The Kinematics and Functional Significance of Chemosensory Tongue-Flicking in Northern Water Snakes (Nerodia sipedon) on Land, in Water, and in between.

As organisms transition between different environments, they must do more than simply move through that transition and those environments. Changes in the environment must be detected via the senses. The types of sensory information and the mechanisms of collecting that information may also change as an individual moves through different environments. We use tongue-flicking in northern water snakes, Nerodia sipedon, to examine the mechanics of sensory behavior as snakes move from terrestrial to aquatic habitats. A combination of high-speed video and mesocosm experiment revealed that water snakes will alter the mechanics of tongue-flicking in the context of their environment. Tongue-flicks on land are distinctive, with multiple oscillations, large protrusion distance, and high velocities. Comparatively, tongue-flicks under water are much shorter events, with reduced protrusion and fewer oscillations. At the surface of the water, in the presence of potential anuran prey, water snakes will tap the tips of the tongue on the surface of the water, without undergoing the full oscillations observed on land or underwater. We attribute the differences in the aerial and underwater tongue-flicks to trade-offs in the physical and chemical properties of the environment. The surface tapping behavior we observed is likely snakes altering their behavior to maximize the encounter and collection of frog-specific chemical cues, which are known to travel on the water's surface. Given the ecological transitions and distinctive biogeographical patterns rooted in water snake ecology, there are likely more examples of changing sensory mechanics to be discovered upon further investigation.

The mechanics of air breathing in African clawed frog tadpoles, Xenopus laevis (Anura: Pipidae).

Frog larvae (tadpoles) undergo many physiological, morphological and behavioral transformations throughout development before metamorphosing into their adult form. The surface tension of water prevents small tadpoles from breaching the surface to breathe air (including those of Xenopus laevis), forcing them to acquire air using a form of breathing called bubble sucking. With growth, tadpoles typically make a behavioral/biomechanical transition from bubble sucking to breaching. Xenopus laevis tadpoles have also been shown to transition physiologically from conforming passively to ambient oxygen levels to actively regulating their blood oxygen. However, it is unknown whether these mechanical and physiological breathing transitions are temporally or functionally linked, or how both transitions relate to lung maturation and gas exchange competency. If these transitions are linked, it could mean that one biomechanical breathing mode (breaching) is more physiologically proficient at acquiring gaseous oxygen than the other. Here, we describe the mechanics and development of air breathing and the ontogeny of lung morphology in X. laevis throughout the larval stage and examine our findings considering previous physiological work. We found that the transitions from bubble sucking to breaching and from oxygen conforming to oxygen regulation co-occur in X. laevis tadpoles at the same larval stage (Nieuwkoop-Faber stages 53-56 and 54-57, respectively), but that the lungs do not increase significantly in vascularization until metamorphosis, suggesting that lung maturation, alone, is not sufficient to account for increased pulmonary capacity earlier in development. Although breach breathing may confer a respiratory advantage, we remain unaware of a mechanistic explanation to account for this possibility. At present, the transition from bubble sucking to breaching appears simply to be a consequence of growth. Finally, we consider our results in the context of comparative air-breathing mechanics across vertebrates.

The evolution of sour taste.

The evolutionary history of sour taste has been little studied. Through a combination of literature review and trait mapping on the vertebrate phylogenetic tree, we consider the origin of sour taste, potential cases of the loss of sour taste, and those factors that might have favoured changes in the valence of sour taste-from aversive to appealing. We reconstruct sour taste as having evolved in ancient fish. By contrast to other tastes, sour taste does not appear to have been lost in any major vertebrate taxa. For most species, sour taste is aversive. Animals, including humans, that enjoy the sour taste triggered by acidic foods are exceptional. We conclude by considering why sour taste evolved, why it might have persisted as vertebrates made the transition to land and what factors might have favoured the preference for sour-tasting, acidic foods, particularly in hominins, such as humans.

The functional morphology of lingual prey capture in a scincid lizard, Tiliqua scincoides (Reptilia: Squamata).

