The rattle is one of the key elements in the complex defensive system of rattlesnakes. The rattle is used to generate sound that deters potentially dangerous animals. Rattling sounds are affected by rattle motion, which in turn is affected by rattle length. However, the ways that rattle length and motion affect the efficiency of sound production (i.e., sound output per unit energy input) are poorly known. We tested whether there is a rattle length that optimizes sound production by studying how rattle length affects motion, mechanical work (an indicator of energy input), and sound loudness (an indicator of energy output) in western diamond-backed rattlesnakes (Crotalus atrox). Specifically, we removed rattle segments one at a time, video taped rattling at each rattle length, and then determined rattle oscillation frequency, displacement, and mechanical work. Rattle motion involved lateral oscillation and longitudinal twisting. Lateral displacements changed with rattle length. Short rattles of 1-4 segments oscillated in a traveling-wave (undulatory) pattern that had relatively large displacements whereas long rattles of 6-16 segments oscillated in a standing-wave pattern with one or two nodes and smaller displacements. Rattle kinetic energy and work increased steadily with rattle length, mainly because torsional displacements increased even though lateral displacements decreased. Rattling sound loudness increased steadily from zero to eight free segments, peaked from 6-12 segments, and became slightly quieter at longer lengths. These results indicate that rattle lengths of 6-8 segments maximize sound output per unit energy cost.
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 SVL) of banded watersnakes. We found that all cranial bones and gape size exhibited significant negative allometry, whereas the muscle pCSAs scaled either isometrically or with positive allometry against SVL. By contrast, we found that gape size, most cranial bones, and muscle pCSAs exhibited highly significant positive allometry against head length. Further, 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.
Constriction was probably one of the key innovations that enabled snakes to subdue relatively large prey animals. It involves a snake winding or wrapping its body around a prey animal and squeezing, which restrains the prey from escaping and defending itself, and typically kills it quickly. Published observations and experiments on constriction have indicated that it is strong enough to kill prey by suffocation, circulatory arrest, or spinal fracture. However, constriction strength has been measured in very few species of snakes, and thus far only in relatively small individuals. In this study, we measured constriction pressure of 5-175 kPa in 12 species and 30 individuals, which varied in diameter from 0.85-12.5 cm. Constriction pressure varied significantly with snake diameter and number of loops in the coil. The measured pressures are high enough to kill many kinds of prey animals by circulatory arrest or spinal fracture, both of which are faster than killing prey by suffocation alone, and therefore are probably safer for the constrictor.
The costs of using and maintaining presumed adaptations are unknown for most animals. Highly specialized traits such as some agonistic behaviors in animals are often energetically expensive, and may incur trade-offs with other aspects of an animal’s life history, such as feeding and reproduction. However, irregular and infrequent 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 low costs to feeding, reproduction, and fitness. These and other results suggest that many seemingly-expensive adaptations may have minimal costs to energy budgets, reproduction, and fitness. Back to publication list
Moon, Brad R. and Alexa Tullis. 2006. The Ontogeny of Contractile Performance and Metabolic Capacity in a High-Frequency Muscle. Physiological and Biochemical Zoology 79:20-30.
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-g to 100-g individuals, but then declined by approximately 30% in individuals approaching 1000 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. Back to publication list
Vincent, Shawn E., Brad R. Moon, Richard Shine, and Anthony Herrel. 2006. The functional meaning of “prey size” in water snakes (Nerodia fasciata, Colubridae). Oecologia 147:204-211.
The evolutionary success of macrostomatan (enlarged-gape) snakes has been attributed to their ability to consume large prey, in turn made possible by their highly kinetic skulls. However, prey can be ‘‘large’’ in several ways, and we have little insight into which aspects of prey size and shape affect skull function during feeding. We used X-ray videos of broad-banded water snakes (Nerodia fasciata) feeding on both frogs and fish to quantify movements of the jaw elements during prey transport, and of the anterior vertebral column during post-cranial swallowing. In a sample of additional individuals feeding on both frogs and fish, we measured the time and the number of jaw protractions needed to transport prey through the buccal cavity. Prey type (fish vs. frog) did not influence transport kinematics, but did influence transport performance. Furthermore, wider and taller prey induced greater movements of most cranial elements, but wider prey were transported with significantly less anterior vertebral bending. In the performance trials, heavier, shorter, and wider prey took significantly more time and a greater number of jaw protractions to ingest. Thus, the functional challenges involved in prey transport depend not only upon prey mass, but also prey type (fish vs. frog) and prey shape (relative height, width and length), suggesting that from the perspective of a gape-limited predator, the difficulty of prey ingestion depends upon multiple aspects of prey size.
