The scaling of terrestrial striking performance in western ratsnakes (Pantherophis obsoletus).

In many organisms, juveniles have performance capabilities that partly offset their disadvantageous sizes. Using high-speed video recordings and imaging software, we measured the scaling of head morphology, axial morphology, and defensive strike performance of Pantherophis obsoletus across their ontogeny to understand how size and morphology affect performance. Head measurements were negatively allometric whereas the cross-sectional area (CSA) of epaxial muscles displayed positive allometry. The greater relative muscle CSA of larger ratsnakes allows them to produce higher forces relative to their mass, and those forces act on a relatively smaller head mass when it is thrust forward during striking. Maximum strike accelerations of 70-273.8 ms-2 and velocities of 1.08-3.39 ms-1 scaled positively with body mass but differed from the geometric predictions. Velocity scaled with mass0.15 and acceleration scaled with mass0.17 . Larger snakes struck from greater distances (range = 4.1-26 cm), but all snakes covered the strike distances with similarly short durations (84 ± 3 ms). The negatively allometric head size, isometry of anterior mass, and positively allometric muscle CSA enable larger P. obsoletus to strike with higher velocities and accelerations than smaller individuals. Our results contrast with the scaling of strike performance in an arboreal viper, whose strike distance and velocity were independent of body mass. When strike distance is modulated, all other performance capacities are affected because of the interdependence of acceleration, velocity, duration, and distance.

The king of snakes: performance and morphology of intraguild predators (Lampropeltis) and their prey (Pantherophis).

Across ecosystems and trophic levels, predators are usually larger than their prey, and when trophic morphology converges, predators typically avoid predation on intraguild competitors unless the prey is notably smaller in size. However, a currently unexplained exception occurs in kingsnakes in the genus Lampropeltis Kingsnakes are able to capture, constrict and consume other snakes that are not only larger than themselves but that are also powerful constrictors (such as ratsnakes in the genus Pantherophis). Their mechanisms of success as intraguild predators on other constrictors remain unknown. To begin addressing these mechanisms, we studied the scaling of muscle cross-sectional area, pulling force and constriction pressure across the ontogeny of six species of snakes (Lampropeltiscaliforniae, L.getula, L.holbrooki, Pantherophisalleghaniensis, P.guttatus and P.obsoletus). Muscle cross-sectional area is an indicator of potential force production, pulling force is an indicator of escape performance, and constriction pressure is a measure of prey-handling performance. Muscle cross-sectional area scaled similarly for all snakes, and there was no significant difference in maximum pulling force among species. However, kingsnakes exerted significantly higher pressures on their prey than ratsnakes. The similar escape performance among species indicates that kingsnakes win in predatory encounters because of their superior constriction performance, not because ratsnakes have inferior escape performance. The superior constriction performance by kingsnakes results from their consistent and distinctive coil posture and perhaps from additional aspects of muscle structure and function that need to be tested in future research.

Debunking the viper's strike: harmless snakes kill a common assumption.

To survive, organisms must avoid predation and acquire nutrients and energy. Sensory systems must correctly differentiate between potential predators and prey, and elicit behaviours that adjust distances accordingly. For snakes, strikes can serve both purposes. Vipers are thought to have the fastest strikes among snakes. However, strike performance has been measured in very few species, especially non-vipers. We measured defensive strike performance in harmless Texas ratsnakes and two species of vipers, western cottonmouths and western diamond-backed rattlesnakes, using high-speed video recordings. We show that ratsnake strike performance matches or exceeds that of vipers. In contrast with the literature over the past century, vipers do not represent the pinnacle of strike performance in snakes. Both harmless and venomous snakes can strike with very high accelerations that have two key consequences: the accelerations exceed values that can cause loss of consciousness in other animals, such as the accelerations experienced by jet pilots during extreme manoeuvres, and they make the strikes faster than the sensory and motor responses of mammalian prey and predators. Both harmless and venomous snakes can strike faster than the blink of an eye and often reach a target before it can move.

The big squeeze: scaling of constriction pressure in two of the world's largest snakes, Python reticulatus and Python molurus bivittatus.

Snakes are important predators that have radiated throughout many ecosystems, and constriction was important in their radiation. Constrictors immobilize and kill prey by using body loops to exert pressure on their prey. Despite its importance, little is known about constriction performance or its full effects on prey. We studied the scaling of constriction performance in two species of giant pythons (Python reticulatus and Python molurus bivittatus) and propose a new mechanism of prey death by constriction. In both species, peak constriction pressure increased significantly with snake diameter. These and other constrictors can exert pressures dramatically higher than their prey's blood pressure, suggesting that constriction can stop circulatory function and perhaps kill prey rapidly by over-pressurizing the brain and disrupting neural function. We propose the latter 'red-out effect' as another possible mechanism of prey death from constriction. These effects may be important to recognize and treat properly in rare cases when constrictors injure humans.

Gape size, its morphological basis, and the validity of gape indices in western diamond-backed rattlesnakes (Crotalus atrox).

