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.     

Response to visual threat following damage to the pulvinar

We present a unique case demonstrating contributions of the pulvinar in response to visual threat. Substantial evidence demonstrates that the amygdala contributes to the emotion of fear and the response to threat. Traditionally, two routes to amygdala activation have been distinguished: a "slow cortical" route through visual and association cortex and a "fast subcortical" route through the thalamus. The pulvinar nucleus of the thalamus is well connected to the amygdala, suggesting that pulvinar damage might interfere with amygdala activation and response to threat. We tested this possibility in patient SM, who suffered complete loss of the left pulvinar. We measured interference from threatening images on goal-directed behavior. In SM's ipsilesional field, threatening images slowed responses more than pleasant images did. This interference decreased rapidly over time. In contrast, in SM's contralesional field, interference from threatening images was initially absent and then increased rather than decreased over time. Processing through the pulvinar therefore plays a significant role in generating response to visual threat. We suggest that, with disruption of the subcortical route to the amygdala, briefly presented images were not fully processed for threat. The reemergence of interference over time may reflect contributions of a slower route.     

Scales drive detection,attention, and memory of snakes in wild vervet monkeys (<Emphasis Type="Italic">Chlorocebus pygerythrus</Emphasis>)

Predatory snakes are argued to have been largely responsible for the origin of primates via selection favoring expansion of the primate visual system, and even today snakes can be deadly to primates. Neurobiological research is now beginning to reveal the mechanisms underlying the ability of primates (including humans) to detect snakes more rapidly than other stimuli. However, the visual cues allowing rapid detection of snakes, and the cognitive and ecological conditions contributing to faster detection, are unclear. Since snakes are often partially obscured by vegetation, the more salient cues are predicted to occur in small units. Here we tested for the salience of snake scales as the smallest of potential visual cues by presenting four groups of wild vervet monkeys (Chlorocebus pytherythrus) with a gopher snake (Pituophis catenifer) skin occluded except for no more than 2.7 cm, in natural form and flat, the latter to control for even small curvilinear cues from their unusual body shape. Each of these treatments was preceded by a treatment without the snakeskin, the first to provide a baseline, and the second, to test for vigilance and memory recall after exposure to the snakeskin. We found that (1) vervets needed only a small portion of snakeskin for detection, (2) snake scales alone were sufficient for detection, (3) latency to detect the snakeskin was longer with more extensive and complex ground cover, and (4) vervets that were exposed to the snakeskin remembered where they last saw “snakes”, as indicated by increased wariness near the occluding landmarks in the absence of the snakeskin and more rapid detection of the next presented snakeskin. Unexpectedly, adult males did not detect the snakeskin as well as adult females and juveniles. These findings extend our knowledge of the complex ecological and evolutionary relationships between snakes and primates.     

Are natural threats superior threats?

Threat superiority effects describe the reaction time advantage for locating threatening objects in a visual search paradigm, compared to locating visually similar non-threatening objects. They are widely reported for threats of both natural (snakes and spiders) and man-made (guns and knives) origins. Across two experiments, the current study contrasts threat superiority effects for natural and man-made targets. When targets are not depicted held, snakes and spiders tended to exhibit larger threat superiority effects, and were searched for with additional caution, than were guns and knives. When snakes and spiders were depicted held and weapons wielded, systematic differences between the natural and man-made threats disappeared. This means the advantage for threats of natural origin observed when all targets were depicted not held may be attributable to differences in animation – snakes and spiders are alive and may strike at any time if in your vicinity, whereas a weapon can only inflict harm if wielded. From these data there is no evidence that evolved visual sensitivities to the basic shapes of venomous animals support faster detection and response times to these animals than can occur to targets such as guns and knives, whose shapes must be learned. The selection pressures that led to the evolution of such sensitivities (observable even in infancy) may therefore lie in protecting young children and babies from envenomation, before they even have the cognitive capacity to understand the dangers that snakes and spiders pose.     

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.     

