take-off velocities, and outperform other large jumping insects such as grasshoppers.

Gravity and active acceleration limit the ability of killer flies (Coenosia attenuata) to steer towards prey when attacking from above.

Insects that predate aerially usually contrast prey against the sky and attack upwards. However, killer flies (Coenosia attenuata) can attack prey flying below them, performing what we term 'aerial dives'. During these dives, killer flies accelerate up to 36 m s-2. Although the trajectories of the killer fly's dives appear highly variable, proportional navigation explains them, as long as the model has the lateral acceleration limit of a real killer fly. The trajectory's steepness is explained by the initial geometry of engagement; steep attacks result from the killer fly taking off when the target is approaching the predator. Under such circumstances, the killer fly dives almost vertically towards the target, and gravity significantly increases its acceleration. Although killer flies usually time their take-off to minimize flight duration, during aerial dives killer flies cannot reach the lateral accelerations necessary to match the increase in speed caused by gravity. Since a close miss still leads the predator closer to the target, and might even slow the prey down, there may not be a selective pressure for killer flies to account for gravity during aerial dives.

Adhesive latching and legless leaping in small, worm-like insect larvae.

Jumping is often achieved using propulsive legs, yet legless leaping has evolved multiple times. We examined the kinematics, energetics and morphology of long-distance jumps produced by the legless larvae of gall midges (Asphondylia sp.). They store elastic energy by forming their body into a loop and pressurizing part of their body to form a transient 'leg'. They prevent movement during elastic loading by placing two regions covered with microstructures against each other, which likely serve as a newly described adhesive latch. Once the latch releases, the transient 'leg' launches the body into the air. Their average takeoff speeds (mean: 0.85 m s-1; range: 0.39-1.27 m s-1) and horizontal travel distances (up to 36 times body length or 121 mm) rival those of legged insect jumpers and their mass-specific power density (mean: 910 W kg-1; range: 150-2420 W kg-1) indicates the use of elastic energy storage to launch the jump. Based on the forces reported for other microscale adhesive structures, the adhesive latching surfaces are sufficient to oppose the loading forces prior to jumping. Energetic comparisons of insect larval crawling versus jumping indicate that these jumps are orders of magnitude more efficient than would be possible if the animals had crawled an equivalent distance. These discoveries integrate three vibrant areas in engineering and biology - soft robotics, small, high-acceleration systems, and adhesive systems - and point toward a rich, and as-yet untapped area of biological diversity of worm-like, small, legless jumpers.

Insect jumping springs.

A quick guide to the springs used by insects to achieve remarkable feats of jumping.

Muscle-spring dynamics in time-limited, elastic movements.

Muscle contractions that load in-series springs with slow speed over a long duration do maximal work and store the most elastic energy. However, time constraints, such as those experienced during escape and predation behaviours, may prevent animals from achieving maximal force capacity from their muscles during spring-loading. Here, we ask whether animals that have limited time for elastic energy storage operate with springs that are tuned to submaximal force production. To answer this question, we used a dynamic model of a muscle-spring system undergoing a fixed-end contraction, with parameters from a time-limited spring-loader (bullfrog: Lithobates catesbeiana) and a non-time-limited spring-loader (grasshopper: Schistocerca gregaria). We found that when muscles have less time to contract, stored elastic energy is maximized with lower spring stiffness (quantified as spring constant). The spring stiffness measured in bullfrog tendons permitted less elastic energy storage than was predicted by a modelled, maximal muscle contraction. However, when muscle contractions were modelled using biologically relevant loading times for bullfrog jumps (50 ms), tendon stiffness actually maximized elastic energy storage. In contrast, grasshoppers, which are not time limited, exhibited spring stiffness that maximized elastic energy storage when modelled with a maximal muscle contraction. These findings demonstrate the significance of evolutionary variation in tendon and apodeme properties to realistic jumping contexts as well as the importance of considering the effect of muscle dynamics and behavioural constraints on energy storage in muscle-spring systems.

Take-off speed in jumping mantises depends on body size and a power-limited mechanism.

