Monkey Pulvinar Neurons Fire Differentially to Snake Postures

There is growing evidence from both behavioral and neurophysiological approaches that primates are able to rapidly discriminate visually between snakes and innocuous stimuli. Recent behavioral evidence suggests that primates are also able to discriminate the level of threat posed by snakes, by responding more intensely to a snake model poised to strike than to snake models in coiled or sinusoidal postures (Etting and Isbell 2014). In the present study, we examine the potential for an underlying neurological basis for this ability. Previous research indicated that the pulvinar is highly sensitive to snake images. We thus recorded pulvinar neurons in Japanese macaques (Macaca fuscata) while they viewed photos of snakes in striking and non-striking postures in a delayed non-matching to sample (DNMS) task. Of 821 neurons recorded, 78 visually responsive neurons were tested with the all snake images. We found that pulvinar neurons in the medial and dorsolateral pulvinar responded more strongly to snakes in threat displays poised to strike than snakes in non-threat-displaying postures with no significant difference in response latencies. A multidimensional scaling analysis of the 78 visually responsive neurons indicated that threat-displaying and non-threat-displaying snakes were separated into two different clusters in the first epoch of 50 ms after stimulus onset, suggesting bottom-up visual information processing. These results indicate that pulvinar neurons in primates discriminate between poised to strike from those in non-threat-displaying postures. This neuronal ability likely facilitates behavioral discrimination and has clear adaptive value. Our results are thus consistent with the Snake Detection Theory, which posits that snakes were instrumental in the evolution of primate visual systems.     

Does women's greater fear of snakes and spiders originate in infancy?

Previous studies with adult humans and nonhuman animals revealed more rapid fear learning for spiders and snakes than for mushrooms and flowers. The current experiments tested whether 11-month-olds show a similar effect in learning associative pairings between facial emotions and fear-relevant and fear-irrelevant stimuli. Consistent with the greater incidence of snake and spider phobias in women, results show that female but not male infants learn rapidly to associate negative facial emotions with fear-relevant stimuli. No difference was found between the sexes for fear-irrelevant stimuli. The results are discussed in relation to fear learning, phobias, and a specialized evolved fear mechanism in humans.     

The Distinct Role of the Amygdala,Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes

Introduction

Visual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals.

Methods

Here we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes.

Results

We found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar.

Conclusion

These results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.     

Behaviour of a young smooth snake, Coronella austriaca Laurenti

In August 1976 two broods of the endangered smooth snake ( Coronella austriaca ) were rescued from a fire at a National Nature Reserve. This material provided a unique opportunity in which to observe the behaviour of the young animals before they were returned to nearby heathland. It soon became apparent that the young snakes have narrow food preferences because only the young of lizards were taken. However, evidence is presented which suggests that later they do take the young of small mammals as do adult smooth snakes. Observations on other aspects of their behaviour, such as burrowing, have helped to elucidate the complex day to day behaviour of the adults.     

Gastrointestinal responses to feeding in a frequently feeding colubrid snake (Natrix maura)

Ectotherm vertebrates show physiological mechanisms that reduce metabolic costs during prolonged fasting. Once feeding, these animals adopt a wide variety of metabolic responses such as changes in gastrointestinal organ masses. Up-regulatory responses after feeding have been widely explored in infrequently feeding snakes like pythons, whereas few studies have been devoted to frequently feeding snakes. In this study, we have considered the gastrointestinal responses after feeding in a frequent feeder, the viperine snake Natrix maura, in the Ebro Delta rice fields. In this habitat, viperine snakes are exposed to long periods of food deprivation due to the lack of available prey as a consequence of the man-induced rice cycle. We weighed prey items and full gut masses, and measured length of combined esophagus and stomach, and intestine of viperine snakes belonging to a wide range of sizes. Snakes concentrate foraging activity when rice fields were flooded. In this period, gut masses increased. Likewise, intestines increased in length during the feeding period, which suggests that viperine snakes probably experience a postfeeding hypertrophy of their small intestines that contributes to their larger length. Once the intestine length was corrected for the snake size, it was shown that adults present longer intestines than immature snakes, reflecting an increase in the posterior part of the body linked to the gonads development. This study contributes to explore the physiological responses to feeding in frequently feeding snakes modelled by abrupt shifts of food availability.     

