Ontogenetic shifts of heart position in snakes

Heart position relative to total body length (TL) varies among snakes, with anterior hearts in arboreal species and more centrally located hearts in aquatic or ground‐dwelling species. Anterior hearts decrease the cardiac work associated with cranial blood flow and minimize drops in cranial pressure and flow during head‐up climbing. Here, we investigate whether heart position shifts intraspecifically during ontogenetic increases in TL. Insular Florida cottonmouth snakes, Agkistrodon conanti , are entirely ground‐dwelling and have a mean heart position that is 33.32% TL from the head. In contrast, arboreal rat snakes, Pantherophis obsoleta , of similar lengths have a mean heart position that is 17.35% TL from the head. In both species, relative heart position shifts craniad during ontogeny, with negative slopes = −.035 and −.021% TL/cm TL in Agkistrodon and Pantherophis , respectively. Using a large morphometric data set available for Agkistrodon (N = 192 individuals, 23–140 cm TL), we demonstrate there is an anterior ontogenetic shift of the heart position within the trunk (= 4.56% trunk length from base of head to cloacal vent), independent of head and tail allometry which are both negative. However, in longer snakes > 100 cm, the heart position reverses and shifts caudally in longer Agkistrodon but continues toward the head in longer individuals of Pantherophis . Examination of data sets for two independent lineages of fully marine snakes (Acrochordus granulatus and Hydrophis platurus ), which do not naturally experience postural gravity stress, demonstrate both ontogenetic patterns for heart position that are seen in the terrestrial snakes. The anterior migration of the heart is greater in the terrestrial species, even if TL is standardized to that of the longer P. obsoleta , and compensates for about 5 mmHg gravitational pressure head if they are fully upright.     

Variation of organ position in snakes

The complex and successful evolutionary history of snakes produced variation in the position and structure of internal organs. Gravity strongly influences hemodynamics, and the impact on structure and function of the cardiovascular system, including pulmonary circulation, is well established. Therefore, we hypothesized that interspecific variation in the position of the heart and vascular (faveolar) lung should exceed that of other internal organs that are less sensitive to gravity. We examined the position of selected internal organs in 72 snakes representing 5 families and 13 species including fully aquatic and scansorial/arboreal species, representing the extremes of gravitational influence. Tests for differences of variance and coefficients of variation largely confirm that interspecific variation in position of the heart and vascular lung generally exceed those of other organs that we measured, particularly posterior organs. The variance of heart position generally exceeded that of more posterior organs, was similar to that of the anterior margin of the vascular lung, and was exceeded by that of the posterior margin of the vascular lung (variance ratio = 0.23). The gravity-sensitive vascular lung exhibited the greatest variation of any organ. Importantly, these findings corroborate previous research demonstrating the influence of gravity on cardiopulmonary morphology. Snakes offer useful model systems to help understand the adaptation of organs to a spectrum of conditions related to diversity of behavior and habitat across a broad range of related taxa.     

Gravity and the evolution of cardiopulmonary morphology in snakes

Physiological investigations of snakes have established the importance of heart position and pulmonary structure in contexts of gravity effects on blood circulation. Here we investigate morphological correlates of cardiopulmonary physiology in contexts related to ecology, behavior and evolution. We analyze data for heart position and length of vascular lung in 154 species of snakes that exhibit a broad range of characteristic behaviors and habitat associations. We construct a composite phylogeny for these species, and we codify gravitational stress according to species habitat and behavior. We use conventional regression and phylogenetically independent contrasts to evaluate whether trait diversity is correlated with gravitational habitat related to evolutionary transitions within the composite tree topology. We demonstrate that snake species living in arboreal habitats, or which express strongly climbing behaviors, possess relatively short blood columns between the heart and the head, as well as relatively short vascular lungs, compared to terrestrial species. Aquatic species, which experience little or no gravity stress in water, show the reverse — significantly longer heart-head distance and longer vascular lungs. These phylogenetic differences complement the results of physiological studies and are reflected in multiple habitat transitions during the evolutionary histories of these snake lineages, providing strong evidence that heart-to-head distance and length of vascular lung are co-adaptive cardiopulmonary features of snakes.     

