What factors influence the rediscovery of lost tetrapod species?

We created a database of lost and rediscovered tetrapod species, identified patterns in their distribution and factors influencing rediscovery. Tetrapod species are being lost at a faster rate than they are being rediscovered, due to slowing rates of rediscovery for amphibians, birds and mammals, and rapid rates of loss for reptiles. Finding lost species and preventing future losses should therefore be a conservation priority. By comparing the taxonomic and spatial distribution of lost and rediscovered tetrapod species, we have identified regions and taxa with many lost species in comparison to those that have been rediscovered-our results may help to prioritise search effort to find them. By identifying factors that influence rediscovery, we have improved our ability to broadly distinguish the types of species that are likely to be found from those that are not (because they are likely to be extinct). Some lost species, particularly those that are small and perceived to be uncharismatic, may have been neglected in terms of conservation effort, and other lost species may be hard to find due to their intrinsic characteristics and the characteristics of the environments they occupy (e.g. nocturnal species, fossorial species and species occupying habitats that are more difficult to survey such as wetlands). These lost species may genuinely await rediscovery. However, other lost species that possess characteristics associated with rediscovery (e.g. large species) and that are also associated with factors that negatively influence rediscovery (e.g. those occupying small islands) are more likely to be extinct. Our results may foster pragmatic search protocols that prioritise lost species likely to still exist.

Communication via Biotremors in the Veiled Chameleon (Chamaeleo calyptratus): Part II-Social Contexts.

This study extends recent research demonstrating that the veiled chameleon (Chamaeleo calyptratus) can produce and detect biotremors. Chameleons were paired in various social contexts: dominance (male-male; female-female C. calyptratus); courtship (male-female C. calyptratus); heterospecific (C. calyptratus + C. gracilis); and inter-size class dominance (adult + juvenile C. calyptratus). Simultaneous video and accelerometer recordings were used to monitor their behavior and record a total of 398 biotremors. Chamaeleo calyptratus produced biotremors primarily in conspecific dominance and courtship contexts, accounting for 84.7% of the total biotremors recorded, with biotremor production varying greatly between individuals. Biotremors were elicited by visual contact with another conspecific or heterospecific, and trials in which chameleons exhibited visual displays and aggressive behaviors were more likely to record biotremors. Three classes of biotremor were identified-hoots, mini-hoots, and rumbles, which differed significantly in fundamental frequency, duration, and relative intensity. Biotremor frequency decreased with increasing signal duration, and frequency modulation was evident, especially in hoots. Overall, the data show that C. calyptratus utilizes substrate-borne vibrational communication during conspecific and possibly heterospecific interactions.

Communication via Biotremors in the Veiled Chameleon (Chamaeleo calyptratus): Part I- Biotremor Production and Response to Substrate-Borne Vibrations.

Biotremors are vibrations, usually surface waves along the boundary of a medium, produced by an organism. While substrate-borne vibrations are utilized by different reptile species, true conspecific communication via biotremors has not yet been demonstrated in lizards. Recent research revealed that the veiled chameleon (Chamaeleo calyptratus) produces biotremors. The prerequisites for any communication system are the ability of an organism to produce and detect a signal. We tested C. calyptratus behavioral responses to vibrations by placing them on a dowel attached to a shaker, emitting vibrations of 25, 50, 150, 300, and 600 Hz and compared their locomotory velocity before and after the stimulus. Adult chameleons exhibited a freeze response to 50 and 150 Hz, while juveniles exhibited a similar response to frequencies between 50 and 300 Hz. In a second experiment, chameleons were induced to produce biotremors via experimenter contact. These biotremors ranged in mean fundamental frequency from 106.4 to 170.3 Hz and in duration from 0.06 to 0.29 s. Overall, two classes of biotremors were identified, "hoots" and "mini-hoots," which differed significantly in mean relative signal intensity (-7.5 and -32.5 dB, respectively). Juvenile chameleons 2 months of age were able to produce biotremors, suggesting this behavior may serve a wide range of ecological functions throughout ontogeny. Overall, the data demonstrate that C. calyptratus can both produce and detect biotremors that could be used for intraspecific communication.

The functional basis for variable antipredatory behavioral strategies in the chameleon Chamaeleo calyptratus.

