Rattlesnakes Create a Context for Localizing Their Search for Potential Prey

This paper presents systematically collected field data on what transpires between free-living rattlesnakes (Crotalus viridis oreganus) and individuals of an important prey species, California ground squirrels (Spermophilus beecheyi). In the course of two field seasons we discovered that rattlesnakes and California ground squirrels can engage in at least six different episode classes: snake watching, snake following, inspecting/probing coiled snakes, interaction, rattlesnake approaching squirrel and envenomation. If a rattlesnake is moving directly toward a squirrel and is within 3 m of its burrow an interaction may develop, but more commonly it does not. Instead of engaging the snake, the squirrels seemed to try to remain stationary in the face of the snake's advance, as if to minimize affording the snake information about the nursery burrow location. The rattlesnakes in turn behaved as though they were using the location of the squirrels that resisted moving away from their advance as the hub of a radial search pattern. We argue that if the squirrel engages the snake before it discovers the burrow, the location of the nursery burrow may be revealed and the pups' vulnerability actually increased.     

Parental defence on the reef: antipredator tactics of coral‐reef fishes against egg‐eating seasnakes

On coral reefs in New Caledonia, the eggs of demersal‐spawning fishes are consumed by turtle‐headed seasnakes (Emydocephalus annulatus). Fish repel nest‐raiding snakes by a series of tactics. We recorded 232 cases (involving 22 fish species) of antipredator behaviour towards snakes on a reef near Noumea. Blennies and gobies focused their attacks on snakes entering their nests, whereas damselfish (Pomacentridae) attacked passing snakes, as well as nest‐raiders (reflecting territorial defence). Biting the snake was the most common form of attack, although damselfish and blennies also slapped snakes with the tail, or (blennies only) plugged the nest entrance with the parent fish's body. Gobies rarely defended the nest, although they sometimes bit or threw sand at the snake. A snake was more likely to flee if it was attacked before it began feeding rather than after it found the eggs (82% versus 3% repelled) and if bitten on the head rather than the body (68% versus 53%). Tail‐slaps were not effective, although plugging the burrow and throwing sand often caused snakes to flee. These strong patterns reflect phylogenetic variation in fish behaviour (e.g. damselfish detect a snake approach sooner than do substrate‐dwelling blennies and gobies) coupled with intraspecific variation in snake diets. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 415–425.     

Vocal and Escape Responses of Columbian Ground Squirrels to Simulated Terrestrial and Aerial Predator Attacks

Most ground-dwelling sciurids emit nonrepetitive and repetitive calls in response to predators. In this study, I simulated terrestrial (badger Taxidea taxus) and aerial (flying disc) predator attacks to elicit escape and vocal responses in Columbian ground squirrels (Spermophilus columbianus). In response to the badger, ground squirrels often ran, but rarely to a burrow, and were most likely to give nonrepetitive calls before running or without running; rarely did they enter burrows. Ground squirrels in direct line of the flying disc (i.e., “target” squirrels under “attack”), ran to, and into, the nearest escape burrow and rarely gave a nonrepetitive call. Squirrels distant from the flying disc often called, usually while running or after assuming an upright posture at the nearest burrow. These results suggest that ground squirrels incur little cost when calling in response to aerial predators. Nonrepetitive and repetitive calling in response to the badger and flying disc did not differ significantly among age-sex classes; however, parous females were more likely than nonparous females to give both types of calls in response to the badger. Nonparous females either with or without close nondescendant kin rarely called in response to the badger. Thus, there was no indication that females exposed to the badger behaved nepotistically toward close kin other than their juvenile offspring. Nonrepetitive calling in response to the badger apparently functions primarily to warn vulnerable offspring and, hence, is a component of maternal investment. Although the occurrence of antipredator calling in response to the flying disc did not vary significantly among parity-kin classes, there was evidence that adult and yearling females were more likely to emit repetitive, and to a lesser extent, nonrepetitive calls, if close nondescendant kin were in the colony. I conclude that indirect fitness benefits, that is, kin selection, probably contributes to the maintenance of antipredator calling in response to aerial predators.     

Probing,Assessment, and Management during Interactions between Ground Squirrels and Rattlesnakes

The predator-prey relationship between California ground squirrels (Spermophilus beecheyi) and northern Pacific rattlesnakes (Crotalus viridis) is a useful system for exploring conflict and assessment. Rattlesnakes are major predators of ground squirrel pups, but pose a less significant threat to adult squirrels. Adults approach, harass, and even attack rattlesnakes in defense of their pups. Two factors that may influence risk to both squirrel and snake during encounters are the size and body temperature of the rattlesnake. We used high-speed video to analyze the strikes of rattlesnakes of various sizes tested at different body temperatures. Results indicate that warmer snakes are more dangerous because they strike with higher velocity, greater accuracy, and less hesitation. Similarly, larger snakes are more dangerous because they can strike farther and at higher speeds, and keep their fangs embedded longer. Thus, ground squirrels would benefit from extracting information about a rattlesnake's size and temperature. The converse of our results is that cooler, smaller rattlesnakes may be more vulnerable. These snakes could mitigate their risk by avoiding dangerous adversaries and minimizing cues that divulge their weaknesses. Such tactics might explain the active probing that squirrels direct at rattlesnakes, which may function to overcome a snake's resistance to disclosing its vulnerability.     