Scaling of Cardiovascular Physiology in Snakes

The elongate body form of snakes and the wide diversity of habitatsinto which they have radiated have affected the form and functionof the cardiovascular system. Heart position is strongly correlatedwith habitat. The heart is located 15–25% of the bodylength from the head in terrestrial and arboreal species, but25–45% in totally aquatic species. Semi-aquatic and fossorialspecies are intermediate. The viperids are exceptional, withgenerally more posterior hearts but arboreal species have heartscloser to the head. An anterior heartis favored when snakesclimb because it reduces the hydrostatic pressure of the bloodcolumn above the heart and tends to stabilize cephalic bloodpressure. In water, where hydrostatic bloodpressure is not aproblem, a more centrally located heart is favored because theheart does less work perfusing the body. In terrestrial species,head-heart distance increases linearly with body length andthe increased hydrostatic pressure is matched by higher restingarterial blood pressure in longer animals. Unlike mammals andbirds, snakes have blood pressures that increasewith body mass.The added stress on the ventricle wall in larger snakes is correlatedwith ventricles that are larger than predicted by other reptiles.Heart mass scales with body mass to the 0.95 power in snakesbut only 0.77–0.91 in other reptiles that are not as subjectto the hydrostatic effects of gravity. The spongy hearts ofreptiles do not conform well to the Principle of Laplace.     

Anatomical position of heart in snakes with vertical orientation: a new hypothesis

It has been observed that climbing arboreal snakes have hearts closer to the head than nonclimbing terrestrial or aquatic snakes. The closeness to the head is said to minimize the work of the heart in pumping blood to the head. However, there is ample evidence that the gravitational pressure in the arteries going to the head is counterbalanced (neutralized) by the gravitational pressure of the blood in the veins going down to the heart. Hence, the heart does not do extra work so, another explanation must be sought. It is proposed that the position of the heart may be related to the filling pressure of the heart which is influenced by the compliance of the vessels above and below the heart. Some observations suggest that the caudal vessels in climbing snakes are less compliant than that of aquatic snakes. This tends to move the hydrostatic indifferent point closer to the head and provides an adequate filling pressure in climbing snakes in the vertical position.     

Morphological adaptations to arboreal habitats and heart position in species of the neotropical whipsnakes genus Chironius

The evolution of arboreality in snakes is accompanied by modifications that are remarkably similar across species. Gravity is one of the most important selective agents, and arboreal snakes present adaptations to circumvent the gradient of pressure, including modifications on heart position (HP) and body slenderness (BS). However, the degree to which different life‐history traits influence the cardiovascular system of snakes remains unclear. Here, we used an ecological and a phylogenetic approach to explore the relationship between habitat, HP, BS, and heart size (HS) in five species of the neotropical whipsnakes genus Chironius that occupy terrestrial, semiarboreal, and arboreal habits. Our ecological comparison indicated that the arboreal species have the most posterior‐positioned heart, the most slender body, and the smallest HS, whereas the terrestrial representative of the group exhibited the most anterior heart, the less flattened body, and the largest HS. After removing the phylogenetic effect, we found no difference in HP and BS between terrestrial and arboreal species. Habitat only differed when contrasting with HS. Body slenderness and HS were correlated with HP. Our results suggest that different restrictions, such as anatomical constraints, behavior, and phylogenetic inertia, may be important for the studied species.     

Length–mass allometry in snakes

Body size and body shape are tightly related to an animal's physiology, ecology and life history, and, as such, play a major role in understanding ecological and evolutionary phenomena. Because organisms have different shapes, only a uniform proxy of size, such as mass, may be suitable for comparisons between taxa. Unfortunately, snake masses are rarely reported in the literature. On the basis of 423 species of snakes in 10 families, we developed clade‐specific equations for the estimation of snake masses from snout–vent lengths and total lengths. We found that snout–vent lengths predict masses better than total lengths. By examining the effects of phylogeny, as well as ecological and life history traits on the relationship between mass and length, we found that viviparous species are heavier than oviparous species, and diurnal species are heavier than nocturnal species. Furthermore, microhabitat preferences profoundly influence body shape: arboreal snakes are lighter than terrestrial snakes, whereas aquatic snakes are heavier than terrestrial snakes of a similar length. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Tolerance of snakes to hypergravity