To counterbalance demands of different selective pressures, many species possess morphological, physiological and behavioral specializations that increase survival in their environments. Predation is one such pressure that can elicit multiple adaptive responses, and the effectiveness of antipredator behaviors likely vary both by environment and individual across time. Chameleons use multiple antipredator strategies, many of which vary with body size and habitat type. Although their unique morphological and physiological traits produce relatively slow locomotion, which is poorly suited for fleeing, chameleons can also use crypsis or aggression to avoid predation. To examine the functional basis for variable antipredator behavioral responses, we subjected chameleons to a series of mock predation trials and determined how often individuals adopted each antipredator strategy, and then quantified the performance capacities underlying each strategy. In particular, we measured bite force as a determinant for aggression, sprint velocity for fleeing, and degree of color change for crypsis. We found that aggression was predicted by traits associated with higher absolute and relative bite force, as well as habitat type; fleeing was predicted by higher normalized sprint velocity and habitat type; and crypsis was predicted by habitat type, color change capacity in bird color space and the interaction between the two. These results illustrate the importance of considering both functional capacity and environmental context in antipredator behavior decision-making.

Relationship between gene expression networks and muscle contractile physiology differences in Anolis lizards.

Muscles facilitate most animal behavior, from eating to fleeing. However, to generate the variation in behavior necessary for survival, different muscles must perform differently; for instance, sprinting requires multiple rapid muscle contractions, whereas biting may require fewer contractions but greater force. Here, we use a transcriptomic approach to identify genes associated with variation in muscle contractile physiology among different muscles from the same individual. We measured differential gene expression between a leg and jaw muscle of Anolis lizards known to differ in muscle contractile physiology and performance. For each individual, one muscle was used to measure muscle contractile physiology, including contractile velocity (Vmax and V40), specific tension, power ratio, and twitch time, whereas the contralateral muscle was used to extract RNA for transcriptomic sequencing. Using the transcriptomic data, we found clear clustering of muscle type. Expression of genes clustered in gene ontology (GO) terms related to muscle contraction and extracellular matrix was, on average, negatively correlated with Vmax and slower twitch times but positively correlated to power ratio and V40. Conversely, genes related to the GO terms related to aerobic respiration were downregulated in muscles with higher power ratio and V40, and over-expressed as twitch time decreased. Determining the molecular mechanisms that underlie variation in muscle contractile physiology can begin to explain how organisms are able to optimize behavior under variable conditions. Future studies pursuing the effects of differential gene expression across muscle types in different environments might inform researchers about how differences develop across species, populations, and individuals varying in ecological history.

Temperature effects on the jumping performance of house crickets.

Insect jumping and other explosive animal movements often make use of elastic-recoil mechanisms to enhance performance. These mechanisms circumvent the intrinsic rate limitations on muscle shortening, allowing for greater power production as well as thermal robustness of the associated movements. Here we examine the performance and temperature effects on jumping in the house cricket, Acheta domesticus, using high-speed imaging and inverse dynamics analysis. We find that adult house crickets jumped with greater performance than would be possible using direct muscle shortening, generating a peak power of over 2000 W/kg of muscle mass and maintaining high performance across the entire tested range of body temperatures (12-32°C). Performance declined at the lowest temperature (12°C), yet jump power still exceeds available muscle power. These results reveal that Acheta domesticus makes use of an elastic-recoil mechanism that enhances both the performance and thermal robustness of jumping.

The role of hyoid muscles in biotremor production in Chamaeleo calyptratus.

The production of biotremors has been described in veiled chameleons (Chamaeleo calyptratus), but the mechanism by which they are produced is unknown. We gathered muscle activation data via electromyography (EMG), with simultaneous recordings of biotremors using an accelerometer, to test for the role of hyoid muscles in biotremor production. We recorded a mean biotremor frequency of 150.87 Hz for females and 136.01 Hz for males. The durations of activity and the latencies to onset and offset for the M. sternohyoideus profundus (SP), M. sternohyoideus superficialis (SS), Mm. mandibulohyoideus (MH) and M. levator scapulae (LS) were all significantly correlated with biotremor durations and biotremor onset and offset, respectively. Linear mixed-effect regression model comparisons of biotremor duration indicated that models containing either the MH and/or the SP and LS account for the most variation in biotremor duration. Twitch times for the SP (100 ms) and the SS (132 ms) at field active body temperature, however, were individually too slow to produce the biotremors at the observed frequency without alteration after production by other anatomical structures. These results implicate the SP, SS, MH and LS in the production of biotremors, but the exact mechanism of production requires further study.

The only complete articulated early Miocene chameleon skull (Rusinga Island, Kenya) suggests an African origin for Madagascar's endemic chameleons.