We investigated the functional morphology of lingual prey capture in the blue-tongued skink, Tiliqua scincoides, a lingual-feeding lizard nested deep within the family Scincidae, which is presumed to be dominated by jaw-feeding. We used kinematic analysis of high-speed video to characterize jaw and tongue movements during prey capture. Phylogenetically informed principal components analysis of tongue morphology showed that, compared to jaw-feeding scincids and lacertids, T. scincoides and another tongue-feeding scincid, Corucia zebrata, are distinct in ways suggesting an enhanced ability for hydrostatic shape change. Lingual feeding kinematics show substantial quantitative and qualitative variation among T. scincoides individuals. High-speed video analysis showed that T. scincoides uses significant hydrostatic elongation and deformation during protrusion, tongue-prey contact, and retraction. A key feature of lingual prey capture in T. scincoides is extensive hydrostatic deformation to increase the area of tongue-prey contact, presumably to maximize wet adhesion of the prey item. Adhesion is mechanically reinforced during tongue retraction through formation of a distinctive "saddle" in the foretongue that supports the prey item, reducing the risk of prey loss during retraction.

AMARO-An On-Board Ship Detection and Real-Time Information System.

The monitoring of worldwide ship traffic is a field of high topicality. Activities like piracy, ocean dumping, and refugee transportation are in the news every day. The detection of ships in remotely sensed data from airplanes, drones, or spacecraft contributes to maritime situational awareness. However, the crucial factor is the up-to-dateness of the extracted information. With ground-based processing, the time between image acquisition and delivery of the extracted product data is in the range of several hours, mainly due to the time consumed by storing and transmission of the large image data. By processing and analyzing them on-board and transmitting the product data directly as ship position, heading, and velocity, the delay can be shortened to some minutes. Real-time connections via satellite telecommunication services allow small packets of information to be sent directly to the user without significant delay. The AMARO (Autonomous Real-Time Detection of Moving Maritime Objects) project at DLR is a feasibility study of an on-board ship detection system involving on-board processing and real-time communication. The operation of a prototype system was successfully demonstrated on an airborne platform in spring 2018. The on-ground user could be informed about detected vessels within minutes after sighting without a direct communication link. In this article, the scope, aim, and design of the AMARO system are described, and the results of the flight experiment are presented in detail.

Circumventing surface tension: tadpoles suck bubbles to breathe air.

The surface tension of water provides a thin, elastic membrane upon which many tiny animals are adapted to live and move. We show that it may be equally important to the minute animals living beneath it by examining air-breathing mechanics in five species (three families) of anuran (frog) tadpoles. Air-breathing is essential for survival and development in most tadpoles, yet we found that all tadpoles at small body sizes were unable to break through the water's surface to access air. Nevertheless, by 3 days post-hatch and only 3 mm body length, all began to breathe air and fill the lungs. High-speed macrovideography revealed that surface tension was circumvented by a novel behaviour we call 'bubble-sucking': mouth attachment to the water's undersurface, the surface drawn into the mouth by suction, a bubble 'pinched off' within the mouth, then compressed and forced into the lungs. Growing tadpoles transitioned to air-breathing via typical surface breaching. Salamander larvae and pulmonate snails were also discovered to 'bubble-suck', and two insects used other means of circumvention, suggesting that surface tension may have a broader impact on animal phenotypes than hitherto appreciated.

The mechanics of air breathing in gray tree frog tadpoles, Hyla versicolor (Anura: Hylidae).

We describe air-breathing mechanics in gray tree frog tadpoles (Hyla versicolor). We found that H. versicolor tadpoles breathe by 'bubble-sucking', a breathing mode typically employed by tadpoles too small to break the water's surface tension, in which a bubble is drawn into the buccal cavity and compressed into the lungs. In most tadpoles, bubble-sucking is replaced by breach breathing (breaking the surface to access air) at larger body sizes. In contrast, H. versicolor tadpoles bubble-suck throughout the larval period, despite reaching body sizes at which breaching is possible. Hyla versicolor tadpoles exhibit two bubble-sucking behaviors: 'single bubble-sucking', previously described in other tadpole species, is characterized by a single suction event followed by a compression phase to fill the lungs; 'double bubble-sucking' is a novel, apparently derived form of bubble-sucking that adds a second suction event. Hyla versicolor tadpoles transition from single bubble-sucking to double bubble-sucking at approximately 5.7 mm snout-vent length (SVL), which corresponds to a period of rapid lung maturation when they transition from low to high vascularization (6.0 mm SVL). Functional, behavioral and morphological evidence suggests that double bubble-sucking increases the efficiency of pulmonary gas exchange by separating expired, deoxygenated air from freshly inspired air to prevent mixing. Hyla versicolor, and possibly other hylid tadpoles, may have specialized for bubble-sucking in order to take advantage of this increased efficiency. Single and double bubble-sucking represent two- and four-stroke ventilation systems, which we discuss in the context of other anamniote air-breathing mechanisms.

