The morphology of the suboccipital region in snakes,and the anatomical and functional diversity of the myodural bridge

The myodural bridge, that is, skeletal muscle fibers attaching to the cervical dura mater, has been described from a variety of mammals and other amniotes. To test an earlier assumption about the presence of the myodural bridge in snakes, a comparative study was designed using a group of Colubrine snakes. Serial histological sections revealed no evidence of the myodural bridge in any of the snakes examined. Further analyses, including histology, computed tomography (CT), and micro-CT imaging of other distantly related snakes, also turned up no evidence of a myodural bridge. The close apposition of adjacent neural arches in snakes may preclude muscle tendons from passing through the intervertebral joint to reach the spinal dura. It is hypothesized that the myodural bridge functions in the clearance of the cerebrospinal fluid (CSF) by creating episodic CSF pressure pulsations, and that snakes are capable of creating equivalent CSF pressure pulsations through vertebral displacement.     

Venom glands and some associated muscles in sea snakes

The venom glands and related muscles of sea snakes conform in their general structure to those of the terrestrial elapids. The venom gland, however, is smaller in size and the accessory gland is considerably reduced. A similar pattern is found in the Australian elapid Notechis. The musculus compressor glandulae is well developed in the sea snakes and in some species its posterior-medial portion runs uninterruptedly from the origin to the insertion of the muscle. This might be considered as a primitive condition suggesting an early divergence of the sea snakes from an ancestral elapid stock. Three species of sea snakes, Aipysurus eydouxi, Emydocephalus annulatus, and E. ijimae, feed on fish eggs and have very small, but still functioning, venom glands. The reduced accessory gland of the sea snakes is apparently connected with their aquatic environment, as a similar condition is found also in the elapine Boulengerina annulata which lives in large lakes of Central Africa. The similarity in structure of the venom gland between sea snakes and Notechis scutatus may point to a possible phylogenetic relationship between this group of Australian elapids and hydrophiine snakes.     

Genetic analyses of Pseudomonas aeruginosa isolated from healthy captive snakes: evidence of high inter‐ and intrasite dissemination and occurrence of antibiotic resistance genes

Faecal carriage of Pseudomonas aeruginosa was investigated by selective plating and PCR identification test, among healthy captive snakes from zoological and private collections from France as well as from wild snakes from Guinea. P. aeruginosa faecal carriage among captive snakes was high (72 out of 83 individuals), but low among wild specimen (3 out of 23 individuals). Genetic diversity analyses of the isolates, based on SpeI‐PFGE profiles, evidenced five dominant clones or clonal complexes spreading among snakes within a site and between sites and persisting over time. Similar clones or clonal complexes were detected from mouth swabs of the owners and from water and preys used to feed the snakes, evidencing various sources of snake colonization and the first cases of P. aeruginosa cross‐contamination between snakes and owners. These observations led to the conclusion that P. aeruginosa behaves as an opportunistic species within snakes in captivity and that colonization and dissemination occurs consecutively to processes similar to those identified within the hospital. Antibiotic susceptibility testing showed that most isolates had a wild‐type resistance profile except for one persistent clone isolated from both snakes and preys that harboured multiple antimicrobial resistance genes mediated by an integron carrying the qacH, aadB, aadA2 and cmlA10 cassettes, and a tetA(C)‐carrying transposon. Biocides or antibiotics used in the zoological garden could have led to the acquisition of this integron.     

The anatomy of the upper cretaceous snake Najash rionegrina Apesteguía & Zaher, 2006, and the evolution of limblessness in snakes

Najash rionegrina Apesteguía & Zaher, 2006 , a terrestrial fossil snake from the Upper Cretaceous of Argentina, represents the first known snake with a sacrum associated with robust, well‐developed hind limbs. Najash rionegrina documents an important gap in the evolutionary development towards limblessness, because its phylogenetic affinities suggest that it is the sister group of all modern snakes, including the limbed Tethyan snakes Pachyrhachis, Haasiophis, and Eupodophis. The latter three limbed marine fossil snakes are shown to be more derived morphologically, because they lack a sacrum, but have articulated lymphapophyses, and their appendicular skeleton is enclosed by the rib cage, as in modern snakes.     