Olfactory Snake‐Predator Discrimination in the Cape Ground Squirrel

Small mammals have a number of means to detect and avoid predators, including visual, auditory and olfactory cues. Olfactory cues are particularly important for nocturnal or fossorial species where visual cues would not be as reliable. The Cape ground squirrel (Xerus inauris) is a semi‐fossorial, diurnal mammal from southern Africa. Cape ground squirrels encounter multiple species of predatory snake that pursue individuals underground where visual and social cues are limited. We assessed whether Cape ground squirrels use odours to discriminate between snakes by presenting a non‐venomous snake, a venomous snake and a control odour collected on polyethylene cubes to 11 adult female squirrels from 11 different social groups. Cape ground squirrels responded by inspecting the cube, displaying snake harassment–associated behaviours and decreasing time spent in close proximity to snake odours when compared with a control. They also displayed discrimination between two snake species by increasing the frequency of cube inspection and increasing harassment behaviours with venomous snake odours when compared with non‐venomous snake odours. We conclude that Cape ground squirrels respond with snake‐specific antipredator behaviours when presented olfactory cues alone. Olfactory discrimination may be maintained by the decreased utility of other methods of predator detection: sight and group detection, in below‐ground encounters.     

When seasnake meets seabird: Ecosystem engineering,facilitation and competition

Ecosystem engineers such as burrowing seabirds can increase habitat availability for sympatric taxa – but only if the burrow's owner allows other species to use the newly created shelter site. Our studies on a small Pacific island suggest that an avian burrower (the wedge‐tailed shearwater Puffinus pacificus) is both a facilitator and a competitor for amphibious seasnakes. Video camera inspection of 102 burrows revealed frequent usage of these burrows as retreat sites by the snakes, with Laticauda laticaudata restricted to burrows <4 m from the water's edge, whereas Laticauda saintgironsi often used burrows further inland. Snakes never occupied burrows that contained adult shearwaters, suggesting active burrow defence by the birds. Model snakes that we inserted into burrows were attacked, especially on the head and upper body, and we found one snake pecked to death outside a burrow. Wedge‐tailed shearwaters act as facilitators, creating a thermally favourable microhabitat and substantially enhancing habitat suitability for snakes; but they are also competitors, aggressively competing with snakes for occupancy of the resource that has been created.     

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 Black-tailed Prairie Dogs (Cynomys ludovicianus)

When exposed to an anesthetized snake, feral black-tailed prairie dogs living in a high-snake-density area approached ambivalently and investigated the snake, typically near the head. Snake-investigation was interrupted intermittently, when the prairie dog jumped away, foot thumped or jump yipped, and approached the snake again. This behavior attracted other prairie dogs, who behaved similarly. Message analyses of two apparent signaling acts — foot thumping and jump yipping — demonstrated that they convey information that withdrawal from the snake has become less likely, and continued interaction with the snake more likely. Prairie dogs in a zoo and feral prairie dogs in a low-snake-density area were unresponsive to immobile snakes, but reacted strongly when the snake was permitted to move. We compared these results to similar data on California ground squirrels and discussed the selection pressures, and ontogenetic and perceptual processes that may have acted as determinants of this snake-directed behavior.     

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.     

Observations and description of a rare escape mechanism in a snake: Cartwheeling in Pseudorabdion longiceps (Cantor, 1847) (Squamata,Colubridea)

We report an observation of cartwheeling behavior to escape predators employed by the Dwarf Reed Snake (Pseudorabdion longiceps). This rolling motion is a rare escape mechanism which has not been formally documented in detail for any other species of snake or reptile. This finding also extends our knowledge on the kinetic abilities in snakes. Abstract in Malay is available with online material.     

Age-dependent use of local and global landmarks during escape: experiments using Columbian ground squirrels

How animals utilize their space often changes during ontogeny, perhaps resulting from alternative use of orientation mechanisms. This study investigated whether landmark-based navigation mechanisms were age-dependent in Columbian ground squirrels (Spermophilus columbianus). In field tests, young (1-2 years old) and adult (3-6 years old) animals had to find an escape burrow when either local, global, or both types of landmarks were obstructed. The comparison of escape times between age groups revealed that adult squirrels found escape burrow faster than young animals if global landmarks were available. However, if only local landmarks were present, young squirrels outperformed older animals. The comparison of escape time within each age group showed that obstruction of global or local landmarks lengthened escape time of adult squirrels. In contrast, young animals had longer escapes only when local landmarks were obstructed. The results suggested that the use of different types of landmarks was age specific.     

Does the Siberian chipmunk respond to the snake by identifying it?