Snake Species Discrimination by Wild Bonnet Macaques (Macaca radiata)

Wild bonnet macaques (Macaca radiata) were studied in southern India to assess their ability to discriminate non‐venomous, venomous and predatory snakes. Realistic snake models were presented to eight troops of bonnet macaques at feeding stations and their behavior was video‐recorded 3 min before and 3 min after snake exposure. Snakes presented were: (1) venomous Indian cobra (Naja naja) displaying an open hood with ‘eyespots’; (2) venomous common Indian krait (Bungarus caeruleus); (3) non‐venomous green keelback (Macropisthodan plumbicolor); (4) non‐venomous rat snake (Ptyas mucosus); and (5) Indian python (Python molurus) which preys on macaques. Latencies to detect and react to the snakes were evaluated to determine initial responsiveness. Longer‐term assessment was measured as the percentage of time individuals looked at the snakes and monitored the activity of nearby individuals before and after snake detection. All snake models engendered caution and maintenance of a safe distance. Alarm calling occurred only during python presentations. The cobra engendered a startle response or running in the largest percentage of individuals after its detection, whereas the rat snake and python elicited bipedal standing or ambulating to monitor the snakes. We also examined the influence of age on snake recognition. Juveniles and subadults looked at the cobra, krait, and python for a larger percentage of time than adults did; albeit, adults looked at the python substantially longer than at the other snakes. Age differences in behavior suggest that, with the exception of the python, repeated experience with snakes in the wild moderates excitability, consistent with the likely threat of envenomation.     

Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

Probing,Assessment and Management during Interactions between Ground Squirrels (Rodentia: Sciuridae) and Rattlesnakes (Squamata: Viperidae). 2: Cues Afforded by Rattlesnake Rattling

The predator-prey relationship between California ground squirrels (Spermophilus beecheyi) and northern Pacific rattlesnakes (Crotalus riridis oreganus) is a useful system in which to explore risk assessment and management. Rattlesnakes are major predators of ground-squirrel pups, but pose only a sublethal threat to adult squirrels. Adults approach, harass, and even attack rattlesnakes when confronted with them. A rattlesnake's response to such harassment can include rattling and striking. Not all rattlesnakes pose the same risk to an adult squirrel. Larger, warmer rattlesnakes strike in ways that may be more effective at overwhelming the defensive leaps of squirrels, and larger snakes can inject more venom if they are successful in landing a bite. It would therefore benefit squirrels to assess and respond appropriately to rattlesnakes of different body size and temperature. We looked for cues in rattling upon which such assessments might be based. We recorded and digitally analyzed the rattling sounds of snakes of different sizes, each tested at four different body temperatures — 10, 18, 27, and 35°C. Results indicate that warmer snakes rattle with faster click rates, higher amplitudes, and shorter latencies. Similarly, larger snakes produce rattling sounds of higher amplitude and lower dominant frequencies. Thus, rattling provides reliable cues about rattlesnake dangerousness. Nevertheless, this highly ‘informative’ characteristic of rattling has its origins in physical and physiological constraints, not in specialization for communication. Ground squirrels appear to probe for the information extractable from rattling, for example by pushing loose substrate at the snake and thus inducing it to rattle. Future reports will discuss the degree to which ground squirrels actually exploit these cues.     

Snake-directed Behavior by Snake Naive and Experienced California Ground Squirrels in a Simulated Burrow

Snake naive and experienced California ground squirrels (Spermophilus beecheyi) were video taped while interacting with either a gopher snake or rattlesnake in a simulated burrow dimly illuminated with red light. Using nonvisually guided behavior, naive and experienced squirrels reacted to snakes in qualitatively similar ways, and behaved more defensively toward snakes than toward a control stimulus (white rat). The squirrels alternately interacted with the snake and attempted to escape from the burrow, which had a sealed entrance. Interaction with the snake included cautious approach in elongate postures, prolonged investigation of adjacent alleys before entering them, kicking sand at the snake, frequent tooth chattering, occasional calling, and building burrow plugs out of sand. These they packed by butting with their heads. When permitted to escape from the burrow, they turned just outside the entrance to tail flag, kick sand, scent mark, and finally plug the burrow. Since visual cues were not available, olfactory and auditory stimuli from the snake appeared to mediate snake-directed behavior in the burrow.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.     