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.     

Molecular evidence that the deadliest sea snake Enhydrina schistosa (Elapidae: Hydrophiinae) consists of two convergent species

We present a striking case of phenotypic convergence within the speciose and taxonomically unstable Hydrophis group of viviparous sea snakes. Enhydrina schistosa, the ‘beaked sea snake’, is abundant in coastal and inshore habitats throughout the Asian and Australian regions, where it is responsible for the large majority of recorded deaths and injuries from sea snake bites. Analyses of five independent mitochondrial and nuclear loci for populations spanning Australia, Indonesia and Sri Lanka indicate that this ‘species’ actually consists of two distinct lineages in Asia and Australia that are not closest relatives. As a result, Australian “E. schistosa” are elevated to species status and provisionally referred to Enhydrina zweifeli. Convergence in the characteristic ‘beaked’ morphology of these species is probably associated with the wide gape required to accommodate their spiny prey. Our findings have important implications for snake bite management in light of the medical importance of beaked sea snakes and the fact that the only sea snake anti-venom available is raised against Malaysian E. schistosa.     

Aposematic colouration does not explain fear of snakes in humans

Snakes elicit a higher level of fear than other vertebrate animals, yet specific cues responsible for fear of snakes are equivocal. The bright colouration hypothesis suggests that fear responses to snakes are triggered by aposematic colouration, not by snakes per se. We investigated the role of aposematic colouration in fear of snakes in a sample of 10- to 15-year-old Slovak children. Both aposematically and cryptically coloured snakes presented as both colour and black-and-white pictures received higher perceived fear scores than other vertebrates. This suggests that aposematic colouration does not play a crucial role in eliciting fear of snakes. Our results support the snake detection theory suggesting that the human visual system has been influenced by long coexistence between predatory snakes and mammals. As a result, humans have evolved an attentional bias ultimately focused on the correct and rapid detection of these threats.     

Coral snake mimicry: live snakes not avoided by a mammalian predator

The occurrence of coral snake coloration among unrelated venomous and non-venomous New World snake species has often been explained in terms of warning coloration and mimicry. The idea that snake predators would avoid coral snakes in nature seems widely established and is postulated in many discussions on coral snake mimicry. However, the few workers that have tested a potential aposematic function of the conspicuous colour pattern focused exclusively on behaviour of snake predators towards coloured abstract models. Here we report on behaviour of temporarily caged, wild coatis (Nasua narica) when confronted with co-occurring live snakes, among which were two species of venomous coral snakes. Five different types of responses have been observed, ranging from avoidance to predation, yet none of the coatis avoided either of the two coral snake species or other species resembling these. As in earlier studies coatis appeared to avoid coral snake models, our findings show that results from studies with abstract snake models cannot unconditionally serve as evidence for an aposematic function of coral snake coloration.     

Rhesus Macaques (Macaca mulatta) Use Posture to Assess Level of Threat From Snakes

Once prey animals have detected predators, they must make decisions about how to respond based on a cost‐benefit analysis of their risk level. The threat sensitivity hypothesis predicts that prey animals match their response to the level of risk, with high‐risk predator encounters eliciting stronger evasive responses than low‐risk encounters. Primates are known prey of snakes, yet they vary their responses toward snakes. We predicted that primates match their response to the threat level from snakes by assessing posture, with striking postures indicating greater risk than coiled postures and coiled postures indicating greater risk than extended sinusoidal postures. We tested this prediction in a series of experimental trials in which captive rhesus macaques (Macaca mulatta) were exposed to snake models in those postures. Results supported the predictions: macaques responded more strongly to a snake model in a striking posture than in a coiled posture and more to a snake model in a coiled posture than to an extended sinusoidal snake model. We also examined responses of macaques to a partially exposed snake model to mimic the condition of incomplete information, as snakes are often occluded by vegetation. The occluded snake model evoked a response comparable to that of the striking snake. These findings support the threat sensitivity hypothesis. Rhesus macaques use the posture of snakes as a cue in threat assessment, responding more intensely as threat increases, and they also behave as if risk is elevated when their information about snakes is incomplete.     

