Muscular mechanisms of snake locomotion: an electromyographic study of lateral undulation of the Florida banded water snake (Nerodia fasciata) and the yellow rat snake (Elaphe obsoleta)

Electromyography and cinematography were used to determine the activity of epaxial muscles of colubrid snakes during terrestrial and aquatic lateral undulatory locomotion. In both types of lateral undulation, at a given longitudinal position, segments of three muscles (Mm. semispinalis-spinalis, longissimus dorsi, and iliocostalis) usually show synchronous activity. Muscle activity propagates posteriorly and generally is unilateral. With each muscle, large numbers of adjacent segments (30 to 100) show simultaneous activity. Terrestrial and aquatic undulation differ in two major respects. (1) During terrestrial undulation, muscle activity in a particular region begins when that portion of the body has reached maximal convex flexion and ends when it is maximally concave; this phase relation is uniform along the entire snake. During swimming, however, muscle activity passes posteriorly faster than the wave of vertebral flexion, causing the relation of muscle activity to flexion to change along the length of the snake. (2) In the terrestrial mode, the block of active muscle segments remains approximately constant in size as it passes down the snake, whereas during swimming the number of adjacent active muscle segments increases posteriorly. Despite the fact that Elaphe obsoleta has nearly twice as many body vertebrate as Nerodia fasciata (240 vs. 125), the only difference observed in the swimming of these two species is that a larger number of adjacent muscle segments is simultaneously active in comparable regions of Elaphe obsoleta than in Nerodia fasciata.     

Histological aspects of natural eustrongyloid infections of the northern water snake, Nerodia sipedon

Encapsulated as well as unencapsulated fourth stage larvae of Eustrongylides sp. were found in four northern water snakes, Nerodia sipedon, from Virginia. Unencapsulated nematodes occurred within muscle, subcutaneous tissue and in the coelom. Encapsulated nematodes occurred in three forms: recently encapsulated, degenerating, or sclerotic; they were found on the mesentery, in muscle and subcutaneous tissue. Encapsulation was associated with muscular hypotrophy, fibroplasia and eosinophilia.     

Dynamic changes in body form during swimming in the water snake Nerodia sipedon

Video records of swimming water snakes show that during moderate to rapid swimming, the rear half to two-thirds of the trunk is compressed laterally, approaching the body form of some sea snakes. Body form of swimming snakes differed significantly from their shape when resting on a flat surface or when anesthetized and suspended in water. The extent of lateral flattening is positively correlated with swimming speed, a relationship generally supported by tests of trunk models in a flow tank. In Nerodia, the ability to temporarily flatten the trunk depends on kinetic costovertebral joints, a large compressible body cavity, and the absence of ventral skeletal support - features found in most snakes. Histological studies and manipulations of partially dissected preserved specimens showed that the resting angle of the ribs is maintained by localized elastic hypertrophy of the costovertebral capsular ligament. Trunk form during swimming in Nerodia is proposed to arise from anteromedial movement of the distal rib powered by deep muscles acting in concert with those proposed to generate undulation of the vertebral column.     

Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci

We describe the isolation and genetic characterization of eight microsatellite DNA loci from the northern water snake, Nerodia sipedon sipedon and use these loci to analyse levels of genetic differentiation between local (< 2 km apart) populations of these snakes in Ontario. These loci are variable, with expected heterozygosities ranging from 0.28 to 0.91, and can correctly exclude nonsires in parentage analyses with a high probability (0.998). Population analyses reveal significant deviation from expected heterozygosity levels for one population, probably a result of a null allele(s) at a single locus and small but significant levels of genetic differentiation among all three populations. This demonstrates that microgeographic genetic structure exists in this species, possibly due to limited dispersal.     

Dietary regulation of digestive enzyme levels in the water snake, Natrix tessellata

Levels of digestive enzymes were analyzed in water snakes following artificial feeding. A prominent increase of total proteolytic activity in the stomach was evident after feeding with a casein solution or after the snake was offered a fish (9- and 6-fold that of the fasting level, respectively). The activity following feeding with starch was much lower. Increased levels of chymotrypsin(ogen) as well as of amylase were evident in the pancreas 1 day after feeding the snake with fish. A specific induction of increased level of chymotrypsin in the pancreas of adult snakes was achieved by feeding with casein (12-fold that of the fasting level). In the group fed with starch, the chymotrypsin level dropped, while a 3-fold increase of amylase was evident. In newborn snakes, fed for the first time, casein induced a dramatic increase in the level of chymotrypsin in the pancreas (58 times the fasting level); feeding with starch induced an approximate 2-fold increase of chymotrypsin. Histological examination of the pancreas 1 day following casein feeding showed acinar cells loaded with zymogen granules. In starved animals and in snakes fed with starch, a much lower concentration of zymogen granules was observed. The pancreas of the snake may, thus, be most suitable for studying the specific induction of synthesis of digestive enzymes.     