Foraging Behavior in the Arboreal Boid Corallus grenadensis

Corallus grenadensis is an arboreal boa endemic to the Grenada Bank. Thirty-five encounters with boas resulted in 17.65 hours of observations, including 6.3 hours of video-tape (which included two acts of predation). Boas under 100 cm are largely active foragers that move slowly through bushes and trees and tongue-flick leaf and branch surfaces apparently seeking chemosensory evidence of nocturnally quiescent lizard (Anolis) prey. Significantly more search time was directed to branches below the snake rather than to either the branches supporting the snake or to those above the snake, and tongue-flick rates were significantly higher for moving snakes than for those that were stationary. Smaller snakes prey on nocturnally quiescent lizards and they spent more time moving than did large snakes that feed on nocturnally active rodents and often employ an ambush foraging strategy. Once visual and, presumably, thermal information was received from a sleeping anole, C. grenadensis adopted a lengthy stalking process devoid of tongue-flicks. Snakes approached inactive lizards from adjacent branches with great stealth, moving at a rate of about 1 cm/min. The strike was made from close range (within 3 cm), and the prey was never released once contact was made. We conclude that, if chemosensory cues successfully lead a treeboa to a visual encounter with a sleeping lizard, subsequent behavior ensures a high rate of predation success.     

Can Wall Lizards Combine Chemical and Visual Cues to Discriminate Predatory from Non‐Predatory Snakes Inside Refuges?

The ability to use multiple cues in assessing predation risk is especially important to prey animals exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds in the open by hiding inside rock crevices, where they may encounter saurophagous ambush smooth snakes. Lizards should avoid refuges with these snakes, but in refuges lizards can also find non‐saurophagous viperine snakes, which lizards do not need to avoid. We investigated in the laboratory whether wall lizards used different predator cues to detect and discriminate between snake species within refuges. We simulated predatory attacks in the open to lizards, and compared their refuge use, and the variation in the responses after a repeated attack, between predator‐free refuges and refuges containing visual, chemical, or visual and chemical cues of saurophagous or non‐saurophagous snakes. Time to enter a refuge was not influenced by potential risk inside the refuge. In contrast, in a successive second attack, lizards sought cover faster and tended to increase time spent hidden in the refuge. This suggests a case of predator facilitation because persistent predators in the open may force lizards to hide faster and for longer in hazardous refuges. However, after hiding, lizards spent less time in refuges with both chemical and visual cues of snakes, or with chemical cues alone, than in predator‐free refuges or in refuges with snake visual cues alone, but there were no differences in response to the two snake species. Therefore, lizards could be overestimating predation risk inside refuges. We discuss which selection pressures might explain this lack of discrimination of predatory from similar non‐predatory snakes.     

Search efficiency but not response interference affects visual selection in frontal eye field

Two manipulations of a visual search task were used to test the hypothesis that the discrimination of a target from distractors by visually responsive neurons in the frontal eye field (FEF) marks the outcome and conclusion of visual processing instead of saccade preparation. First, search efficiency was reduced by increasing the similarity of the distractors to the target. Second, response interference was introduced by infrequently changing the location of the target in the array. Both manipulations increased reaction time, but only the change in search efficiency affected the time needed to select the target by visually responsive neurons. This result indicates that visually responsive neurons in FEF form an explicit representation of the location of the target in the image.     

Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges

The threat sensitivity hypothesis assumes that multiple cues from a predator should contribute in an additive way to determine the degree of risk-sensitive behaviour. The ability to use multiple cues in assessing the current level of predation risk should be especially important to prey exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds or mammals by hiding inside rock crevices, where they may encounter another predator, the smooth snake, Coronella austriaca. We investigated in the laboratory whether chemical cues may be important to wall lizards for detection of snakes. The greater tongue-flick rate and shorter latency to first tongue-flick in response to predator scents indicated that lizards were able to detect the snakes' chemical cues. We also investigated the use of different predatory cues by lizards when detecting the presence of snakes within refuges. We simulated successive predator attacks and compared the propensity of lizards to enter the refuge and time spent within it for predator-free refuges, refuges containing either only visual or chemical cues of a snake, or a combination of these. The antipredatory response of lizards was greater when they were exposed to both visual and chemical cues than when only one cue was presented, supporting the threat sensitivity hypothesis. This ability may improve the accuracy of assessments of the current level of predation risk inside the refuge. It could be especially important in allowing lizards to cope with threats posed by two types of predators requiring conflicting prey defences.     