Sensitivity of carotid blood flow to increased gravitational force acting in the head-to-tail direction(+Gz) was studied in diverse species of snakes hypothesized to show adaptive variation of response. Tolerance to increased gravity was measured red as the maximum graded acceleration force at which carotid blood flow ceased and was shown to vary according to gravitational adaptation of species defined by their ecology and behavior. Multiple regression analysis showed that gravitational habitat, but not body length, had a significant effect on Gz tolerance. At the extremes, carotid blood flow decreased in response to increasing G force and approached zero near +1 Gz in aquatic and ground-dwelling species, whereas in climbing species carotid flow was maintained at forces in excess of +2 Gz. Tolerant (arboreal) species were able to withstand hypergravic forces of +2 to +3 Gz for periods up to 1 h without cessation of carotid blood flow or loss of body movement and tongue flicking. Data suggest that the relatively tight skin characteristic of tolerant species provides a natural antigravity suit and is of prime importance in counteracting Gz stress on blood circulation.     

Marine invasions by non-sea snakes, with thoughts on terrestrial-aquatic-marine transitions

Few species of snakes show extensive adaptations to aquatic environments and even fewer exploit the oceans. A survey of morphology, lifestyles, and habitats of 2552 alethenophidian snakes revealed 362 (14%) that use aquatic environments, are semi-aquatic, or aquatic; about 70 (2.7%) of these are sea snakes (Hydrophiinae and Laticaudinae). The ancient and aquatic family Acrochordidae contains three extant species, all of which have populations inhabiting brackish or marine environments, as well as freshwater. The Homalopsidae have the most ecologically diverse representatives in coastal habitats. Other families containing species exploiting saline waters with populations in freshwater environments include: the Dipsadidae of the western hemisphere, the cosmopolitan Natricidae, the African Grayinae, and probably a few Colubridae. Species with aquatic and semi-aquatic lifestyles are compared with more terrestrial (fossorial, cryptozoic, and arboreal) species for morphological traits and life histories that are convergent with those found in sea snakes; this may provide clues to the evolution of marine snakes and increase our understanding of snake diversity.     

Anatomical and gravitational influences on cardiac displacement in snakes (Lepidosauria,Serpentes)

Summary Radiographs of live, unanesthetized snakes were used to document the position of the heart in the body cavity during horizontal, head-up, and head-down postures. The extent of cardiac displacement observed during these postural changes differed substantially among the snakes examined, ranging from virtually none in a thin-bodied arboreal snake to as much as three vertebral lengths (=half the length of the heart) in a heavy-bodied terrestrial Crotalus. The basis of this differential cardiac displacement is attributed to the anatomical packaging of the pericardial sac. In some snakes the pericardial sac is loosely suspended in the body cavity by the great vessels and connective tissue sheets. In contrast, in other snakes the pericardial sac is buttressed against the body wall, the lung, or the liver. We hypothesize that cardiac displacement during postural change may alter the pattern of blood flow in the aortae of snakes.     

Early experience influences both habitat choice and locomotor performance in tiger snakes

Through adaptive developmental plasticity, individuals may function most effectively in the type of environment in which they have spent most of their time. Such habitat-specific modifications may favor active selection of that habitat type later in life, further reinforcing developmentally plastic phenotypic modifications. The interaction between these processes may have profound evolutionary implications. In nature, Australian tiger snakes (Notechis scutatus) use a complex mosaic of terrestrial, arboreal, and aquatic habitats. We raised juvenile tiger snakes for the first 11 months of life in enclosures mimicking one of these habitats and then tested their habitat selection when offered a choice of habitat types. Snakes consistently selected the habitat types in which they had been reared, and they were more effective at locomotion in those habitats than in the others. This attachment to a familiar habitat and phenotypically flexible adjustments in order to function effectively in that habitat constitute a positive feedback loop. That is, animals benefit by choosing a familiar habitat because they can fine-tune behaviors in ways that enable them to function better in that habitat, and, by consistently selecting that kind of habitat, they not only reinforce those phenotypically plastic adjustments but also are placed under continuing selection to cope with the challenges (of foraging, predator evasion, etc.) imposed by that habitat type. The end result may be to create ecomorphs, whereby different individuals within a population become specialized for different types of habitats even in the absence of genetic differentiation.     