The forebrain and midbrain of some squamates and their bearing on the origin of snakes

Anatomical analysis of the forebrain and midbrain of Anelytropsis, Dibamus and feyliniids reveals structural similarities with those of skinks and snakes. Skinks and feyliniids are probably derived from a common ancestral stock. This is suggested by mutual reduction of several telencephalic nuclei, by similar trends in the development of the dorsal thalamus, and by similarities in the lamination of their optic tecta. Anelytropsis, Dibamus, feyliniids and snakes show interdigitation of the periventricular gray zones of the optic tectum and enlargement of lamina 7 of the posterior colliculus. Of these three taxa, Dibamus is most similar to burrowing snakes and many of its brain characters are intermediate between skinks and burrowing snakes. These similarities may suggest common ancestry between Dibamus and snakes rather than parallelism.     

Are gobiid fish more susceptible to predation if parasitized by Eustrongylides excisus? An answer from robbed snakes

Aspects of the predator–prey relationship between dice snake, Natrix tessellata and gobiid fish infected with Eustrongylides excisus were studied in Lake Sinoe, Romania. A population of snakes residing here shows a high prevalence of subcutaneous larvae of this nematode. The hypothesis of the altered motility in infected fish leading to increased depredation by snakes was tested by comparing gobiids collected from dice snakes with gobiids caught via electrofishing. Out of a total of seven identified gobiid species, three were used for analysis: syrman goby Neogobius syrman, mushroom goby Neogobius eurycephalus, and round goby Neogobius melanostomus. No significant differences in prevalence and intensity of E. excisus infection were found between fish caught by snakes and those obtained by electrofishing. However, significantly higher abundance of E. excisus larvae in fish caught by snakes was reported. These findings suggest limited influence of the presence of E. excisus larvae in studied gobiids regarding their susceptibility to predation by dice snakes.     

Evolution of sex-chromosomes and formation of W-chromatin in snakes

The analysis of sex-chromosome complexes and formation of W-chromatin in 16 species of snakes of the families Boidae, Colubridae, Elapidae, and Hydrophiidae, reveal three very pertinent facts. First, the snakes exhibit various states of the differentiation of the Z and W chromosomes, apparently according to the evolutionary status of the families, being homomorphic in primitive families and well differentiated in highly evolved ones. Second, the demonstration of a heteropycnotic body in the interphase nuclei of the families of a large number of species of snakes has definitely shown that the nuclear sexing is possible not only in those species of snakes where the W chromosome is morphologically distinguishable from the Z, but also in those species where it is not so, but shows an asynchrony in the replicating pattern of W. It is suggested that development of allocycly rather than establishment of structural changes is the first step in the differentiation of the W from the Z in snakes. Third, the absence of coexistence of nucleolus and W-chromatin in a condensed state in the interphase nuclei of different tissues in a few species of snakes reported in this paper suggests that the W-chromatin is responsible for the synthesis of the nucleolus in these snakes.Paper presented at the Third Oxford Chromosome Conference, September, 1970.     

Cytogenetics of the Javan file snake (Acrochordus javanicus) and the evolution of snake sex chromosomes

Advanced snakes (Caenophidia) are an important group including around 90% of the recent species of snakes. The basal splitting of the clade is still rather controversial, and it is not fully understood when the differentiation of sex chromosomes started in snake evolution. To help resolve these questions, we performed cytogenetic analysis on the Javan file snake, also known as the elephant trunk snake (Acrochordus javanicus) from the family Acrochordidae, which occupies an informative phylogenetic position. For the first time for acrochordids, we identified heteromorphic ZZ/ZW sex chromosomes with a highly heterochromatic W chromosome. These traits are likely synapomorphies of advanced snakes. In contrast to other caenophidian snakes, the Javan file snake lacks an accumulation of Bkm repeats and interstitial telomeric repeats on the W chromosome. This observation supports the sister group relationship between acrochordids and all other caenophidian snakes including the family Xenodermatidae and questions the suggested role of Bkm repeats in the formation of sex heterochromatin in snakes. The revealed partial gene content of the Z chromosome in acrochordids supports the hypothesis that the progressive degeneration of the W chromosome commenced in snakes before the basal split of Caenophidia, albeit its evolutionary rate in file snakes might be slower than in their sister lineage.     