A simple, inexpensive system for digital particle image velocimetry (DPIV) in biomechanics.

Functional morphology and biomechanics seek to reveal the mechanistic bases of organismal functions and the physical principles involved at the phenotype-environment interface. Characterization of fluid flow (air or water) within and around organismal structures is an example of this approach. Digital particle imaging velocimetry (DPIV) has been exploited in a variety of biological systems to visualize fluid flow associated with animal movement. DPIV employs particles suspended in air or water that are illuminated by a laser light sheet and recorded with a high-speed video camera. Software tracks particle movement across a specified number of video frames, generating vector diagrams showing patterns of fluid flow through time. As powerful as DPIV methods are, they are limited in application by the high cost and complexity of the equipment required. In this article, we describe a simple DPIV system that substitutes widely available, inexpensive consumer components for scientific-grade equipment to achieve low cost (<$1,000 total) and high accuracy (total error calculated to be approx. 6%, as compared with 5% in professional systems). We have employed this system successfully in our studies on the fluid dynamics of chemosensory tongue-flicking in snakes. This system can be used for research and teaching in labs that typically cannot afford the expense or commitment of a traditional DPIV apparatus and is particularly suited for obtaining preliminary data required to justify further grant and institutional support.

The mechanism of chemical delivery to the vomeronasal organs in squamate reptiles: a comparative morphological approach.

Vomeronasal chemoreception, an important chemical sense in squamate reptiles (lizards and snakes), is mediated by paired vomeronasal organs (VNOs), which are only accessible via ducts opening through the palate anteriorly. We comparatively examined the morphology of the oral cavity in lizards with unforked tongues to elucidate the mechanism of stage I delivery (transport of chemical-laden fluid from the tongue tips to the VNO fenestrae) and to test the generality of the Gillingham and Clark (1981. Can J Zool 59:1651-1657) hypothesis (based on derived snakes), which suggests that the sublingual plicae act as the direct conveyors of chemicals to the VNOs. At rest, the foretongue lies within a chamber formed by the sublingual plicae ventrally and the palate dorsally, with little or no space around the anterior foretongue when the mouth is closed. There is a remarkable conformity between the shape of this chamber and the shape of the foretongue. We propose a hydraulic mechanism for stage I chemical transport in squamates: during mouth closure, the compliant tongue is compressed within this cavity and the floor of the mouth is elevated, expressing fluid from the sublingual glands within the plicae. Chemical-laden fluid covering the tongue tips is forced dorsally and posteriorly toward the VNO fenestrae. In effect, the tongue acts as a piston, pressurizing the fluid surrounding the foretongue so that chemical transport to the VNO ducts is effected almost instantaneously. Our findings falsify the Gillingham and Clark (1981. Can J Zool 59:1651-1657) hypothesis for lizards lacking forked, retractile tongues.

Grand challenges in organismal biology.

A renaissance in organismal biology has been sparked by recent conceptual, theoretical, methodological, and computational advances in the life sciences, along with an unprecedented interdisciplinary integration with Mathematics, Engineering, and the physical sciences. Despite a decades-long trend toward reductionist approaches to biological problems, it is increasingly recognized that whole organisms play a central role in organizing and interpreting information from across the biological spectrum. Organisms represent the nexus where sub- and supra-organismal processes meet, and it is the performance of organisms within the environment that provides the material for natural selection. Here, we identify five "grand challenges" for future research in organismal biology. It is intended that these challenges will spark further discussion in the broader community and identify future research priorities, opportunities, and directions, which will ultimately help to guide the allocation of support for and training in organismal biology.

Horned lizards (Phrynosoma) incapacitate dangerous ant prey with mucus.