Moon, Brad R., Michael R. Urquhart, Stan L. Lindstedt, and Kevin E. Conley. 2003. Minimal shortening in a high frequency muscle. Journal of Experimental Biology 206(8): 1291-1297.
Reducing the cost of high-frequency muscle contractions can be accomplished by minimizing cross-bridge cycling or by recycling elastic strain energy. Energy savings by contractile minimization has very different implications for muscle strain and activation patterns than does 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 strain ever recorded in vertebrate muscle during movement. The relative shortening velocities (V/Vmax) of 0.2 to 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/Vmax. 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. Back to publication list
Moon, Brad R., Travis J. LaDuc, Robert Dudley, and Andrew Chang. 2002. A twist to the rattlesnake tail. In Topics in Functional and Ecological Vertebrate Morphology (eds. Aerts, P., D'Août, K., Herrel, A., and Van Damme, R.), pp. 63-76. Maastricht: Shaker Publishing B.V. ISBN 90-423-0204-6.
Rattling is an important defensive behaviour in rattlesnakes. It is also one of the fastest sustainable vertebrate movements and consequently has a high energetic cost. Rattle motion therefore is an important link between rattlesnake physiology and behavioural ecology. We studied rattle motion using high-speed video recordings of rattling in western diamondback rattlesnakes (Crotalus atrox). Rattling frequencies ranged from 23 to 100 Hz over temperatures of 10° to 35° C. Rattle motion is sinusoidal with two major components, lateral undulation and longitudinal torsion: The rattle twists as it swings from side to side. These two motions interact in long rattles to produce more complex movements, such as a standing wave oscillation on the dorsal edge simultaneously with travelling waves along the ventral edge of the rattle. Lateral displacements decrease with increasing temperature and rattling frequency, whereas torsional displacements do not change substantially. Rattle linear and angular velocities are moderately high and rattle accelerations are extremely high. Rattle movements and their changes with temperature underlie the energetic and acoustic results reported in other studies, and point to biomechanical features that may have been associated with rattle evolution.
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Moon, Brad R., J. Johanna Hopp and Kevin E. Conley. 2002. Mechanical trade-offs explain how performance increases without increasing cost in rattlesnake tailshaker muscle. Journal of Experimental Biology 205(5): 667-675.
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 (1) 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 (2) 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.
See also: Cover pictures and Phillips, K. 2002. Furious and Fast. Journal of Experimental Biology 205(5): 502. Go there from here.
Moon, Brad R. 2000. The mechanics of swallowing and the muscular control of diverse behaviours in gopher snakes. Journal of Experimental Biology 203(17): 2589-2601.
Snakes are excellent subjects for studying functional versatility and potential constraints because their movements are constrained to vertebral bending and twisting. In many snakes, swallowing is a kind of inside-out locomotion. During swallowing, vertebral bends push food from the jaws along a substantial length of the body to the stomach. In gopher snakes (Pituophis melanoleucus) and king snakes (Lampropeltis getula), swallowing often begins with lateral bending of the head and neck as the jaws advance unilaterally over the prey. Axial movement then shifts to accordion-like, concertina bending as the prey enters the oesophagus. Once the prey is completely engulfed, concertina bending shifts to undulatory bending that pushes the prey to the stomach. The shift from concertina to undulatory bending reflects a shift from pulling the prey into the throat (or advancing the mouth over the prey) to pushing it along the oesophagus towards the stomach. Undulatory kinematics and muscular activity patterns are similar in swallowing and undulatory locomotion. However, the distinct mechanical demands of internal versus external force exertion result in different duty factors of muscle activity. Feeding and locomotor movements are thus integral functions of the snake axial system. Back to publication list
Moon, Brad R. 2000. The mechanics and muscular control of constriction in gopher snakes (Pituophis melanoleucus) and a king snake (Lampropeltis getula). Journal of Zoology, London 252(1): 83-98.