The Hidden Snake in the Grass: Superior Detection of Snakes in Challenging Attentional Conditions

Snakes have provided a serious threat to primates throughout evolution. Furthermore, bites by venomous snakes still cause significant morbidity and mortality in tropical regions of the world. According to the Snake Detection Theory (SDT Isbell, 2006; 2009), the vital need to detect camouflaged snakes provided strong evolutionary pressure to develop astute perceptual capacity in animals that were potential targets for snake attacks. We performed a series of behavioral tests that assessed snake detection under conditions that may have been critical for survival. We used spiders as the control stimulus because they are also a common object of phobias and rated negatively by the general population, thus commonly lumped together with snakes as “evolutionary fear-relevant”. Across four experiments (N = 205) we demonstrate an advantage in snake detection, which was particularly obvious under visual conditions known to impede detection of a wide array of common stimuli, for example brief stimulus exposures, stimuli presentation in the visual periphery, and stimuli camouflaged in a cluttered environment. Our results demonstrate a striking independence of snake detection from ecological factors that impede the detection of other stimuli, which suggests that, consistent with the SDT, they reflect a specific biological adaptation. Nonetheless, the empirical tests we report are limited to only one aspect of this rich theory, which integrates findings across a wide array of scientific disciplines.     

Why do kangaroo rats (Dipodomys spectabilis) footdrum at snakes?

We examined alternative hypotheses for the benefits of footdrummingin the presence of snakes by the banner-tailed kangaroo rat,Dipodomys spectabitis, by testing whether the target of thesignal includes conspecifics, the predator or both. Footdrummingrecorded in the field revealed that rats altered their footdrummingsignatures when drumming at snakes. In playback tests, however,neighbors failed to show any measurable change in behavior tobroadcasts of the snake drumming pattern, but mothers footdrummedsignificantly more than nonmothen in the presence of a tetheredsnake. Gopher snakes, Pituophis melanolsucus affinis, respondedto footdrumming vibrations created by a mechanical thumper.Nonhungry snakes avoided footdrumming, while hungry snakes approachedthe seismic footdrumming. Snakes decreased stalking rates asfootdrumming increased, but they spent more time stalking drummingthan nondnimming rats. We conclude that D. spectabilis footdrumsin individual defense and in parental care, rather than to warnadult conspecfics. Footdrumming deters pursuit by informingthe snake that the rat is alert and the chances of predationare low. We find little evidence that footdrumming startles,confuses, or harasses the snake. Hungry gopher snakes, however,may locate prey by eavesdropping on territorial footdrumming     

Canine detection of free-ranging brown treesnakes on Guam

We investigated canine teams (dogs and their handlers) on Guam as a potential tool for finding invasive brown treesnakes (Boiga irregularis) in the wild. Canine teams searched a 40 × 40 m forested area for a snake that had consumed a dead mouse containing a radio-transmitter. To avoid tainting the target or target area with human scent, no snake was handled or closely approached prior to searches. Trials were conducted during the morning when these nocturnal snakes were usually hidden in refugia. A radiotracker knew the snake's location, but dog handlers and search navigators did not. Of 85 trials conducted over four months, the two canine teams had an average success rate of 35% of correctly defining an area ≤ 5 × 5 m that contained the transmittered snake; the team with more experience prior to the trials had a success rate of 44% compared with 26% for the less experienced team. Canine teams also found 11 shed skins from wild snakes. Although dogs alerted outside the vicinity of transmittered snakes, only one wild, non-transmittered snake was found during the trials, possibly reflecting the difficulty humans have in locating non-transmittered brown treesnakes in refugia. We evaluated success at finding snakes as a function of canine team, number of prior trials (i.e. experience gained during the trials), recent canine success at finding a target snake, various environmental conditions, snake perch height, and snake characteristics (snout-vent length and sex). Success rate increased over the course of the trials. Canine team success also increased with increasing average humidity and decreased with increasing average wind speed. Our results suggest dogs could be useful at detecting brown treesnakes in refugia, particularly when compared to daytime visual searches by humans, but techniques are needed to help humans find and extract snakes once a dog has alerted.     