Maximum gape is important to the ecology and evolution of many vertebrates, particularly gape-limited predators, because it can restrict the sizes and shapes of prey that can be eaten. Although many cranial elements probably contribute to gape, it is typically estimated from jaw length or jaw width, or occasionally from a combination of these two measures. We measured maximum gape directly for 18 individuals of the western diamond-backed rattlesnake, Crotalus atrox. We measured each individual's body length, several external cranial dimensions, several cranial osteological dimensions from cleaned skeletons, and we calculated gape index values from two published gape indices (GI). Cranial bone lengths and gape circumference showed negative allometry with snout-vent length (SVL), indicating that small individuals have relatively larger heads and gapes than their larger conspecifics. We then used Akaike's Information Criterion to determine which external and osteological measurements were the best predictors of gape. Body size (SVL) was the best predictor of maximum gape overall; however, when SVL was excluded from the analysis, quadrate (QL) and mandible lengths (MdLs) were the best predictors of maximum gape using both external and osteological measurements. Quadrate length probably contributes directly to gape; however, the importance of MdL to gape is less clear and may be due largely to its allometric relationships with head length and SVL. The two published GI did not prove to be better indicators of actual gape than the jaw and QLs in this study, and the gape values they produced differed significantly from our empirically determined gapes. For these reasons, we urge caution with the use and interpretation of computed GI in future studies. The extensive variation in quadrate and mandible morphology among lineages suggest that these bones are more important to variation in gape among species and lineages than within a single species.

The effects of atrazine on spotted salamander embryos and their symbiotic alga.

Worldwide amphibian declines have been a concern for biologists for the past several decades. The causes of such declines may include habitat loss, invasive species, pathogens, and man-made chemicals. Agricultural herbicides, in particular, are known to interfere with reproduction in amphibians and are likely contributing to population declines. We tested the effects of the herbicide atrazine on developing spotted salamanders (Ambystoma maculatum) and their symbiotic green alga Oophila amblystomatis. We exposed spotted salamander egg masses to atrazine at concentrations of 0 microg/L (control), 50, 100, 200, and 400 microg/L. Algae were eliminated in all atrazine treatments. Hatching success was significantly lower for atrazine-treated egg masses than for the controls, and was inversely related to atrazine concentration. The highest developmental stage reached by the embryos was significantly lower in the atrazine treatments than in the controls, and was inversely related to atrazine concentration. These results indicate that atrazine exposure affected spotted salamanders both directly by causing pathologies and mortality in embryos and indirectly by eliminating their symbiotic alga.

Tail morphology in the Western Diamond-backed rattlesnake, Crotalus atrox.

The shaker muscles in the tails of rattlesnakes are used to shake the rattle at very high frequencies. These muscles are physiologically specialized for sustaining high-frequency contractions. The tail skeleton is modified to support the enlarged shaker muscles, and the muscles have major anatomical modifications when compared with the trunk muscles and with the tail muscles of colubrid snakes. The shaker muscles have been known for many years to consist of three large groups of muscles on each side of the tail. However, the identities of these muscles and their serial homologies with the trunk muscles were not previously known. In this study, we used dissection and magnetic resonance imaging of the tail in the Western Diamond-backed Rattlesnake, Crotalus atrox, to determine that the three largest muscles that shake the rattle are the M. longissimus dorsi, the M. iliocostalis, and the M. supracostalis lateralis. The architecture of these muscles differs from their serial homologs in the trunk. In addition, the rattlesnake tail also contains three small muscles. The M. semispinalis-spinalis occurs in the tail, where it is a thin, nonvibratory, postural muscle that extends laterally along the neural spines. An additional muscle, which derives from fusion of the M. interarticularis inferior and M. levator costae, shares segmental insertions with the M. longissimus dorsi and M. iliocostalis. Several small, deep ventral muscles probably represent the Mm. costovertebrocostalis, intercostalis series, and transversohypapophyseus. The architectural rearrangements in the tail skeleton and shaker muscles, compared with the trunk muscles, probably relate to their roles in stabilizing the muscular part of the tail and to shaking the rattle at the tip of the tail. Based on comparisons with the tail muscles of a colubrid snake described in the literature, the derived tail muscle anatomy in rattlesnakes evolved either in the pitvipers or within the rattlesnakes. J. Morphol., 2008. (c) 2008 Wiley-Liss, Inc.

Are ontogenetic shifts in diet linked to shifts in feeding mechanics? Scaling of the feeding apparatus in the banded watersnake Nerodia fasciata.

The effects of size on animal behaviour, ecology, and physiology are widespread. Theoretical models have been developed to predict how animal form, function, and performance should change with increasing size. Yet, numerous animals undergo dramatic shifts in ecology (e.g. habitat use, diet) that may directly influence the functioning and presumably the scaling of the musculoskeletal system. For example, previous studies have shown that banded watersnakes (Nerodia fasciata) switch from fish prey as juveniles to frog prey as adults, and that fish and frogs represent functionally distinct prey types to watersnakes. We therefore tested whether this ontogenetic shift in diet was coupled to changes in the scaling patterns of the cranial musculoskeletal system in an ontogenetic size series (70-600 mm snout-vent length) of banded watersnakes. We found that all cranial bones and gape size exhibited significant negative allometry, whereas the muscle physiological cross-sectional area (pCSAs) scaled either isometrically or with positive allometry against snout-vent length. By contrast, we found that gape size, most cranial bones, and muscle pCSAs exhibited highly significant positive allometry against head length. Furthermore, the mechanical advantage of the jaw-closing lever system remained constant over ontogeny. Overall, these cranial allometries should enable watersnakes to meet the functional requirements of switching from fusiform fish to bulky frog prey. However, recent studies have reported highly similar allometries in a wide diversity of vertebrate taxa, suggesting that positive allometry within the cranial musculoskeletal system may actually be a general characteristic of vertebrates.

