Journal: The Journal of experimental biology
Many animals live in groups because of the potential benefits associated with defense and foraging. Group living may also induce a ‘calming effect’ on individuals, reducing overall metabolic demand. This effect could occur by minimising the need for individual vigilance and reducing stress through social buffering. However, this effect has proved difficult to quantify. We examined the effect of shoaling on metabolism and body condition in the gregarious damselfish Chromis viridis Using a novel respirometry methodology for social species, we found that the presence of shoal-mate visual and olfactory cues led to a reduction in the minimum metabolic rate of individuals. Fish held in isolation for 1 week also exhibited a reduction in body condition when compared with those held in shoals. These results indicate that social isolation as a result of environmental disturbance could have physiological consequences for gregarious species.
A prominent feature of gliding flight in snakes of the genus Chrysopelea is the unique cross-sectional shape of the body, which acts as the lifting surface in the absence of wings. When gliding, the flying snake Chrysopelea paradisi morphs its circular cross-section into a triangular shape by splaying its ribs and flattening its body in the dorsoventral axis, forming a geometry with fore-aft symmetry and a thick profile. Here, we aimed to understand the aerodynamic properties of the snake’s cross-sectional shape to determine its contribution to gliding at low Reynolds numbers. We used a straight physical model in a water tunnel to isolate the effects of 2D shape, analogously to studying the profile of an airfoil of a more typical flyer. Force measurements and time-resolved (TR) digital particle image velocimetry (DPIV) were used to determine lift and drag coefficients, wake dynamics and vortex-shedding characteristics of the shape across a behaviorally relevant range of Reynolds numbers and angles of attack. The snake’s cross-sectional shape produced a maximum lift coefficient of 1.9 and maximum lift-to-drag ratio of 2.7, maintained increases in lift up to 35 deg, and exhibited two distinctly different vortex-shedding modes. Within the measured Reynolds number regime (Re=3000-15,000), this geometry generated significantly larger maximum lift coefficients than many other shapes including bluff bodies, thick airfoils, symmetric airfoils and circular arc airfoils. In addition, the snake’s shape exhibited a gentle stall region that maintained relatively high lift production even up to the highest angle of attack tested (60 deg). Overall, the cross-sectional geometry of the flying snake demonstrated robust aerodynamic behavior by maintaining significant lift production and near-maximum lift-to-drag ratios over a wide range of parameters. These aerodynamic characteristics help to explain how the snake can glide at steep angles and over a wide range of angles of attack, but more complex models that account for 3D effects and the dynamic movements of aerial undulation are required to fully understand the gliding performance of flying snakes.
Crocodilians are among the most vocal non-avian reptiles. Adults of both sexes produce loud vocalizations known as ‘bellows’ year round, with the highest rate during the mating season. Although the specific function of these vocalizations remains unclear, they may advertise the caller’s body size, because relative size differences strongly affect courtship and territorial behaviour in crocodilians. In mammals and birds, a common mechanism for producing honest acoustic signals of body size is via formant frequencies (vocal tract resonances). To our knowledge, formants have to date never been documented in any non-avian reptile, and formants do not seem to play a role in the vocalizations of anurans. We tested for formants in crocodilian vocalizations by using playbacks to induce a female Chinese alligator (Alligator sinensis) to bellow in an airtight chamber. During vocalizations, the animal inhaled either normal air or a helium/oxygen mixture (heliox) in which the velocity of sound is increased. Although heliox allows normal respiration, it alters the formant distribution of the sound spectrum. An acoustic analysis of the calls showed that the source signal components remained constant under both conditions, but an upward shift of high-energy frequency bands was observed in heliox. We conclude that these frequency bands represent formants. We suggest that crocodilian vocalizations could thus provide an acoustic indication of body size via formants. Because birds and crocodilians share a common ancestor with all dinosaurs, a better understanding of their vocal production systems may also provide insight into the communication of extinct Archosaurians.
Nociception allows for immediate reflex withdrawal whereas pain allows for longer-term protection via rapid learning. We examine here whether shore crabs placed within a brightly lit chamber learn to avoid one of two dark shelters when that shelter consistently results in shock. Crabs were randomly selected to receive shock or not prior to making their first choice and were tested again over 10 trials. Those that received shock in trial 2, irrespective of shock in trial 1, were more likely to switch shelter choice in the next trial and thus showed rapid discrimination. During trial 1, many crabs emerged from the shock shelter and an increasing proportion emerged in later trials, thus avoiding shock by entering a normally avoided light area. In a final test we switched distinctive visual stimuli positioned above each shelter and/or changed the orientation of the crab when placed in the chamber for the test. The visual stimuli had no effect on choice, but crabs with altered orientation now selected the shock shelter, indicating that they had discriminated between the two shelters on the basis of movement direction. These data, and those of other recent experiments, are consistent with key criteria for pain experience and are broadly similar to those from vertebrate studies.
Mammalian hair cells possess only a limited ability to repair damage after trauma. In contrast, sea anemones show a marked capability to repair damaged hair bundles by means of secreted repair proteins (RPs). Previously, it was found that recovery of traumatized hair cells in blind cavefish was enhanced by anemone-derived RPs; therefore, the ability of anemone RPs to assist recovery of damaged hair cells in mammals was tested here. After a 1 h incubation in RP-enriched culture media, uptake of FM1-43 by experimentally traumatized murine cochlear hair cells was restored to levels comparable to those exhibited by healthy controls. In addition, RP-treated explants had significantly more normally structured hair bundles than time-matched traumatized control explants. Collectively, these results indicate that anemone-derived RPs assist in restoring normal function and structure of experimentally traumatized hair cells of the mouse cochlea.