Visual acuity of the midland banded water snake estimated from evoked telencephalic potentials

The visual acuity of seven midland banded water snakes was measured by recording evoked responses from telencephalon to temporally modulated square wave grating patterns. Using conventional electrophysiological techniques and signal averaging, high contrast square wave gratings of different spatial frequencies were presented. Acuity was estimated by extrapolating relative response amplitude/log₁₀ spatial frequency functions which yielded an average acuity of 4.25 cycles/degree. Refractive state was also estimated by recording evoked potentials to intermediate spatial frequencies with different lenses in front of the eye. Polynomial fits indicated that under the experimental conditions the snakes were around 6.4 diopters hyperopic suggesting a corrected acuity of 4.89 cycles/degree. Reduction of grating luminance resulted in a reduction in evoked potential acuity measurements. These results indicate that the spatial resolution of midland banded water snakes is the equal of cat; about 20/120 in human clinical terms.     

Low genetic diversity and evidence of population structure among subspecies of Nerodia harteri, a threatened water snake endemic to Texas

Nerodia harteri is a threatened small-bodied water snake that occupies one of the most restricted ranges of any snake within the continental United States. It is found closely associated with rivers and tributaries in the Colorado and Brazos river basins, which flow through north-central Texas. Nerodia harteri has been at the center of debate owing to conflicts between conservation efforts and the construction of dams that change or destroy its preferred habitat. Additionally, its taxonomic status has also been under contention with some authors recognizing two subspecies, the Brazos water snake (N. h. harteri) and the Concho water snake (N. h. paucimaculata), whereas other authors consider each separate species. Despite its relatively recent discovery during the 1940s, N. harteri has been the subject of several ecological studies, yet no population genetic assessment of either subspecies has been performed to date. We first evaluated the phylogenetic placement of both subspecies among other North American Nerodia using partial sequence data from the mitochondrial gene cytochrome-b. We then tested for population subdivision among four rivers encompassing the range of N. harteri and tested for the presence of admixture between river basins using mitochondrial sequence data (920?bp of cyt-b) and five cross-species amplified microsatellite loci. We found low mitochondrial haplotype diversity represented by two unique haplotypes in each river basin, which were separated by no more than four nucleotide changes. Nuclear loci showed low genetic diversity and population structuring within and among river basins. We did not find conclusive evidence of admixture between basins, and we support the presence of two separate evolutionarily significant units and two separate management units corresponding to each major river basin. Given increasing natural and anthropogenic threats, we recommend continued ecological and genetic monitoring of both subspecies.     

Post-testicular change in the reptile sperm surface with particular reference to the snake, Natrix fasciata

Sperm surface changes occurring in the reptile Wolffian duct have been explored with particular references to the snake, Natrix fasciata. In the snake Wolffian duct there are several proteins not present in serum, the pattern of which changes in concert with the seasonal testicular cycle. Whereas testicular spermatozoa did not bind antibody to duct secretions, all Wolffian duct spermatozoa did so over both head and tail, according to immunofluorescence patterns. Thus, on entering the Wolffian duct, the entire surface of N. fasciata spermatozoa acquires one of more of the duct's secretory components. As indicated by immunofluorescence, immunoelectrophoresis, and immunodiffusion, epitopes on at least some molecules that bind to spermatozoa or that remain free in the duct fluid are shared with those in other Natrix species, but not in more distant reptiles (turtle, anole lizard), nor chicken, rat, or rabbit. In regard to glycoproteins, one prominent con A-reactive band was present in polyacrylamide gel electrophoresis (PAGE) of snake fluid and more were evident in fluid collected from the turtle duct. However, such lectin-reactive elements did not bind to spermatozoa as judged by an absence of any change in snake, turtle and lizard sperm lectin-binding patterns in passing from the testis into and through the Wolffian duct. In all, evidence from these and other species studied begins to suggest that the nature of the post-testicular sperm surface modification displayed in most vertebrates that fertilize internally may differ in sub-therian and therian groups, respectively. There appears to be a relative emphasis on glycosyl-rich surface elements in the latter. The possible significance of these changes for sperm function in the different groups is discussed briefly in terms of sperm survival/storage, as well as capacitation and sperm binding to the zona.     