Physiological and hormonal control of thermal depression in the tiger snake, Notechis scutatus

Plasma sodium concentrations in field-caught Western tiger snakes, Notechis scutatus, from semi-arid Carnac Island (CI) varied seasonally, with snakes exhibiting significant hypernatraemia during summer and normal concentrations following autumn rain. In contrast, field-caught tiger snakes from a perennial fresh-water swamp (Herdsman Lake, HL) exhibited no significant increase in plasma sodium concentrations during summer. Laboratory-induced hypernatraemia caused thermal depression in both populations; there was a weak negative relationship between plasma sodium concentration and temperature selection that was significant for CI snakes. Hypernatraemia significantly elevated circulating concentrations of the neuropeptide arginine vasotocin (AVT) in both CI and HL snakes. CI snakes injected with a physiological dosage of AVT also evidenced thermal depression. Despite the positive correlation between AVT and both plasma sodium concentration and osmolality for laboratory snakes, field samples from CI snakes indicate that circulating levels of AVT may be influenced more by plasma osmolality than sodium levels. The data suggest that, in CI snakes, chronic dehydration in the field leads to hypernatraemia which may lead to elevated levels of AVT if plasma osmolality also increases. This will in turn invoke a depression in thermal behaviour that may improve the water economy and survival of snakes on semi-arid CI. Although HL snakes do not experience seasonal dehydration, physiological changes away from the stable homeostatic state appear to prompt the same behavioural shifts, illustrating the intrinsic nature of the thermal behaviour in different populations of the same species of snake.     

Systematics of the Eimerian Parasites from North American Snakes of the Family Colubridae,and their Prevalence in the Colubrids of Iowa*

A survey of 117 Iowa snakes, representing 18 species within 12 genera, revealed the presence of 6 species of Eimeria, 5 of which are described as new and 1 of which (E. zamenis) is redescribed. Those species found, the average length-width dimensions of their oocysts ( in micrometers ), and the respective hosts from which they were isolated were as follows: E. attenuata sp. n., 22.2 × 12.6, from 1 of 25 red-sided garter snakes [Thamnophis sirtalis parietalis (Say)] and 1 of 14 northern water snakes [Natrix sipedon sipedon (Linnaeus)]; E. iowaensis sp. n., 17.8 × 14.5, from 1 of 25 redsided garter snakes; E. hydrophis sp. n., 15.4 × 10.9, from 5 of 14 northern water snakes and 1 of 1 diamond-backed water snake [N. rhombifera rhombifera (Hallowell)]; E. helmisophis sp. n., 13.8 × 10.6, from 1 of 5 western worm snakes [Carphophis amoenus vermis (Kennicott)]; E. collanuli sp. n., 33.1 × 18.3, from 1 of 14 prairie ring-neck snakes (Diadophis punctatus arnyi Kennicott), and E. zamenis, 31.0 × 17.0, from 1 of 6 eastern yellow-bellied racers (Coluber constrictor flaviventris Say) and 1 of 1 eastern milk snake [Lampropeltis triangulum triangulum (Lacépède)]. The overall infection rate for the 117 snakes examined was 9.2%; these data are tabulated. In addition, the possible synonymy of E. lampropeltis with E. zamenis is considered, and the probable status of E. attenuata, E. hydrophis, E. zamenis, and E. annea, as parasites of multiple host species, is reviewed with regard to the phylogenetic relationships of the respective hosts from which they have been reported.     

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).     

Amphibians and squamates from the Neogene Siwalik beds of Jammu and Kashmir, India

The Neogene Siwalik deposits of Jammu Province (India) have yielded amphibians and squamates. The collection includes the first amphibians and the first colubroid snakes from the Siwalik Group. Amphibians comprise only anurans: a possible Ranidae and one, or perhaps two, non-ranid frogs Squamates include one lizard,Varanus sp. (Varanidae), whereas snakes are represented by three taxa:Acrochordus dehmi (Acrochordidae), an indeterminate Colubridae, and a snake that is either a Colubridae or an Elapidae.Varanus sp. andA. dehmi have been yielded by the Upper Miocene Ramnagar Member, whereas the anurans and colubroid snakes come from the Upper Pliocene Labli Member. These taxa are indicative of aquatic palaeoenvironment.     