We here present the first detailed study of the specimen KNM-RU 18340 from Rusinga Island (Kenya), the only known complete early Miocene chameleon skull, using micro-CT. This specimen represents one of the oldest chameleon fossils ever recovered. For the first time, the skull bone internal surfaces, their sutures, and elements contained inside the rocky matrix are observed. Our morphological comparisons and phylogenetic analyses place this specimen confidently in the genus Calumma and a new species, Calumma benovskyi sp. nov., is erected for it. Since all species of this genus are endemic to Madagascar, this fossil uniquely demonstrates the existence of Calumma on continental Africa in the past. Our results challenge the long-held view that chameleons originated on Madagascar and dispersed over water to Africa, and provide a strong evidence of an African origin for some Malagasy lineages. The Oligocene-early Miocene dispersal to Madagascar, using oceanic currents that favoured eastward dispersal at that time, is a highly supported scenario matching the suggested dispersal of lemurs to this island. This is consistent with a previously suggested hypothesis based on molecular data.

Gular pouch diversity in the Chamaeleonidae.

Numerous chameleon species possess an out-pocketing of the trachea known as the gular pouch. After surveying more than 250 specimens, representing nine genera and 44 species, we describe two different morphs of the gular pouch. Species of the genera Bradypodion and Chamaeleo, as well as Trioceros goetzei, all possess a single gular pouch (morph one) formed from ventral expansion of soft tissue where the larynx and trachea meet. Furcifer oustaleti and Furcifer verrucosus possess from one to four gular pouches (morph two) formed by the expansion of soft tissue between sequential hyaline cartilage rings of the trachea. In Trioceros melleri, examples of both morphs of the gular pouch were observed. Morphometric data are presented for 100 animals representing eight species previously known to possess a gular pouch and two additional species, Bradypodion thamnobates and Bradypodion transvaalense. In the species with the absolutely and relatively largest gular pouch, Chamaeleo calyptratus, a significant difference was found between sexes in its width and volume, but not its length. In C. calyptratus, we show that an inflated gular pouch is in contact with numerous hyoid muscles and the tongue. Coupled with the knowledge that C. calyptratus generates vibrations from the throat region, we posit that the tongue (M. accelerator linguae and M. hyoglossus) and supporting hyoid muscles (i.e., Mm. sternohyoideus profundus et superficialis and Mm. mandibulohyoideus) are involved in the production of vibrations to produce biotremors that are amplified by the inflated gular pouch and used in substrate-borne communication.

The need for speed: functional specializations of locomotor and feeding muscles in Anolis lizards.

Muscles often perform diverse mechanical roles within an organism. Tuning of contractile properties may therefore provide an opportunity for muscles to better perform their different roles and impact their associated whole-organism performance. Here, we examined the muscle contractile physiology of a jaw and a leg muscle in five Anolis species to determine whether consistent physiological differences are found in these muscles. We found that these jaw and leg muscles exhibited consistent patterns of variation across species, which may be related to the functional use of each muscle. In particular, we found that each muscle had differentially increased different measures of muscle speed. Although the jaw muscles had faster peak contractile velocities than the leg muscles, the leg muscles had faster twitch times and faster contractile velocities under intermediate loads. We also found that the jaw muscles exerted higher specific tensions and had a greater curvature to their force-velocity relationship. The consistent patterns across five species suggest that these jaw and leg muscles have specialized in different ways. Examination of these contractile property variations may help illuminate important features relating to performing their individual functional roles.

Off like a shot: scaling of ballistic tongue projection reveals extremely high performance in small chameleons.

Stretching elastic tissues and using their recoil to power movement allows organisms to release energy more rapidly than by muscle contraction directly, thus amplifying power output. Chameleons employ such a mechanism to ballistically project their tongue up to two body lengths, achieving power outputs nearly three times greater than those possible via muscle contraction. Additionally, small organisms tend to be capable of greater performance than larger species performing similar movements. To test the hypothesis that small chameleon species outperform larger species during ballistic tongue projection, performance was examined during feeding among 20 chameleon species in nine genera. This revealed that small species project their tongues proportionately further than large species, achieving projection distances of 2.5 body lengths. Furthermore, feedings with peak accelerations of 2,590 m s(-2), or 264 g, and peak power output values of 14,040 W kg(-1) are reported. These values represent the highest accelerations and power outputs reported for any amniote movement, highlighting the previously underestimated performance capability of the family. These findings show that examining movements in smaller animals may expose movements harbouring cryptic power amplification mechanisms and illustrate how varying metabolic demands may help drive morphological evolution.

Captive Care, Raising, and Breeding of the Veiled Chameleon (Chamaeleo calyptratus).