Lack of postprandial thermophily in diamondback water snakes,Nerodia rhombifera

We compared the preferred body temperature (T_b) of fasted and satiated diamondback water snakes (Nerodia rhombifera) in linear thigmothermal gradients. We found no significant postprandial thermophily. Thermoregulatory precision varied among 6 days of testing and was most precise during the first day (24–48 hr after feeding).     

Good species despite massive hybridization: genetic research on the contact zone between the watersnakes Nerodia sipedon and N. fasciata in the Carolinas, USA

Genomic markers generated with the amplified fragment length polymorphism method revealed extensive, panmictic-like hybridization along the narrow contact zone between the water snakes Nerodia sipedon and Nerodia fasciata in the Carolinas, USA. However, asymmetric distributions of diagnostic markers between both species and low frequencies of backcrossed hybrids with a high value of interspecific mixture infer selection against certain genotypes. This is consistent with a pronounced genetic and morphological preponderance of N. fasciata characters in the hybrid zone. Despite massive hybridization within the contact zone, the existence of nearly fixed genetic markers and the potential inferiority of certain hybrid genotypes support the species status of the two taxa and corroborate known, but nondiagnostic differences in morphology and ecology. This study stretches the applicability of species concepts to cases, where the genetic compatibility between two closely related species is very high, yet, they still evolve and persist as independent entities.     

Sexual abstinence and the cost of reproduction in adult male water snakes, Nerodia sipedon

Low frequency of reproduction among iteroparous organisms is most often observed among female ectothermic vertebrates and is thought to be a strategy used to defer reproductive costs. We assessed reproductive costs of male water snakes ( Nerodia sipedon ) to determine why half of adult males abstain from reproduction each year. There was no evidence of a short-term energetic cost of reproduction. Change in mass did not differ between reproductive and non-reproductive males during the one-month mating season or during the entire four-month activity season. Changes in mass of reproductive males were similar at two sites in which the spatial distribution of females differed. However, there were size-specific differences in growth and survival between reproductive and non-reproductive males. Among reproductive males growth rate decreased with body size at a lower rate than among non-reproductive males. Survival increased with body size for reproductive males, but decreased with body size among non-reproductive males. Most of the differential survival between reproductive and non-reproductive males did not occur during the mating season but rather during hibernation. Size-related differences between reproductive and non-reproductive males may reflect selection having eliminated low quality males from the larger size classes. Overall our results appear most consistent with there being high variance in male quality, such that the best males can bear the cost of reproducing and still grow and survive as well or better than low quality males that abstain from reproduction.     

Larval Gnathostoma hispidum detected in the red banded odd-tooth snake, Dinodon rufozonatum rufozonatum, from China

A total of 205 larval gnathostomes were collected from 18 (22.5%) of 80 red banded odd-tooth snakes, Dinodon rufozonatum rufozonatum, which had been smuggled from China and confiscated at Customs in Busan, Republic of Korea. In order to identify the species, some of the larvae were observed by a light microscope and a scanning electron microscope (SEM). The larvae were 2.18 x 0.29 mm in average size, and had a pair of lips at the anterior end, a muscular esophagus, 2 pairs of cervical sacs, and brownish intestines. The head bulb was characteristically equipped with 4 rows of hooklets; the average number of hooklets in each respective row was 38.6, 40.5, 41.5, and 43.7. In SEM views, the mouth evidenced a pair of lateral lips of equal size in a half-moon shape. Each lip featured a couple of labial papillae and a small amphid located between the 2 papillae. The hooklets on the head bulb had single-pointed, posteriorly-curved tips. The cuticular spines were larger and more densely distributed on the anterior part of the body, and decreased gradually in size and number toward the posterior body. On the basis of these morphological characteristics, the larvae were identified as the third stage larvae of Gnathostoma hispidum.     

Specific dynamic action and postprandial thermophily in juvenile northern water snakes,Nerodia sipedon

1. We measured oxygen consumption of seven juvenile Northern water snakes, Nerodia sipedon, at 3, 19, 41, and 89 h after feeding. 2. Oxygen consumption 19 h after eating was significantly higher than at 3, 41, and 89 h after feeding and the values at 3 h post-feeding were significantly higher than those at 41 and 89 h. 3. We monitored substrate temperature preference in nine juvenile N. sipedon at 2000, 0000, 0800, 1200, and 1600 h for 3 days. 4. After feeding and at night snakes selected warmer substrate temperatures.     