Predator-specific camouflage in chameleons

A crucial problem for most animals is how to deal with multiple types of predator, which differ in their sensory capabilities and methods of prey detection. For animals capable of rapid colour change, one potential strategy is to change their appearance in relation to the threat posed by different predators. Here, we show that the dwarf chameleon, Bradypodion taeniabronchum, exhibits different colour responses to two predators that differ in their visual capabilities. Using a model of animal colour perception to gain a 'predator's eye view', we show that chameleons showed better background colour matching in response to birds than snakes, yet they appear significantly more camouflaged to the snake visual system because snakes have poorer colour discrimination.     

Species specificity of methyl ketone profiles in the skin lipids of female garter snakes,genus Thamnophis

One of the relatively few vertebrate pheromones to be chemically identified, the female sex pheromone of the red-sided garter snake (Thamnophis sirtalis parietalis) is a series of saturated and monounsaturated methyl ketones contained within female skin lipids. During the breeding season, this pheromone is responsible for eliciting male courtship behaviors and males are able to utilize pheromonal variation to discriminate among females. While the pheromone system of the red-sided garter snake has been the subject of many studies, relatively little is known about the pheromone systems of other garter snakes. Through chemical analyses, we demonstrate that female skin lipids of the red-spotted garter snake (Thamnophis sirtalis concinnus), northwestern garter snake (Thamnophis ordinoides), and plains garter snake (Thamnophis radix) contain similar methyl ketones. The methyl ketone profiles of these snakes differ qualitatively from one another and from the methyl ketone profiles of red-sided garter snakes with differences particularly pronounced between sympatric species. Our results provide evidence that the use of methyl ketones in sexual signaling may be ubiquitous for Thamnophis species and suggest that these compounds could play a role in reproductive isolation between species in this genus.     

Organization of receptive fields of motion-senstitive neurons in the cat pulvinar

The distribution of 70 visually sensitive neurons in the cat pulvinar sensitive to motion in the receptive fields was studied. The experimental results showed that components with directional characteristics are present in the structure of these fields of both direction-selective and unselective neurons. In the receptive fields of direction-selective neurons the directional elements of the substructure have identical preferred directions, which coincide with the preferred directions of response to stimulus movement over the entire receptive field. The organization of receptive fields of direction-selective neurons of the visual association structure thus does not differ significantly from that of analogous fields of visual projection neurons. Directional elements of the receptive fields of direction-unselective neurons were found to have different preferred directions, thereby providing a basis for organization of the nondirectional response of the neuron to a stimulus moving across the entire receptive field.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 14, No. 4, pp. 339–346, July–August, 1982.     

Collapse of the endemic lizard Podarcis pityusensis on the island of Ibiza mediated by an invasive snake

The invasive snake Hemorrhois hippocrepis colonized the island of Ibiza (Balearic Islands) in 2003 as stowaways inside trunks of olive trees imported for gardening. It has quickly spread since 2010, posing a threat to the island’s only remaining endemic vertebrate, the Ibiza wall lizard Podarcis pityusensis. We map the yearly expansion rate of the snake and estimate via transect surveys how severely it affects the distribution and abundance of the endemic lizard. As well, we surveyed 9 of 30 small lizard populations on islets surrounding Ibiza that have been isolated since the Last Glacial Maximum. Snakes had invaded 49% of Ibiza’s land area by 2018, and censuses show a critical contrast in lizard abundance between areas with and without snakes; almost all censuses in areas without snakes show lizard presence whereas nearly all censuses in areas with H. hippocrepis lack lizard sightings. Moreover, at least one subspecies previously thriving on one of the offshore islets has become extinct, and there have been several snakes recorded swimming between Ibiza and the surrounding islets. Therefore, lizard populations have been dramatically reduced or have vanished within the range of the snake, and our results quantitatively support upgrading this species’ threat level for extinction. This study can inform to programs to manage invasive snake populations and to conservation actions to recover the endemic lizard.     

Auditory modulation of the inferior temporal cortex neurons in rhesus monkey

We performed a systematic study to check whether neurons in the area TE (the anterior part of inferotemporal cortex) in rhesus monkey, regarded as the last stage of the ventral visual pathway, could be modulated by auditory stimuli. Two fixating rhesus monkeys were presented with visual, auditory or combined audiovisual stimuli while neuronal responses were recorded. We have found that the visually sensitive neurons are also modulated by audiovisual stimuli. This modulation is manifested as the change of response rate. Our results have shown also that the visual neurons were responsive to the sole auditory stimuli. Therefore, the concept of inferotemporal cortex unimodality in information processing should be re-evaluated.