Induced defences in an endangered amphibian in response to an introduced snake predator

Introduced species have contributed significantly to the extinction of endemic species on islands. They also create new selection pressures on their prey that may result in modified life history strategies. Introduced viperine snakes (Natrix maura) have been implicated in the decline of the endemic midwife toad of Mallorca (Alytes muletensis). A comparison of A. muletensis tadpoles in natural pools with and without snakes showed that those populations subject to snake predation possessed longer tails with narrower tail fins but deeper tail muscles. Field and laboratory experiments showed that these changes in tail morphology could be induced by chemical and tactile cues from snakes. Populations of tadpoles that were subject to snake predation also displayed clear bimodal size-frequency distributions, with intermediate-sized tadpoles missing from the pools completely. Tadpoles in pools frequented by snakes developed faster in relation to their body size than those in pools without snakes. Variation in morphology between toad populations may therefore be caused by a combination of size-selective predation and tadpole plasticity. The results of this study indicate that the introduction of alien species can result in selection for induced defences, which may facilitate coexistence between predator and prey under certain conditions.     

The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Golubridae)

The bright coloured, highly venomous coral snakes, Leptomicrurus, Micrurus and Micruroides (family Elapidae) and a series of harmless or mildly toxic mimics form an important component of the snake fauna of the Americas. Coral snake patterns are defined as any dorsal pattern found in any species of venomous coral snake and/or any dorsal pattern containing a substantial amount of red, pink or orange distributed so as to resemble that of some species of venomous coral snake. The components of coral snake colouration are described and four principal dorsal patterns are recognized: unicolour, bicolour, tricolour and quadricolour. The tricolour patterns may be further clustered based on the number of black bands or rings separating the red ones as: monads, dyads, triads, tetrads or pentads. A detailed classification of all coral snake colour patterns is presented and each pattern is illustrated. The taxonomic distribution of these patterns is surveyed for mimics and the 56 species of highly venomous coral snakes. Among the latter, the most frequent encountered patterns are tricolour monads, tricolour triads and bicolour rings, in that order. No venomous coral snakes have a tricolour dyad, tricolour tetrad or quadricolour pattern. As many as 115 species of harmless or mildly toxic species, c. 18% of all American snakes, are regarded as coral snake mimics. The colouration and behavioural traits of venomous coral snakes combine to form a significant antipredator defence of an aposematic type. The mimics in turn receive protection from predators that innately or through learning avoid coral snake colour patterns. The precise resemblances in colouration between sympatric non-coral snakes and venomous coral snakes and the concordant geographic variation between the two strongly support this view. Batesian mimicry with the highly venomous coral snakes as the models and the other forms as the mimics is the favoured explanation for this situation. It is further concluded that a number of species in the genera Elaphe, Farancia, Nerodia and Thamnophis, although having red in their colouration, should not be included in the coral snake mimic guild.     

Mitochondrial DNA sequences suggest unexpected phylogenetic position of Corso-Sardinian grass snakes (<Emphasis Type="Italic">Natrix cetti</Emphasis>) and do not support their species status,with notes on phylogeography and subspecies delineation of grass snakes

We supplement a previously published mitochondrial DNA data set of grass snake sequences (ND1, ND2, ND4, cyt b, in total 3,806 bp) with sequences of Corso-Sardinian and Tuscan specimens and infer their phylogeny using Bayesian, maximum likelihood and maximum parsimony methods. In addition, we estimate divergence times of grass snake clades using a relaxed molecular clock calibrated with fossil evidence, and, in a second approach, the post-Messinian reopening of the Strait of Gibraltar. Recently it was suggested that Corso-Sardinian grass snakes represent a distinct species: Natrix cetti. All tree-building methods revealed well-supported branching patterns and deep divergences among grass snakes. However, sequences of N. natrix were consistently paraphyletic with respect to Corso-Sardinian sequences. The sister group of Corso-Sardinian grass snakes is a clade embracing N. n. helvetica and N. n. lanzai. Extensive gene flow between N. n. helvetica and a more distantly related subspecies (N. n. natrix) is well known, which is why we conclude that the status of Corso-Sardinian grass snakes as subspecies of N. natrix should be reinstated. Many currently recognized grass snake subspecies conflict with mitochondrial clades, suggestive of inappropriate morphological taxon delineation and mitochondrial introgression. Divergences among grass snakes are old, and the results of the two independent dating approaches are largely congruent. Accordingly, the Alpine orogenesis seems to have caused the origin of the oldest clade, corresponding to Iberian N. n. astreptophora. The formation of Corso-Sardinian grass snakes was dated to the Early Pliocene and could result from post-Messinian flooding of the Mediterranean Basin. Another deeply divergent clade of approximately the same age, endemic in central and northern Europe, suggests the Pleistocene survival of grass snakes north of the Alps. At least one glacial refuge in which old lineages survived Pleistocene cold periods was located on each of the three major southern European peninsulas and in Anatolia. Due to pronounced sequence divergences among Italian and southern Swiss grass snakes, we hypothesize multiple refugia south of the Alps and in the Apennine Peninsula, and there is evidence for two refuges on the Balkan Peninsula.     