Fungus gardens of the leafcutter ant Atta colombica function as egg nurseries for the snake Leptodeira annulata

Attine ants are well known for their mutualistic symbiosis with fungus gardens, but many other symbionts and commensals have been described. Here, we report the discovery of two clusters of large snake eggs in neighboring fungus gardens of a mature Atta colombica colony. The eggs were completely embedded within the fungus garden and were ignored by the host ants, even when we placed them into another, freshly excavated fungus garden of the same colony. All five eggs contained embryos and two snakes eventually hatched, which we identified as being banded cat eyed snakes Leptodeira annulata L. Ant fungus gardens are likely to provide ideal climatic conditions for developing snake eggs and almost complete protection from egg predation. Our observations therefore indicate that mature banded cat eyed snakes are able to enter and oviposit in large and well defended Atta colonies without being attacked by ant soldiers and that also newly hatched snakes manage to avoid ant attacks when they leaving their host colony. We speculate that L. annulata might use Atta and Acromyrmex leafcutter ant colonies as egg nurseries by some form of chemical insignificance, but more work is needed to understand the details of this interaction. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effects of size, sex, temperature and condition on activity metabolism and defence behaviour of the viperine snake, Natrix maura

The activity metabolism (aerobic and anaerobic), performance (burst speed and endurance) and defence behaviour (static or active) of the snake Natrix maura were investigated in relation to size, sex, temperature and fasting. Conditions which reduced performance (low temperature, fasting) promoted the use of static defensive behaviour. Aerobic scope for activity decreased with increasing size, but this was compensated for by increased capacity for anaerobic metabolism. Burst speed (as lengths time^-1) was slightly lower in large snakes; endurance was much lower in small snakes. Increased use of static defence by small snakes is related to their predators, which are likely to take occasional snakes in a diet of worms; a balled, still snake may not provide a stimulus for feeding. Large snakes have predators which feed on vertebrates and may recognize them as food in any position, and so they are better off trying to escape.
Aerobic scope was not maximal at the mean selected body temperature (25 °C), but increased right up to near lethal temperatures (> 35 °C). Anaerobic metabolism (lactate production) was less temperature-sensitive, and accounted for about 80 and 50% of the energy produced during 30 and 5 min of maximal activity, respectively. Resting and active oxygen consumption were weight-dependent, VO₂∝ W^0·75, the same exponent as that of interspecific comparisons. This exponent was independent of temperature and acclimation state. Acclimation to a variable or constant temperature regime had no effect on maximal oxygen consumption, but there was a significant effect on resting metabolic rate, possibly attributable to energy conservation when inactive. There were no differences in activity metabolism, performance or defence behaviour between similar-sized snakes of different sexes.     

Molecular evidence and marine snake origins

A molecular phylogeny was used to refute the marine scenario for snake origins. Nuclear gene sequences suggested that snakes are not closely related to living varanid lizards, thus also apparently contradicting proposed relationships between snakes and marine mosasaurs (usually considered to be varanoids). However, mosasaurs share derived similarities with both snakes and living varanids. A reanalysis of the morphological data suggests that, if the relationships between living taxa are constrained to the proposed molecular tree, with fossil forms allowed to insert in their optimal positions within this framework, mosasaurs cluster with snakes rather than with varanids. Combined morphological and molecular analyses also still unite marine lizards with snakes. Thus, the molecular data do not refute the phylogenetic evidence for a marine origin of snakes.     