Constriction of prey by gopher snakes Pituophis melanoleucus and king snakes Lampropeltis getula is highly variable in posture, muscular activity and force exertion. These snakes typically use lateral bends of the anterior trunk to wind the body into a vertical coil around the prey. Three common constriction postures are fully encircling loops that form a coil, partially encircling loops, and non-encircling loops that pinion the prey. Initial tightening of a coil occurs by winding or pressing the loops tighter to reduce the diameter of the coil. The epaxial muscles are highly active during striking and coil formation and intermittently active during sustained constriction. These results refute the hypothesis of a mechanical constraint on constriction in snakes with elongate epaxial muscles. Constricting gopher and king snakes can detect muscular, ventilatory and circulatory movements in rodent prey. In response to simulated heartbeats or ventilation in mice, the snakes twitch visibly, recruit epaxial muscle activity, and increase constriction pressure temporarily, but then quickly relax. Muscular activity and constriction pressure are increased most and sustained longest in response to muscular struggling in prey. Although muscle activity and pressure exertion are intermittent, the constriction posture is maintained until the prey has been completely still for several seconds; thus, a snake can reapply pressure in response to any circulatory, ventilatory or muscular movement by the prey. The pressures of 6.1-30.9 kPa (46-232 mm Hg) exerted on small mammal prey by constricting snakes range from about half to over twice a mouse's systolic blood pressure, and are probably 10 times larger than the venous pressure. These high pressures probably kill mammalian prey by inducing immediate circulatory and cardiac arrest, rather than by suffocation alone.
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Moon, Brad R. 1999. Testing an inference of function from structure: Snake vertebrae do the twist. Journal of Morphology 241(3): 217-225.
The zygapophyses and zygosphene-zygantrum articulations of snake vertebrae are hypothesized to restrict or eliminate vertebral torsion. This hypothesis is apparently based solely on the inference of function from structure, despite the limitations of such inferences, as well as contradictory observations and measurements. In this study, I observed and measured axial torsion in gopher snakes, Pituophis melanoleucus. To examine the structural basis of axial torsion, I measured the vertebral articulation angles along the body and the insertion angles of five epaxial muscles. To examine torsion in a natural behavior, I digitized video images and measured the degree of apparent axial torsion during terrestrial lateral undulation. Finally, I measured the mechanical capacity of the vertebral joints for actual torsion over intervals of 10 vertebrae in fresh, skinned segments of the trunk. Vertebral articulation angles vary up to 30 degrees, and are associated with variation in torsional capacity, along the trunk. The freely crawling P. melanoleucus twisted up to 2.19 degrees per vertebra, which produced substantial overall torsion when added over several vertebrae. The vertebral joints are mechanically capable of torsion up to 2.89 degrees per joint. Therefore, despite the mechanical restriction imposed by the complex articulations, vertebral torsion occurs in snakes and appears to be functionally important in several natural behaviors. Even in cases in which mechanical function appears to be narrowly constrained by morphology, specific functions should not be inferred solely from structural analyses.
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Moon, Brad R. and Carl Gans. 1998. Kinematics, muscular activity, and propulsion in gopher snakes. Journal of Experimental Biology 201(19): 2669-2684.