Squamate reptiles comprise approximately one-third of all living amniotes. In most of these species, it is difficult to study gastrulation and neurulation because the embryos are at a late stage of development at the time of oviposition. This is not the case, however, in veiled chameleons (Chamaeleo calyptratus), which are increasingly being used as a model organism to study these and other developmental and evolutionary phenomena. Originating from the Arabian Peninsula, veiled chameleons are arboreal specialists that possess extensive morphological specializations for climbing. They naturally inhabit semitropical habitats, but they also have an almost 30-yr history of being bred in captivity. Veiled chameleons breed readily and do not require a period of cooling to induce the reproductive cycle, and females can produce ∼45-90 eggs multiple times per year. Thus, compared with other reptiles, relatively few animals are needed to maintain a productive breeding colony. Herein, we present the conditions, equipment, and techniques required for proper husbandry and breeding of veiled chameleons within a laboratory environment.

The Veiled Chameleon (Chamaeleo calyptratus Duméril and Duméril 1851): A Model for Studying Reptile Body Plan Development and Evolution.

Vertebrate model organisms have facilitated the discovery and exploration of morphogenetic events and developmental pathways that underpin normal and pathological embryological events. In contrast to amniotes such as Mus musculus (Mammalia) and Gallus gallus (Aves), our understanding of early patterning and developmental events in reptiles (particularly nonavians) remains weak. Squamate reptiles (lizards, snakes, and amphisbaenians) comprise approximately one-third of all living amniotes. But studies of early squamate development have been limited because, in most members of this lineage, embryo development at the time of oviposition is very advanced (limb bud stages and older). In many cases, squamates give birth to fully developed offspring. However, in the veiled chameleon (Chamaeleo calyptratus), embryos have progressed only to a primitive pregastrula stage at the time of oviposition. Furthermore, the body plan of the veiled chameleon is highly specialized for climbing in an arboreal environment. It possesses an entire suite of skeletal and soft anatomical modifications, including cranioskeletal ornamentation, lingual anatomy and biomechanics for projection, autopodial clefting for grasping, adaptations for rapid integumental color changes, a prehensile tail with a lack of caudal autotomy, the loss of the tympanum in the middle ear, and the acquisition of turreted eyes. Thus, C. calyptratus is an important model organism for studying the role of ecological niche specialization, as well as genetic and morphological evolution within an adaptive framework. More importantly, this species is easily bred in captivity, with only a small colony (<10 individuals) needed to obtain hundreds of embryos every year.

Thermal effects on the performance, motor control and muscle dynamics of ballistic feeding in the salamander Eurycea guttolineata.

Temperature strongly affects muscle contractile rate properties and thus may influence whole-organism performance. Movements powered by elastic recoil, however, are known to be more thermally robust than muscle-powered movements. We examined the whole-organism performance, motor control and muscle contractile physiology underlying feeding in the salamander Eurycea guttolineata. We compared elastically powered tongue projection with the associated muscle-powered retraction to determine the thermal robustness of each of these functional levels. We found that tongue-projection distance in E. guttolineata was unaffected by temperature across the entire 4-26°C range, tongue-projection dynamics were significantly affected by temperature across only the 4-11°C interval, and tongue retraction was affected to a higher degree across the entire temperature range. The significant effect of temperature on projection dynamics across the 4-11°C interval corresponds to a significant decline in projector muscle burst intensity and peak contractile force of the projector muscle across the same interval. Across the remaining temperature range, however, projection dynamics were unaffected by temperature, with muscle contractile physiology showing typical thermal effects and motor patterns showing increased activity durations and latencies. These results reveal that elastically powered tongue-projection performance in E. guttolineata is maintained to a higher degree than muscle-powered tongue retraction performance across a wide temperature range. These results further indicate that thermal robustness of the elastically powered movement is dependent on motor control and muscle physiology that results in comparable energy being stored in elastic tissues across a range of temperatures.

Comparative feeding kinematics of tropical hylid tadpoles.