Many insects such as fleas, froghoppers and grasshoppers use a catapult mechanism to jump, and a direct consequence of this is that their take-off velocities are independent of their mass. In contrast, insects such as mantises, caddis flies and bush crickets propel their jumps by direct muscle contractions. What constrains the jumping performance of insects that use this second mechanism? To answer this question, the jumping performance of the mantis Stagmomantis theophila was measured through all its developmental stages, from 5 mg first instar nymphs to 1200 mg adults. Older and heavier mantises have longer hind and middle legs and higher take-off velocities than younger and lighter mantises. The length of the propulsive hind and middle legs scaled approximately isometrically with body mass (exponent=0.29 and 0.32, respectively). The front legs, which do not contribute to propulsion, scaled with an exponent of 0.37. Take-off velocity increased with increasing body mass (exponent=0.12). Time to accelerate increased and maximum acceleration decreased, but the measured power that a given mass of jumping muscle produced remained constant throughout all stages. Mathematical models were used to distinguish between three possible limitations to the scaling relationships: first, an energy-limited model (which explains catapult jumpers); second, a power-limited model; and third, an acceleration -: limited model. Only the model limited by muscle power explained the experimental data. Therefore, the two biomechanical mechanisms impose different limitations on jumping: those involving direct muscle contractions (mantises) are constrained by muscle power, whereas those involving catapult mechanisms are constrained by muscle energy.

A buckling region in locust hindlegs contains resilin and absorbs energy when jumping or kicking goes wrong.

If a hindleg of a locust slips during jumping, or misses its target during kicking, energy generated by the two extensor tibiae muscles is no longer expended in raising the body or striking a target. How, then, is the energy in a jump (4100-4800 µJ) or kick (1700 µJ) dissipated? A specialised buckling region found in the proximal hind-tibia where the bending moment is high, but not present in the other legs, buckled and allowed the distal part of the tibia to extend. In jumps when a hindleg slipped, it bent by a mean of 23±14 deg at a velocity of 13.4±9.5 deg ms(-1); in kicks that failed to contact a target it bent by 32±16 deg at a velocity of 32.9±9.5 deg ms(-1). It also buckled 8.5±4.0 deg at a rate of 0.063±0.005 deg ms(-1) when the tibia was prevented from flexing fully about the femur in preparation for both these movements. By experimentally buckling this region through 40 deg at velocities of 0.001-0.65 deg ms(-1), we showed that one hindleg could store about 870 µJ on bending, of which 210 µJ was dissipated back to the leg on release. A band of blue fluorescence was revealed at the buckling region under UV illumination that had the two key signatures of the elastic protein resilin. A group of campaniform sensilla 300 µm proximal to the buckling region responded to imposed buckling movements. The features of the buckling region show that it can act as a shock absorber as proposed previously when jumping and kicking movements go wrong.

Biomechanics: an army marching with its stomach.

A novel X-ray technique shows that the internal organs of crawling caterpillars slide past the body walls like pistons in a new kind of legged locomotion.

The mechanics of azimuth control in jumping by froghopper insects.

Many animals move so fast that there is no time for sensory feedback to correct possible errors. The biomechanics of the limbs participating in such movements appear to be configured to simplify neural control. To test this general principle, we analysed how froghopper insects control the azimuth direction of their rapid jumps, using high speed video of the natural movements and modelling to understand the mechanics of the hind legs. We show that froghoppers control azimuth by altering the initial orientation of the hind tibiae; their mean angle relative to the midline closely predicts the take-off azimuth. This applies to jumps powered by both hind legs, or by one hind leg. Modelling suggests that moving the two hind legs at different times relative to each other could also control azimuth, but measurements of natural jumping showed that the movements of the hind legs were synchronised to within 32 mus of each other. The maximum timing difference observed (67 micros) would only allow control of azimuth over 0.4 deg. to either side of the midline. Increasing the timing differences between the hind legs is also energetically inefficient because it decreases the energy available and causes losses of energy to body spin; froghoppers with just one hind leg spin six times faster than intact ones. Take-off velocities also fall. The mechanism of azimuth control results from the mechanics of the hind legs and the resulting force vectors of their tibiae. This enables froghoppers to have a simple transform between initial body position and motion trajectory, therefore potentially simplifying neural control.

The effect of leg length on jumping performance of short- and long-legged leafhopper insects.