Ecological and phylogenetic variability in the spinalis muscle of snakes

Understanding the origin and maintenance of functionally important subordinate traits is a major goal of evolutionary physiologists and ecomorphologists. Within the confines of a limbless body plan, snakes are diverse in terms of body size and ecology, but we know little about the functional traits that underlie this diversity. We used a phylogenetically diverse group of 131 snake species to examine associations between habitat use, sidewinding locomotion and constriction behaviour with the number of body vertebrae spanned by a single segment of the spinalis muscle, with total numbers of body vertebrae used as a covariate in statistical analyses. We compared models with combinations of these predictors to determine which best fit the data among all species and for the advanced snakes only (N = 114). We used both ordinary least‐squares models and phylogenetic models in which the residuals were modelled as evolving by the Ornstein–Uhlenbeck process. Snakes with greater numbers of vertebrae tended to have spinalis muscles that spanned more vertebrae. Habitat effects dominated models for analyses of all species and advanced snakes only, with the spinalis length spanning more vertebrae in arboreal species and fewer vertebrae in aquatic and burrowing species. Sidewinding specialists had shorter muscle lengths than nonspecialists. The relationship between prey constriction and spinalis length was less clear. Differences among clades were also strong when considering all species, but not for advanced snakes alone. Overall, these results suggest that muscle morphology may have played a key role in the adaptive radiation of snakes.     

Eye size variation reflects habitat and daily activity patterns in colubrid snakes

The functioning of the vertebrate eye depends on its absolute size, which is presumably adapted to specific needs. Eye size variation in lidless and spectacled colubrid snakes was investigated, including 839 specimens belonging to 49 genera, 66 species and subspecies. Variations of adult eye diameters (EDs) in both absolute and relative terms between species were correlated with parameters reflecting behavioral ecology. In absolute terms, eye of arboreal species was larger than in terrestrial and semiaquatic species. For diurnal species, EDs of terrestrial species do not differ from semiaquatic species; for nocturnal species the ED of terrestrial species is larger than fossorial species but not different from semiaquatic species. In relative terms, ED did not differ significantly by habitat for diurnal species. Although the ED of terrestrial species is larger than fossorial species there were no differences for nocturnal species between semiaquatic and fossorial snakes. In contrast to other vertebrates studied to date, colubrid EDs in absolute and relative terms are larger in diurnal than in nocturnal species. These observations suggest that among colubrid snakes, eye size variation reflects adaptation to specific habitats, foraging strategies and daily activities, independently of phylogeny. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

On the structure of the aortic valves in snakes (Reptilia: Serpentes)

Aortic valve morphology was examined in 32 species of snakes representing 28 genera and 11 families and a diversity of habitat preferences. The results largely agree with previous studies but include some previously undescribed features, such as the cranial displacement of the cusps in the left aorta in some species and the structure of the opposing cusps of the interaortic foramen. Few features of the aortic valves are uniform among species. The pattern of morphological variation does not correlate with simple habitat preference (e.g., terrestrial, arboreal); however, some of the variation, particularly in the valves themselves, correlates with taxonomic relationships. We suggest that the presence of an interaortic foramen, with its associated valve, could result in an interaortic shunt of blood that potentially alters hemodynamics and flow patterns in the systemic circulation of snakes. © 1993 Wiley-Liss, Inc.     