Feeding behavior and venom toxicity of coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity

The feeding behavior and venom toxicity of the coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity were investigated. Coral snakes searched for their prey (the colubrid snake Geophis godmani) in the cages. Once their preys were located, coral snakes stroke them with a rapid forward movement, biting predominantly in the anterior region of the body. In order to assess the role of venom in prey restraint and ingestion, a group of coral snakes was 'milked' in order to drastically reduce the venom content in their glands. Significant differences were observed between snakes with venom, i.e., 'nonmilked' snakes, and 'milked' snakes regarding their behavior after the bite. The former remained hold to the prey until paralysis was achieved, whereas the latter, in the absence of paralysis, moved their head towards the head of the prey and bit the skull to achieve prey immobilization by mechanical means. There were no significant differences in the time of ingestion between these two groups of coral snakes. Susceptibility to the lethal effect of coral snake venom greatly differed in four colubrid species; G. godmani showed the highest susceptibility, followed by Geophis brachycephalus, whereas Ninia psephota and Ninia maculata were highly resistant to this venom. In addition, the blood serum of N. maculata, but not that of G. brachycephalus, prolonged the time of death of mice injected with 2 LD(50)s of M. nigrocinctus venom, when venom and blood serum were incubated before testing. Subcutaneous injection of coral snake venom in G. godmani induced neurotoxicity and myotoxicity, without causing hemorrhage and without affecting heart and lungs. It is concluded that (a) M. nigrocinctus venom plays a role in prey immobilization, (b) venom induces neurotoxic and myotoxic effects in colubrid snakes which comprise part of their natural prey, and (c) some colubrid snakes of the genus Ninia present a conspicuous resistance to the toxic action of M. nigrocinctus venom.     

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).     

Variation in the diet of the viperine snake Natvix mama in relation to prey availability

The diet of the viperine snake was compared with food availability in the Ebro Delta, a wetland largely occupied by rice fields, in 1990 and 1991. Snake selection of prey type and size was studied seasonally and by snake group: males, females and immature snakes. Overall, feeding activity (percentage of individuals with prey and number of prey per stomach) increased with food availability. Diet analysis showed that viperine snakes mainly foraged on the green frog Rana perezi (adults and tadpoles) and the carp Cyprinus earpio. Conversely, viperine snakes rejected the mosquito fish Gambusia holbroki which is the most abundant species in autumn, when Natrix maura has a low feeding activity. Statistical comparisons between viperine snake diet and prey availability showed that males selected small carp, immature snakes selected tadpoles and, in spring, females selected frogs. The selection of small carp by males may reflect a sexual divergence of trophic niche related to sexual size dimorphism, as females are larger than males. As tadpoles are presumably easier to catch than fish, tadpole selection by immature individuals may reflect variance in capture abilities. In spring, the selection of frogs by females overlapped with vitellogenesis, suggesting that females compensate for the cost of reproduction by selecting green frogs, which have a greater biomass and higher energy content than fish. Carps eaten in spring were smaller than in summer. Moreover, in summer viperine snakes selected smaller carp than the available mean size. This divergent tendency between carp size selection and carp size availability reveals how seasonal diet shifts in prey size selection may be a response to an increase in prey size.     

Cross-hybridizing snake satellite, Drosophila, and mouse DNA sequences may have arisen independently

Previous reports have interpreted hybridization between snake satellite DNA and DNA clones from a variety of distant taxonomic groups as evidence for evolutionary conservation, which implies common ancestry (homology) and/or convergence (analogy) to produce the cross- hybridizing sequences. We have isolated 11 clones from a genomic library of Drosophila melanogaster, using a cloned 2.5-kb snake satellite probe of known nucleotide sequence. We have also analysed published sequence data from snakes, mice, and Drosophila. These data show that (1) all of the cross-hybridization between the snake, fly, and mouse clones can be accounted for by the presence of either of two tandem repeats, [GATA]n and [GACA]n and (2) these tandem repeats are organized differently among the different species. We find no evidence that these sequences are homologous apart from the existence of the simple repeat itself, although their divergence from a common ancestral sequence cannot be ruled out. The sequences contain a variety of homogeneous clusters of tandem repeats of CATA, GA, TA, and CA, as well as GATA and GACA. We suggest that these motifs may have arisen by a self-accelerating process involving slipped-strand mispairing of DNA. Homogeneity of the clusters might simply be the result of a rate of accumulation of tandem repeats that exceeds that of other mutations.