Previous studies have addressed the physical principles and muscular activity patterns underlying terrestrial lateral undulation in snakes, but not the mechanism by which muscular activity produces curvature and propulsion. In this study, we used synchronized electromyography and videography to examine the muscular basis and propulsive mechanism of terrestrial lateral undulation in gopher snakes Pituophis melanoleucus affinis. Specifically, we used patch electrodes to record from the semispinalis, longissimus dorsi and iliocostalis muscles in snakes pushing against one or more pegs. Axial bends propagate posteriorly along the body and contact the pegs at or immediately posterior to an inflection of curvature, which then reverses anterior to the peg. The vertebral column bends broadly around a peg, whereas the body wall bends sharply and asymmetrically around the anterior surface of the peg. The epaxial muscles are always active contralateral to the point of contact with a peg; they are activated slightly before or at the point of maximal convexity and deactivated variably between the inflection point and the point of maximal concavity. This pattern is consistent with muscular shortening and the production of axial bends, although variability in the pattern indicates that other muscles may affect the mechanics of the epaxial muscles. The kinematic and motor patterns in snakes crawling against experimentally increased drag indicated that forces are produced largely by muscles that are active in the axial bend around each peg, rather than by distant muscles from which the forces might be transmitted by connective tissues. At each point of force exertion, the propulsive mechanism of terrestrial lateral undulation may be modeled as a type of cam-follower, in which continuous bending of the trunk around the peg produces translation of the snake. Back to publication list
Moon, Brad R. and Teresa Candy. 1997. Muscular and coelomic cross-sectional areas in three families of snakes. Journal of Herpetology 31: 37-44.
The coelomic and muscular cross-sectional areas of snakes reflect a compromise between competing demands for muscular force exertion during locomotion and large coelomic volume for feeding or carrying developing offspring. In this paper, we examine the allometry of coelomic and muscular cross-sectional area in 32 species of colubrid, elapid, and viperid snakes. To do so, we digitized images of transverse sections of preserved specimens and then calculated the cross-sectional areas from these images. Coelomic and musculoskeletal cross-sectional areas were significantly correlated with body mass in colubrid and viperid snakes, but only musculoskeletal area was significantly correlated with mass in our small sample of elapids. The allometry of coelomic volume was nearly identical to that of coelomic area. There was significant variation in the allometric patterns among families. In colubrids, neither constriction nor habitat preference had a significant effect on musculoskeletal area. The functional implications of variation in relative coelomic and muscular cross-sectional areas may involve diverse aspects of behavior, ecology, and life history, and generally are amenable to experimental testing.
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Moon, Brad R. 1996. Sampling rates, aliasing, and the analysis of electrophysiological signals. Proceedings of the Fifteenth Southern Biomedical Engineering Conference, pp. 401-404.
Low analog to digital (A-D) sampling rates, including the Nyquist rate, are inadequate for direct display and analysis of many electrophysiological signals (i.e., without inverse Fourier reconstruction). Recent empirical studies have reported some results that do not follow from sampling theory, such as increasing spike frequency with increasing sampling rate, and thus require explanation. This study addresses the effects of A-D sampling rate on the frequency and amplitude of known artificial signals and of electromyograms.
A-D sampling rate need not always be a multiple of the upper band limit because electromyograms, and many other electrophysiological signals, do not always contain frequency components near the upper band limit. Rather, sampling rate must be matched to particular signal frequencies. Furthermore, A-D sampling rate has different effects on frequency and amplitude. Higher sampling rates are required for accurate amplitude reproduction than for accurate frequency reproduction. Very high sampling rates significantly bias quantitative results by detecting low-level noise in signals. This bias is exacerbated in taped signals sampled at reduced tape speeds.
Zug, George R. and Brad R. Moon. 1995. Systematics of the South Pacific slender-toed geckos, Nactus pelagicus complex: Oceania, Vanuatu, and Solomon Islands populations. Herpetologica 51: 77-90.
The current nominal species Nactus pelagicus represents a species complex that includes bisexual and unisexual populations. Four karyotypic morphs are known, but previous authors have noted that populations do not differ in gross external morphology. In this study, a comparison of samples from five bisexual and five unisexual populations confirms a high level of morphological uniformity (mensural and meristic) within and between samples. Morphological differences are slight but, in some cases, significantly different. Although the differences are slight, multivariate analyses (PCA, DFA) segregate some bisexual populations from unisexual ones and support specific recognition of the bisexual populations (N. multicarinatus--southern Solomon Islands and Vanuatu) and unisexual populations (N. pelagicus--southern Vanuatu, New Caledonia, and Oceania). Lectotypes are designated, and type-localities are restricted for both species; each species is redescribed.
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Updated September 2009