Immune response in the water snake,Natrix erythrogaster transversa

One month after an intramuscular injection of bovine albumin, the plasma of a water snake (Natrix erythrogaster transversa) contained a macroglobulin which bound radiolabeled bovine serum albumin.     

Microsatellite variation, population structure, and bottlenecks in the threatened copperbelly water snake

Habitat loss and isolation is pervasive in the Midwest U.S. Wetlands are experiencing particularly dramatic declines, yet there is a paucity of information on the genetic impacts of these losses to obligate wetland vertebrates. We quantified the genetic variation of extant populations of a shallow wetland specialist and evaluated potential reductions in population size (i.e. bottlenecks) using seven polymorphic microsatellite DNA markers. We analyzed 228 copperbelly water snakes (Nerodia erythrogaster neglecta), representing populations from three states. Moderate genetic differentiation exists among all three regions (F _ST = 0.12, P < 0.001), with evidence for low levels of differentiation within the federally protected Ohio region (F _ST = 0.025, P = 0.007), and moderate to strong differentiation within the Indiana region (F _ST = 0.23, P < 0.001). Furthermore, Bayesian clustering (i.e. STRUCTURE) supports the separation of the Indiana sites, both from each other and from all other sampling sites. However, it does not support the separation of the Ohio sites from the Kentucky sites. Differentiation among sampling sites did not appear to be related to geographic distance, but rather depended on the quality of terrestrial corridors used for dispersal. Mode shifts in allele frequencies and excess heterozygosity tests were negative, while M-ratio tests were nearly all positive, indicating the likelihood of historical rather than contemporary population bottlenecks. However, potential subspecific intergradation in the Kentucky region may have artificially lowered the M-ratio, and we suggest caution when using the M-ratio approach if intergradation is suspected. Our results have conservation implications for wetland management and management of the copperbelly populations, and emphasizes the importance of protecting wetland complexes.     

Effects of seasonal variation in prey abundance on field metabolism, water flux, and activity of a tropical ambush foraging snake

The responses of animals to seasonal food shortages can have important consequences for population dynamics and the structure and function of food webs. We investigated how an ambush foraging snake, the northern death adder Acanthophis praelongus, responds to seasonal fluctuations in prey availability in its tropical environment. In the dry season, field metabolic rates and water flux, as measured by doubly labeled water, were significantly lower than in the wet season. Unlike some other reptiles of the wet-dry tropics, death adders showed no seasonal difference in their resting metabolism. About 94% of the decrease in energy expended in the dry season was due to a decrease in activity and digestion, with lower body temperatures accounting for the remainder. In the dry season, death adders were less active and moved shorter distances between foraging sites than in the wet season. Analysis of energy expenditure suggested that adders fed no more than every 2-3 wk in the dry season but fed more frequently during the wet season. Unlike many lizards that cease feeding during the dry season, death adders remain active and attempt to maximize their energy intake year-round.     

Ventilation and gas exchange in the diamondback water snake,Natrix rhombifera

Summary Simultaneous measurements of pulmonary and cutaneous oxygen and carbon dioxide exchange, pulmonary ventilation and heart rate were made on the diamondback water snake,Natrix rhombifera at 28°C using body plethysmography. Resting lung volume, maximum lung volume and tracheal volume were also measured.The following mean values were measured in undisturbed snakes breathing room air: total (pulmonary and cutaneous) O₂ uptake 46 mol · (kg min)^–1; total CO₂ output, 49 mol · (kg min)^–1; tidal volume, 12 ml (BTPS) · kg^–1; ventilatory rate, 6.9 min^–1; heart rate, 42 min^–1. From the measurements of tracheal volume, the effective (alveolar) ventilation was estimated as approximately 70% of total ventilation resulting in effective pulmonary and of 130 Torr and 20 Torr respectively. Cutaneous exchange accounted for 8.1% of the total and 12.4% of the total .Resting lung volume of anaesthetized snakes was 75 ml (BTPS) · kg^–1, maximum lung volume was 341 ml (BTPS) · kg^–1 and tracheal volume was 3.9 ml (BTPS) · kg^–1.