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.
Cursorial ground birds are paragons of bipedal running that span a 500-fold mass range from quail to ostrich. Here we investigate the task-level control priorities of cursorial birds by analysing how they negotiate single-step obstacles that create a conflict between body stability (attenuating deviations in body motion) and consistent leg force-length dynamics (for economy and leg safety). We also test the hypothesis that control priorities shift between body stability and leg safety with increasing body size, reflecting use of active control to overcome size-related challenges. Weight-support demands lead to a shift towards straighter legs and stiffer steady gait with increasing body size, but it remains unknown whether non-steady locomotor priorities diverge with size. We found that all measured species used a consistent obstacle negotiation strategy, involving unsteady body dynamics to minimise fluctuations in leg posture and loading across multiple steps, not directly prioritising body stability. Peak leg forces remained remarkably consistent across obstacle terrain, within 0.35 body weights of level running for obstacle heights from 0.1 to 0.5 times leg length. All species used similar stance leg actuation patterns, involving asymmetric force-length trajectories and posture-dependent actuation to add or remove energy depending on landing conditions. We present a simple stance leg model that explains key features of avian bipedal locomotion, and suggests economy as a key priority on both level and uneven terrain. We suggest that running ground birds target the closely coupled priorities of economy and leg safety as the direct imperatives of control, with adequate stability achieved through appropriately tuned intrinsic dynamics.
Understanding the external stimuli and natural contexts that elicit complex behaviors, such as parental care, is key in linking behavioral mechanisms to their real-life function. Poison frogs provide obligate parental care by shuttling their tadpoles from terrestrial clutches to aquatic nurseries, but little is known about the proximate mechanisms that control these behaviors. In this study, we used Allobates femoralis, a poison frog with predominantly male parental care, to investigate whether tadpole transport can be induced in both sexes by transferring unrelated tadpoles to the backs of adults in the field. Specifically, we asked if the presence of tadpoles on an adult’s back can override the decision-making rules preceding tadpole pick-up and induce the recall of spatial memory necessary for finding tadpole deposition sites. We used telemetry to facilitate accurate tracking of individual frogs and spatial analyses to compare movement trajectories. All tested individuals transported their foster-tadpoles to water pools outside their home area. Contrary to our expectation, we found no sex difference in the likelihood to transport nor in the spatial accuracy of finding tadpole deposition sites. We reveal that a stereotypical cascade of parental behaviors that naturally involves sex-specific offspring recognition strategies and the use of spatial memory can be manipulated by experimental placement of unrelated tadpoles on adult frogs. As individuals remained inside their home area when only the jelly from tadpole-containing clutches was brushed on the back, we speculate that tactile rather than chemical stimuli are triggering these parental behaviors.
Fishes commonly use their lateral line system to detect moving bodies such as prey and predators. A remarkable case is the Mexican blind cavefish Astyanax fasciatus who evolved the ability to detect non-moving obstacles. The swimming body of A. fasciatus generates fluid disturbances, whose alteration by an obstacle can be sensed by the fish’s lateral line system. It is generally accepted that these alterations can provide information on the distance to the obstacle. We observed that A. fasciatus swimming in an unfamiliar environment open and close their mouths at high frequency (0.7-4.5 Hz), in order to generate suction flows. We hypothesized that repeated mouth suction generate a hydrodynamic velocity field, whose alterations by an obstacle induce pressure gradients in the neuromasts of the lateral line, and corresponding strong lateral line stimuli. We observed that the frequency and rates of mouth opening events varied with the fish’s distance to obstacles, a hallmark of pulse-based navigation mechanisms such as echolocation. We formulated a mathematical model of this hitherto unrecognized mechanism of obstacle detection and parameterized it experimentally. This model suggests that suction flows induce lateral line stimuli that are weakly dependent on the fish’s speed, and may be an order of magnitude stronger than the correspondent stimuli induced by the fish’s gliding body. We illustrate that A. fasciatus can navigate non-visually using a combination of two deeply ancestral and highly conserved mechanisms of ray-finned fishes: the mechanism of sensing water motion by the lateral line system and the mechanism of generating water motion by mouth suction.
Toxocara canis is a parasitic nematode that infects canines worldwide, and as a consequence of the widespread environmental dissemination of its ova in host faeces, other abnormal hosts including mice and humans are exposed to infection. In such abnormal or paratenic hosts, the immature third-stage larvae undergo a somatic migration through the organs of the body but fail to reach maturity as adult worms in the intestine. The presence of the migrating larvae contributes to pathology that is dependent upon the intensity of infection and the location of the larvae. A phenomenon of potential public health significance in humans and of ecological significance in mice is that T. canis larvae exhibit neurotrophic behaviour, which results in a greater concentration of parasites in the brain, as infection progresses. Toxocara larval burdens vary between individual outbred mice receiving the same inocula, suggesting a role for immunity in the establishment of cerebral infection. Although the systemic immune response to T. canis has been widely reported, the immune response in the brain has received little attention. Differential cytokine expression and other brain injury-associated biomarkers have been observed in infected versus uninfected outbred and inbred mice. Preliminary data have also suggested a possible link between significant memory impairment and cytokine production associated with T. canis infection. Mice provide a useful, replicable animal model with significant applicability and ease of manipulation. Understanding the cerebral host-parasite relationship may shed some light on the cryptic symptoms of human infection where patients often present with other CNS disorders such as epilepsy and mental retardation.