To assess the effect of leg length on jumping ability in small insects, the jumping movements and performance of a sub-family of leafhopper insects (Hemiptera, Auchenorrhyncha, Cicadellidae, Ulopinae) with short hind legs were analysed and compared with other long-legged cicadellids (Hemiptera, Auchenorrhyncha, Cicadellidae). Two species with the same jumping characteristics but distinctively different body shapes were analysed: Ulopa, which had an average body length of 3 mm and was squat, and Cephalelus, which had an average body length of 13 mm with an elongated body and head. In both, the hind legs were only 1.4 times longer than the front legs compared with 1.9-2.3 times in other cicadellid leafhoppers. When the length of the hind legs was normalised relative to the cube root of their body mass, their hind legs had a value of 1-1.1 compared with 1.6-2.3 in other cicadellids. The hind legs of Cephalelus were only 20% of the body length. The propulsion for a jump was delivered by rapid and synchronous rotation of the hind legs about their coxo-trochanteral joints in a three-phase movement, as revealed by high-speed sequences of images captured at rates of 5000 s(-1). The hind tarsi were initially placed outside the lateral margins of the body and not apposed to each other beneath the body as in long-legged leafhoppers. The hind legs were accelerated in 1.5 ms (Ulopa) and 2 ms (Cephalelus) and thus more quickly than in the long-legged cicadellids. In their best jumps these movements propelled Ulopa to a take-off velocity of 2.3 m s(-1) and Cephalelus to 2 m s(-1), which matches that of the long-legged cicadellids. Both short-legged species had the same mean take-off angle of 56 degrees but Cephalelus adopted a lower angle of the body relative to the ground (mean 15 degrees) than Ulopa (mean 56 degrees). Once airborne, Cephalelus pitched slowly and rolled quickly about its long axis and Ulopa rotated quickly about both axes. To achieve their best performances Ulopa expended 7 microJ of energy, generated a power output of 7 mW, and exerted a force of 6 mN; Cephalelus expended 23 microJ of energy, generated a power output of 12 mW and exerted a force of 11 mN. There was no correlation between leg length and take-off velocity in the long- and short-legged species, but longer legged leafhoppers had longer take-off times and generated lower ground reaction forces than short-legged leafhoppers, possibly allowing the longer legged leafhoppers to jump from less stiff substrates.

The mechanics of elevation control in locust jumping.

How do animals control the trajectory of ballistic motions like jumping? Targeted jumps by a locust, which are powered by a rapid extension of the tibiae of both hind legs, require control of the take-off angle and speed. To determine how the locust controls these parameters, we used high speed images of jumps and mechanical analysis to reach three conclusions: (1) the extensor tibiae muscle applies equal and opposite torques to the femur and tibia, which ensures that tibial extension accelerates the centre of mass of the body along a straight line; (2) this line is parallel to a line drawn from the distal end of the tibia through the proximal end of the femur; (3) the slope of this line (the angle of elevation) is not affected if the two hind legs extend asynchronously. The mechanics thus uncouple the control of elevation and speed, allowing simplified and independent control mechanisms. Jump elevation is controlled mechanically by the initial positions of the hind legs and jump speed is determined by the energy stored within their elastic processes, which allows us to then propose which proprioceptors are involved in controlling these quantities.

Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing.

Swallowing and biting responses in the marine mollusk Aplysia are both mediated by a cyclical alternation of protraction and retraction movements of the grasping structure, the radula and underlying odontophore, within the feeding apparatus of the animal, the buccal mass. In vivo observations demonstrate that Aplysia biting is associated with strong protractions and rapid initial retractions, whereas Aplysia swallowing is associated with weaker protractions and slower initial retractions. During biting, the musculature joining the radula/odontophore to the buccal mass (termed the "hinge") is stretched more than in swallowing. To test the hypothesis that stretch of the hinge might contribute to rapid retractions observed in biting, we analyzed the hinge's passive properties. During biting, the hinge is stretched sufficiently to assist retraction. In contrast, during swallowing, the hinge is not stretched sufficiently for its passive forces to assist retraction, because the odontophore's anterior movement is smaller than during biting. A quantitative model demonstrated that steady-state passive forces were sufficient to generate the retraction movements observed during biting. Experimental measures of the relative magnitude of the hinge's active and passive forces at the protraction displacements of biting suggest that passive forces are at least a third of the total force.