The ontogeny of contractile performance and metabolic capacity in a high-frequency muscle.

High-performance muscles such as the shaker muscles in the tails of western diamond-backed rattlesnakes (Crotalus atrox) are excellent systems for studying the relationship between contractile performance and metabolic capacity. We observed that shaker muscle contraction frequency increases dramatically with growth in small individuals but then declines gradually in large individuals. We tested whether metabolic capacity changed with performance, using shaker muscle contraction frequency as an indicator of performance and maximal activities of citrate synthase and lactate dehydrogenase as indicators of aerobic and anaerobic capacities, respectively. Contraction frequency increased 20-fold in 20-100-g individuals but then declined by approximately 30% in individuals approaching 1,000 g. Mass-independent aerobic capacity was positively correlated with contractile performance, whereas mass-independent anaerobic capacity was slightly but negatively correlated with performance; body mass was not correlated with performance. Rattle mass increased faster than the ability to generate force. Early in ontogeny, shaker muscle performance appears to be limited by aerobic capacity, but later performance becomes limited equally by aerobic capacity and the mechanical constraint of moving a larger mass without proportionally thicker muscles. This high-performance muscle appears to shift during ontogeny from a metabolic constraint to combined metabolic and mechanical constraints.

From physiology to fitness: the costs of a defensive adaptation in rattlesnakes.

The costs of using and maintaining presumed adaptations are unknown for most animals. Energetically expensive traits, such as some agonistic and antipredator behaviors in animals, may incur trade-offs with other aspects of an animal's life history, such as feeding and reproduction. However, infrequent and brief use may reduce the costs of vigorous behaviors. The shaker muscles in the tails of rattlesnakes are an excellent system for studying the potential costs of a specialized defensive system. The high energetic cost of rattling may increase feeding requirements or use energy that could otherwise be available for reproduction. I used energetic modeling to test whether the cost of rattling in western diamond-backed rattlesnakes (Crotalus atrox) can be high enough to increase feeding demands or reduce fecundity and fitness. Only very frequent and prolonged rattling would increase feeding needs and perhaps reduce fecundity to some degree. Typically, rattling probably incurs very low costs to feeding, reproduction, and hence fitness. These and other results suggest that many seemingly expensive adaptations may have minimal costs to energy budgets, reproduction, and fitness.

Minimal shortening in a high-frequency muscle.

Reducing the cost of high-frequency muscle contractions can be accomplished by minimizing cross-bridge cycling or by recycling elastic strain energy. Energy saving by contractile minimization has very different implications for muscle strain and activation patterns than by elastic recoil. Minimal cross-bridge cycling will be reflected in minimal contractile strains and highly reduced force, work and power output, whereas elastic energy storage requires a period of active lengthening that increases mechanical output. In this study, we used sonomicrometry and electromyography to test the relative contributions of energy reduction and energy recycling strategies in the tailshaker muscles of western diamondback rattlesnakes (Crotalus atrox). We found that tailshaker muscle contractions produce a mean strain of 3%, which is among the lowest strains ever recorded in vertebrate muscle during movement. The relative shortening velocities (V/V(max)) of 0.2-0.3 were in the optimal range for maximum power generation, indicating that the low power output reported previously for tailshaker muscle is due mainly to contractile minimization rather than to suboptimal V/V(max). In addition, the brief contractions (8-18 ms) had only limited periods of active lengthening (0.2-0.5 ms and 0.002-0.035%), indicating little potential for elastic energy storage and recoil. These features indicate that high-frequency muscles primarily reduce metabolic energy input rather than recycle mechanical energy output.

Mechanical trade-offs explain how performance increases without increasing cost in rattlesnake tailshaker muscle.

Rattling by rattlesnakes is one of the fastest vertebrate movements and involves some of the highest contraction frequencies sustained by vertebrate muscle. Rattling requires higher accelerations at higher twitch frequencies, yet a previous study showed that the cost per twitch of rattling is independent of twitch frequency. We used force and video recordings over a range of temperatures to examine how western diamondback rattlesnakes (Crotalus atrox) achieve faster movements without increases in metabolic cost. The key findings are (i) that increasing muscle twitch tension trades off with decreasing twitch duration to keep the tension-time integral per twitch nearly constant over a wide range of temperatures and twitch frequencies and (ii) that decreasing lateral displacement of the rattle joint moderates the mechanical work and power required to shake the rattle at higher frequencies. These mechanical trade-offs between twitch tension and duration and between joint force and displacement explain how force, work and power increase without an increase in metabolic cost.