Horned lizards (Iguanidae, Phrynosomatinae, Phrynosoma) are morphologically specialized reptiles characterized by squat, tank-like bodies, short limbs, blunt snouts, spines and cranial horns, among other traits. They are unusual among lizards in the degree to which they specialize on a diet of ants, but exceptional in the number of pugnacious, highly venomous, stinging ants they consume, especially harvester ants (genus Pogonomyrmex). Like other iguanian lizards, they capture insect prey on the tongue, but unlike other lizards, they neither bite nor chew dangerous prey before swallowing. Instead, they employ a unique kinematic pattern in which prey capture, transport and swallowing are combined. Nevertheless, horned lizards consume dozens of harvester ants without harm. We show that their derived feeding kinematics are associated with unique, mucus-secreting pharyngeal papillae that apparently serve to immobilize and incapacitate dangerous ants as they are swallowed by compacting them and binding them in mucus strands. Radially branched esophageal folds provide additional mucus-secreting surfaces the ants pass through as they are swallowed. Ants extracted from fresh-killed horned lizard stomachs are curled ventrally into balls and bound in mucus. We conclude that the pharyngeal papillae, in association with a unique form of hyolingual prey transport and swallowing, are horned lizard adaptations related to a diet of dangerous prey. Harvester ant defensive weapons, along with horned lizard adaptations against such weapons, suggest a long-term, predator-prey, co-evolutionary arms race between Phrynosoma and Pogonomyrmex.

History and the global ecology of squamate reptiles.

The structure of communities may be largely a result of evolutionary changes that occurred many millions of years ago. We explore the historical ecology of squamates (lizards and snakes), identify historically derived differences among clades, and examine how this history has affected present-day squamate assemblages globally. A dietary shift occurred in the evolutionary history of squamates. Iguanian diets contain large proportions of ants, other hymenopterans, and beetles, whereas these are minor prey in scleroglossan lizards. A preponderance of termites, grasshoppers, spiders, and insect larvae in their diets suggests that scleroglossan lizards harvest higher energy prey or avoid prey containing noxious chemicals. The success of this dietary shift is suggested by dominance of scleroglossans in lizard assemblages throughout the world. One scleroglossan clade, Autarchoglossa, combined an advanced vomeronasal chemosensory system with jaw prehension and increased activity levels. We suggest these traits provided them a competitive advantage during the day in terrestrial habitats. Iguanians and gekkotans shifted to elevated microhabitats historically, and gekkotans shifted activity to nighttime. These historically derived niche differences are apparent in extant lizard assemblages and account for some observed structure. These patterns occur in a variety of habitats at both regional and local levels throughout the world.

Morphology of the tongue in the tuatara, Sphenodon punctatus (Reptilia: Lepidosauria), with comments on function and phylogeny.

The morphology and histology of the tongue in Sphenodon punctatus are described and used to infer function and to determine character state polarities in lepidosaurs. The tongue lacks an anterior notch and is covered with filamentous papillae, including specialized gustatory papillae containing taste buds. Lingual glands are restricted to mucocytes covering the papillae. Three intrinsic tongue muscles are identified and shown to be discrete fiber systems and not merely elaborations of the M. hyoglossus. These muscles interact with a connective tissue skeleton, particularly three septal planes, to cause changes in tongue shape. Tongue protrusion is probably caused by hyoid protraction and contraction of posterior genioglossus fibers; retraction by hyoid retraction, hyoglossus contraction, and contraction of anterior genioglossus fibers. It is argued that taste is important in prey discrimination and possibly in courtship. Vomeronasal function is probably mediated by inhalation and not tongue movement. Insertion of genioglossus fibers into the buccal floor is a derived feature of lepidosaur tongues. Derived features of squamate tongues include an anterior bifurcation, a divided genioglossus comprising medial and lateral portions, ventral transverse and circular muscle fiber systems around the hyoglossus, and the presence of a median septum. The tongue of the squamate family Iguanidae shares many plesiomorphic features with Sphenodon.

Predation upon reptiles in Mediterranean habitats of Chile, Spain and California: A comparative analysis.

Pradation on reptiles at three Mediterranean-type habitat sites was assessed by computing the incidence of reptiles as a percentage of vertebrates in the diet of each predator species and the incidence of each reptile species as prey for the entire assemblage of predators at each locality. The overall importance of reptiles is lowest in Chile, intermediate in California, and highest in Spain. These differences do not appear to result from interlocality variation in the size distributions of predators or of prey. The incidence of particular reptile species as prey is correlated with their relative abundances in Spain and California, but not in Chile. Behavioral and morphological attributes evidently make some species more vulnerable to predation and others less so than their abundances would predict. Predation on the speciose lizard genus Liolaemus in Chile is sufficient to promote behavioral responses but not major morphological divergence.