Black Bear Reactions to Venomous and Non‐venomous Snakes in Eastern North America

Bears are often considered ecological equivalents of large primates, but the latter often respond with fear, avoidance, and alarm calls to snakes, both venomous and non‐venomous, there is sparse information on how bears respond to snakes. We videotaped or directly observed natural encounters between black bears (Ursus americanus) and snakes. Inside the range of venomous snakes in Arkansas and West Virginia, adolescent and adult black bears reacted fearfully in seven of seven encounters upon becoming aware of venomous and non‐venomous snakes; but in northern Michigan and Minnesota where venomous snakes have been absent for millennia, black bears showed little or no fear in four encounters with non‐venomous snakes of three species. The possible roles of experience and evolution in bear reactions to snakes and vice versa are discussed. In all areas studied, black bears had difficulty to recognize non‐moving snakes by smell or sight. Bears did not react until snakes moved in 11 of 12 encounters with non‐moving timber rattlesnakes (Crotalus horridus) and four species of harmless snakes. However, in additional tests in this study, bears were repulsed by garter snakes that had excreted pungent anal exudates, which may help explain the absence of snakes, both venomous and harmless, in bear diets reported to date.     

The snake hiss: potential acoustic mimicry in a viper–colubrid complex

Examples of acoustic Batesian mimicry are scarce, in contrast to visual mimicry. Here we describe a potential case of acoustic mimicry of a venomous viper model by harmless viperine snakes (colubrid). Viperine snakes resemble vipers in size, shape, colour, pattern, and anti‐predatory behaviours, including head flattening, false strikes, and hissing. We sought to investigate whether hissing evolved as part of, or separately to, the viper mimic syndrome. To do this, we recorded and analysed the hissing sounds of several individual asp vipers, viperine snakes, and grass snakes (a close relative of viperine snakes that hisses but does not mimic the asp viper). Frequencies consistently ranged from 40 to 12 000 Hz across species and individuals. All vipers (100%) and most viperine snakes (84%) produced inhalation hissing sounds, in comparison to only 25% of grass snakes. Inhalation hissing sounds lasted longer in vipers than in viperine snakes. The hissing‐sound composition of grass snakes differed significantly from that of both asp vipers and viperine snakes; however, the hissing‐sound composition between viperine snakes and asp vipers was not statistically distinguishable. Whilst grass snake hissing sounds were characterized by high frequencies (5000–10 000 Hz), both vipers and viperine snake hissing sounds were dominated by low frequencies (200–400 Hz). A principal component analysis revealed no overlap between grass snakes and vipers, but important overlaps between viperine snakes and vipers, and between viperine snakes and grass snakes. The likelihood that these overlaps respectively reflect natural selection for Batesian mimicry and phylogeny constraints is discussed. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1107–1114.     

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.     

Ontogenetic change in blood oxygen capacity and maximum activity in garter snakes (Thamnophis sirtalis)

Summary There is an ontogenetic increase in the time that garter snakes (Thamnophis s. sirtalis) can maintain maximum activity at 25°C. Newborn snakes are exhausted by 3–5 min of activity while adults can be active for 20–25 min. The increased endurance of adult snakes results from ontogenetic increases in both aerobic and anaerobic energy generation. At rest juvenile and adult snakes have the same whole-body lactic acid concentrations, but at exhaustion adult lactic acid concentrations are 1.5 times those of juveniles. This increase in anaerobic energy production accounts for part of the endurance of adult snakes, but increased aerobic metabolism appears to be more important. Among the mechanisms increasing aerobic metabolism are more effective pulmonary ventilation and a 3-fold ontogenetic increase in blood oxygen capacity.The rapid exhaustion of small garter snakes probably limits the microhabitats they can occupy and the sorts of hunting methods they can employ. Small garter snakes feed only on small prey that are easily subdued. There is an ontogenetic increase in the relative size of prey eaten by garter snakes that parallels the ontogenetic increase in endurance. Adult feeding habits are adopted at the same body size at which adult blood oxygen capacity and endurance are attained.