Anuran larvae, which are otherwise simple in shape, typically have complex keratinized mouthparts (i.e. labial teeth and jaw sheaths) that allow them to graze upon surfaces. The diversity in these structures among species presumably reflects specializations that allow for maximal feeding efficiency on different types of food. However, we lack a general understanding of how these oral structures function during feeding. We used high-speed digital imaging (500 Hz) to observe tadpoles of six species from the anuran family Hylidae grazing on a standardized food-covered substrate. Tadpoles of these species vary in the number of labial tooth rows, belong to two different feeding guilds (benthic and nektonic), and inhabit ponds and streams. We confirmed that the labial teeth in these species serve two functions: anchoring the mouth to the substrate and raking material off of the substrate. In general, tadpoles with a larger maximum gape or those with fewer labial tooth rows opened and closed their mouths slower than tadpoles with smaller gape or more tooth rows. Nektonic feeding tadpoles released each of their tooth rows proportionally earlier in the gape cycle compared with benthic feeding tadpoles. Lastly, we found some support for the idea that deformation of the jaw sheaths during a feeding cycle is predictable based on tadpole feeding guild. Collectively, our data show that anatomical (e.g. number of labial teeth) and ecological features (e.g. feeding guild) of tadpoles significantly influence how tadpoles open and close their mouths during feeding.

Thermal effects on motor control and in vitro muscle dynamics of the ballistic tongue apparatus in chameleons.

Temperature strongly affects whole-organism performance through its effect on muscle contractile rate properties, but movements powered by elastic recoil are liberated from much of the performance decline experienced by muscle-powered movements at low temperature. We examined the motor control and muscle contractile physiology underlying an elastically powered movement - tongue projection in chameleons - and the associated muscle powered retraction to test the premise that the thermal dependence of muscle contractile dynamics is conserved. We further tested the associated hypothesis that motor control patterns and muscle contractile dynamics must change as body temperature varies, despite the thermal robustness of tongue-projection performance. We found that, over 14-26°C, the latency between the onset of the tongue projector muscle activity and tongue projection was significantly affected by temperature (Q(10) of 2.56), as were dynamic contractile properties of the tongue projector and retractor muscles (Q(10) of 1.48-5.72), supporting our hypothesis that contractile rates slow with decreasing temperature and, as a result, activity durations of the projector muscle increase at low temperatures. Over 24-36°C, thermal effects on motor control and muscle contractile properties declined, indicating that temperature effects are more extreme across lower temperature ranges. Over the entire 14-36°C range, intensity of muscle activity for the tongue muscles was not affected by temperature, indicating that recruitment of motor units in neither muscle increases with decreasing temperature to compensate for declining contractile rates. These results reveal that specializations in morphology and motor control, not muscle contractile physiology, are responsible for the thermal robustness of tongue projection in chameleons.

Scaling of the ballistic tongue apparatus in chameleons.

Body dimensions of organisms can have a profound impact on their functional and structural properties. We examined the morphological proportions of the feeding apparatus of 105 chameleon specimens representing 23 species in seven genera, spanning a 1,000-fold range in body mass to test whether the feeding apparatus conforms to the null hypotheses of geometric similarity that is based on the prevalence of geometric similarity in other ectothermic vertebrates. We used a phylogenetically corrected regression analysis based on a composite phylogenetic hypothesis to determine the interspecific scaling patterns of the feeding apparatus. We also determined the intraspecific (ontogenetic) scaling patterns for the feeding apparatus in three species. We found that both intraspecifically and interspecifically, the musculoskeletal components of the feeding apparatus scale isometrically among themselves, independent of body length. The feeding apparatus is thus of conserved proportions regardless of overall body length. In contrast, we found that the tongue apparatus as a whole and its musculoskeletal components scale with negative allometry with respect to snout-vent length--smaller individuals have a proportionately larger feeding apparatus than larger individuals, both within and among species. Finally, the tongue apparatus as a whole scales with negative allometry with respect to body mass through ontogeny, but with isometry interspecifically. We suggest that the observed allometry may be maintained by natural selection because an enlarged feeding apparatus at small body size may maximize projection distance and the size of prey that smaller animals with higher mass-specific metabolic rates can capture.

Ballistic tongue projection in chameleons maintains high performance at low temperature.

Environmental temperature impacts the physical activity and ecology of ectothermic animals through its effects on muscle contractile physiology. Sprinting, swimming, and jumping performance of ectotherms decreases by at least 33% over a 10 degrees C drop, accompanied by a similar decline in muscle power. We propose that ballistic movements that are powered by recoil of elastic tissues are less thermally dependent than movements that rely on direct muscular power. We found that an elastically powered movement, ballistic tongue projection in chameleons, maintains high performance over a 20 degrees C range. Peak velocity and power decline by only 10%-19% with a 10 degrees C drop, compared to >42% for nonelastic, muscle-powered tongue retraction. These results indicate that the elastic recoil mechanism circumvents the constraints that low temperature imposes on muscle rate properties and thereby reduces the thermal dependence of tongue projection. We propose that organisms that use elastic recoil mechanisms for ecologically important movements such as feeding and locomotion may benefit from an expanded thermal niche.