Ontogenetic shifts and spatial associations in organ positions for snakes

Snakes possess an elongated body form and serial placement of organs which provides the opportunity to explore historic and adaptive mechanisms of organ position. We examined the influence of body size and sex on the position of, and spatial associations between, the heart, liver, small intestine, and right kidney for ten phylogenetically diverse species of snakes that vary in body shape and habitat. Snake snout–vent length explained much of the variation in the position of these four organs. For all ten species, the position of the heart and liver relative to snout–vent length decreased as a function of size. As body size increased from neonate to adult, these two organs shifted anteriorly an average of 4.7% and 5.7% of snout–vent length, respectively. Similarly, the small intestine and right kidney shifted anteriorly with an increase in snout–vent length for seven and five of the species, respectively. The absolute and relative positioning of these organs did not differ between male and female Burmese pythons (Python molurus). However, for diamondback water snakes (Nerodia rhombifer), the liver and small intestine were more anteriorly positioned in females as compared to males, whereas the right kidney was positioned more anteriorly for males. Correlations of residuals of organ position (deviation from predicted position) demonstrated significant spatial associations between organs for nine of the ten species. For seven species, individuals with hearts more anterior (or posterior) than predicted also tended to possess livers that were similarly anteriorly (or posteriorly) placed. Positive associations between liver and small intestine positions and between small intestine and right kidney positions were observed for six species, while spatial associations between the heart and small intestine, heart and right kidney, and liver and right kidney were observed in three or four species. This study demonstrates that size, sex, and spatial associations may have potential interacting effects when testing evolutionary scenarios for the position of snake organs.     

Why do Juvenile Chinese Pit‐Vipers (Gloydius shedaoensis) Select Arboreal Ambush Sites?

Ontogenetic shifts in habitat use are widespread, especially in ectothermic taxa in which juveniles may be an order of magnitude smaller than large adult conspecifics. The factors that generate such habitat shifts are generally obscure, but we studied an unusual system that allowed us to compare consequences of habitat selection between adults and juveniles. Pit‐vipers (Gloydius shedaoensis) on a small island in north‐eastern China feed almost entirely on seasonally migrating birds. During the spring bird‐migration period, individual snakes consistently re‐used either arboreal or terrestrial ambush sites. Snakes in trees were smaller (and more philopatric) than snakes on the ground. This ontogenetic shift in habitat use may reflect the difficulty of capturing birds on the ground, especially by small snakes. In laboratory trials, large (adult) pit‐vipers struck faster, further and more accurately than did small (juvenile) snakes. In experiments with free‐ranging snakes, the proportion of strikes hitting the bird was lower for juveniles than for adults, and lower for terrestrial snakes than for arboreal snakes. Additionally, adult snakes generally seized the bird by the head whereas juveniles frequently struck the body or wings (and thus, obtained a less secure grip). Arboreal ambush sites may facilitate prey capture not only because they give access to smaller birds but also because they render the bird's location more predictable and, hence, enable the snake to position itself optimally prior to the prey's arrival. Because juvenile pit‐vipers are less capable strikers, and are small relative to available prey items, they may benefit from the greater ease of prey capture from branches. Thus, the ontogenetic shift in habitat selection within this species may be because of ontogenetic shifts in the vipers’ ability to capture and ingest large, mobile prey.     

Morphology and evolution of the snake cornea

To investigate whether the thickness of the cornea in snakes correlates with overall anatomy, habitat or daily activity pattern, we measured corneal thickness using optical coherence tomography scanning in 44 species from 14 families (214 specimens) in the collection at the Natural History Museum (Denmark). Specifically, we analyzed whether the thickness of the cornea varies among species in absolute terms and relative to morphometrics, such as body length, spectacle diameter, and spectacle thickness. Furthermore, we examined whether corneal thickness reflects adaptation to different habitats and/or daily activity patterns. The snakes were defined as arboreal (n = 8), terrestrial (n = 22), fossorial (n = 7), and aquatic (n = 7); 14 species were classified as diurnal and 30 as nocturnal. We reveal that the interspecific variation in corneal thickness is largely explained by differences in body size, but find a tendency towards thicker corneas in diurnal (313 ± 227 μm) compared to nocturnal species (205 ± 169 μm). Furthermore, arboreal snakes had the thickest corneas and fossorial snakes the thinnest. Our study shows that body length, habitat, and daily activity pattern could explain the interspecific variation in corneal morphology among snakes. This study provides a quantitative analysis of the evolution of the corneal morphology in snakes, and it presents baseline values of corneal thickness of multiple snake species. We speculate that the cornea likely plays a role in snake vision, despite the fact that results from previous studies suggest that the cornea in snakes is not relevant for vision (Sivak, Vision Research, 1977, 17, 293–298).     

Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina,Laticaudidae)

Yellow‐lipped sea kraits (Laticauda colubrina) are amphibious in their habits. We measured their locomotor speeds in water and on land to investigate two topics: (1) to what degree have adaptations to increase swimming speed (paddle‐like tail etc.) reduced terrestrial locomotor ability in sea kraits?; and (2) do a sea krait’s sex and body size influence its locomotor ability in these two habitats, as might be expected from the fact that different age and sex classes of sea kraits use the marine and terrestrial environments in different ways? To estimate ancestral states for locomotor performance, we measured speeds of three species of Australian terrestrial elapids that spend part of their time foraging in water. The evolutionary modifications of Laticauda for marine life have enhanced their swimming speeds by about 60%, but decreased their terrestrial locomotor speed by about 80%. Larger snakes moved faster than smaller individuals in absolute terms but were slower in terms of body lengths travelled per second, especially on land. Male sea kraits were faster than females (independent of the body‐size effect), especially on land. Prey items in the gut reduced locomotor speeds both on land and in water. Proteroglyphous snakes may offer exceptional opportunities to study phylogenetic shifts in locomotor ability, because (1) they display multiple independent evolutionary shifts from terrestrial to aquatic habits, and (2) one proteroglyph lineage (the laticaudids) displays considerable intraspecific and interspecific diversity in terms of the degree to which they use terrestrial vs. aquatic habitats.     

Diet and habit explain head-shape convergences in natricine snakes

The concept of ecomorphs, whereby species with similar ecologies have similar phenotypes regardless of their phylogenetic relatedness, is often central to discussions regarding the relationship between ecology and phenotype. However, some aspects of the concept have been questioned, and sometimes species have been grouped as ecomorphs based on phenotypic similarity without demonstrating ecological similarity. Within snakes, similar head shapes have convergently evolved in species living in comparable environments and/or with similar diets. Therefore, ecomorphs could exist in some snake lineages, but this assertion has rarely been tested for a wide-ranging group within a single framework. Natricine snakes (Natricinae) are ecomorphologically diverse and currently distributed in Asia, Africa, Europe and north-central America. They are primarily semiaquatic or ground-dwelling terrestrial snakes, but some are aquatic, burrowing or aquatic and burrowing in habit and may be generalist or specialist in diet. Thus, natricines present an interesting system to test whether snakes from different major habit categories represent ecomorphs. We quantify morphological similarity and disparity in head shape among 191 of the ca. 250 currently recognized natricine species and apply phylogenetic comparative methods to test for convergence. Natricine head shape is largely correlated with habit, but in some burrowers is better explained by dietary specialism. Convergence in head shape is especially strong for aquatic burrowing, semiaquatic and terrestrial ecomorphs and less strong for aquatic and burrowing ecomorphs. The ecomorph concept is useful for understanding natricine diversity and evolution, though would benefit from further refinement, especially for aquatic and burrowing taxa.     

CONSTRAINTS ON REPRODUCTIVE INVESTMENT: A COMPARISON BETWEEN AQUATIC AND TERRESTRIAL SNAKES

Life-history theory predicts that “costs” of reproduction may be important evolutionary determinants of reproductive investment; previous studies on reptiles indicate that decrements to maternal mobility may be among the most important components of such costs. Biomechanical models suggest that reproductive investment in aquatic snakes may be constrained by the important locomotory role of the posterior part of the body during swimming: carrying eggs or offspring in this region would more seriously impair locomotory efficiency in swimming than in terrestrial lateral undulation. If this constraint is important, aquatic snakes would be expected to have lower clutch masses relative to body mass than terrestrial species and to carry the clutch in a more anterior position (commencing at the same proportion of maternal body length anteriorly, but not extending as far posteriorly). Comparisons between aquatic and terrestrial snakes of several families confirm these predictions. Phylogenetic analysis suggests that this pattern of reduced reproductive investment has evolved independently in each of the four ophidian lineages that contain marine species (acrochordids, homalopsine colubrids, laticaudid sea snakes, and hydrophiid sea snakes). Although it thus seems likely that these patterns represent adaptations to aquatic versus terrestrial life, the nature of the selective forces involved remains speculative. The hypothesis based on locomotory impairment of gravid females has better empirical support than any alternative hypothesis, as it successfully predicts modifications in the position of the clutch within the female's body, as well as overall reduced reproductive investment.