The risk of nodal metastasis in early adenocarcinoma of the uterine cervix.

A functional and widely accepted definition of microinvasive cervical adenocarcinoma remains elusive. The purpose of this study was to determine at which depth of invasion the likelihood of lymph node metastasis or disease recurrence was so small that conservative surgery could be considered appropriate. Charts of patients with adenocarcinoma of the cervix (ACC) who underwent radical hysterectomy and pelvic lymphadenectomy (n = 98) at Indiana University Medical Center from 1987 to 1998 were retrospectively reviewed. Patients with stage IA1-IB1 lesions were included in the study. Patients treated with preoperative radiotherapy were excluded. Pathologic parameters evaluated included histologic type, depth of stromal invasion (DOI), and the presence of lymphatic vascular space invasion, or lymph node metastases. The patient median age was 39 years (20-65). The median time of follow-up was 30 months (4-124). Lymph node metastases were found in ten patients and 11 developed recurrences. The precise DOI could be measured in 84 patients. Of the 48 patients with cancers with a DOI 5 mm had nodal metastases (P = 0.00069). None of these 48 patients with a tumor DOI 5 mm developed recurrent disease (P = 0.0048). The risk of nodal metastases and recurrence is so low in patients with ACC and DOI

Urine GABA levels in ovarian cancer patients: elevated GABA in malignancy.

The association of malignancy with elevated diamine oxidase (DAO), an enzyme producing gamma-aminobutyric acid (GABA) is well documented. In ovarian cancer, increased DAO occurs in the malignant tissues and plasma. Since higher DAO levels cause GABA accumulation, elevated GABA may occur in ovarian cancer and be reflected in urine. We tested this hypothesis and found that half the ovarian cancer patients had a clearly elevated urine GABA, a result that is in agreement with previous reports on DAO and malignancy. The published findings on DAO, GABA and malignancy suggest that elevated GABA is associated with cancer. This proposal could lead to a GABA urine monitor or new directions in cancer treatment or research.

Primary yolk sac tumor of the rectum.

Extragonadal germ cell tumors are well recognized in men but have rarely been reported in women. Reports have primarily focused on the pediatric population and have suggested a poor prognosis for extragonadal yolk sac tumors. A 23-year-old woman with a yolk sac tumor arising in the rectum is described. A review of the English-language literature (MEDLINE 1966-1998) regarding extragonadal germ cell tumors in females is provided. Treatment with four courses of cisplatin, etoposide, and bleomycin was followed by surgical resection of the involved area. No residual tumor was identified. She remains disease free 3.5 years later. Previous reports are limited by the small number of patients, focus on the pediatric population, and treatment before the availability of cisplatin. Extragonadal germ cell tumors in women are extremely rare but can be successfully treated with aggressive chemotherapy and surgery similar to testis cancer.

Phase I trial of paclitaxel and etoposide for recurrent ovarian carcinoma: a Gynecologic Oncology Group Study.

A phase I study was performed to determine the maximum tolerated doses of intravenous etoposide and paclitaxel for women with previously treated persistent or recurrent ovarian cancer. Starting doses were paclitaxel 135 mg/m2 during 24 hours and etoposide 50 mg/m2/day for 3 consecutive days. The study was designed to escalate first the dose of etoposide, and then the dose of paclitaxel, in successive cohorts of patients. In an attempt to determine whether toxicity was affected by sequence of the drugs, the order of administration of the two drugs was reversed on alternate cycles. The starting doses of paclitaxel (135 mg/m2/24 hours) and etoposide (50 mg/m2/day x 3) caused severe neutropenia even with the addition of granulocyte colony-stimulating factor, and the trial was amended to administer the paclitaxel during 3 hours. However, this also proved too myelosuppressive without growth factor support. Twenty-one women were treated. A complete response was observed in one of nine patients with measurable disease, and a major decrease in CA-125 was noted in two patients who did not have measurable disease. Because of the severe myelosuppression observed in most patients, dose reduction was often required after the first cycle. The power to detect sequence-dependent variation in toxicity was minimal; however, no large differences were observed. A combination of the usual doses of these drugs will be difficult to administer in patients who have received previous chemotherapy for ovarian cancer.