Siberian chipmunks were presented with snakes and 4 control animals (tortoises, frogs, eels, quails) in a large outdoor pen to examine whether the snakedirected behavior of the chipmunk is a response to identifying the snake or simply an exploratory behavior toward generally strange objects. The animals were presented to chipmunks in 3 manners; tethered, anesthetized, and in perforated opaque boxes and in wire netting boxes. In “tethered” and “anesthetized”, chipmunks responded significantly more intensively to snakes than to other animals. When the animals were presented in the boxes, that is, when chipmunks could perceive only olfactory stimulus from the animals, they also showed the strongest response to snakes. The results suggest that 1) snake-directed behavior of chipmunks is not a general exploratory response toward strange objects but a response to identifying the snakes, and that 2) olfaction is an important cue for the chipmunks to identify snakes.     

Chemosensory Response of Desert Iguanas (Dipsosaurus dorsalis) to Skin Lipids from A Lizard-Eating Snake (Lampropeltis getula californiae)

Several species of lizards respond to chemicals from sympatric lizard‐eating snakes with increased tongue‐extrusion rates. These substances also elicit antipredator behavior indicating that they have important ecological functions and the resulting behavior can have serious implications for individual fitness of lizards. However, the source and type of snake chemical cues that elicit these behavioral changes in lizards have yet to be determined. We tested the ability of adult desert iguanas (Dipsosaurus dorsalis) to detect and identify a potential predator by exposing them to lipids extracted from shed snakeskins. Lipids were extracted from cast skins of a known lizard‐eating snake, the California kingsnake (Lampropeltis getula californiae), using chloroform and methanol. Test subjects were presented with skin lipids as well as clean, pungent, and chloroform controls on cotton‐tipped applicators in random order. Desert iguanas directed significantly more tongue extrusions toward applicators bearing snakeskin lipids when compared with controls. In addition, overall tongue‐extrusion frequency increased following exposure to lipids during the 5‐min trials. Desert iguanas clearly detected snakeskin lipids, but this stimulus failed to elicit changes in body posture and movement patterns previously observed in experiments using chemical cues from live snakes. Increased tongue flicking by lizards in response to snakeskin lipids may represent a generalized response to this class of chemicals. Additional potential sources of chemicals used in the detection of lizard‐eating snakes are discussed.     

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.     

Cooperative hunting in Brown-Necked Raven (Corvus rufficollis) on Egyptian Mastigure (Uromastyx aegyptius)

We describe cooperative hunting by Brown-necked Raven (Corvus ruficollis) on Egyptian Mastigure (Uromastyx aegyptius) in the Arava Valley, Israel. At first, in all nine observed hunts, the ravens were observed to be in the vicinity and were seen simultaneously. The Mastigure was almost always at a distance from the burrow entrance and either foraging on the bushes or lying flattened on a bush sunning itself. The attack started when a circling pair of ravens flew in at high speed and landed on the entrance of the burrow, cutting off the escape route of the lizard. Following this maneuver, the other ravens attacked the lizard. The ravens pecked randomly at the most exposed part of the lizard, eventually causing its death. Only when the lizard was evidently dead did the two individuals that blocked the escape route join in the feeding ravens.     

Post-bite Elevation in Tongue-flick Rate by Neonatal Garter Snakes (Thamnophis radix)

A post-biting elevation in tongue-flicking rate was demonstrated experimentally in neonatal, ingestively naive garter snakes (Thamnophis radix). That the snakes also exhibited apparent searching movements suggests that strike-induced chemosensory searching occurs in nonvenomous snakes lacking previous experience with food or prey chemicals. Two litters of neonates differed in numbers of tongue-flicks emitted, but had similar relative magnitudes of response across experimental conditions. The existence of post-bite elevation in tongue-flick rate (and presumably strike-induced chemosensory searching) argues for a genetic basis for these chemosensory behaviors in a nonvenomous species of snake, extending the recent finding that strike-induced chemosensory searching is fully developed in ingestively naive neonatal rattlesnakes. Possible patterns of evolution of post-bite elevation in tongue-flick rate, and the strike-release-trail strategy of highly venomous snakes are discussed.     

Division of Labour and Extended Parenting in a Desert Tenebrionid Beetle

Parastizopus armaticeps (Peringuey) is a nocturnal detritivorous desert tenebrionid beetle which can only reproduce after heavy rainfall. Both parents care for the young and excavate a breeding burrow together. They play similar roles in burrow excavation and protection until the eggs hatch, after which male and female roles diverge markedly Females collect detritus on the surface at night, depositing this at the burrow entrance, which they also clear of sand in the early evening. Males remain inside the burrow and dig to deepen and extend it, maintaining its moisture level as the sand desiccates They also pull the food dropped by the female down to the burrow base to form a food store for the offspring. Both sexes guard the burrow and attack same-sex intruders, especially in the early phases of reproduction. The parents remain inside with the pupal cocoons until the teneral adults eclose. Males dig continually to maintain burrow humidity while females, which rarely forage during the pupal Period, recommence foraging for a further 16-18d after pupal eclosure. They provide food for the newly eclosed beetles until the exoskeletons have hardened and melanization is almost complete, then the family disperses. Offspring over 10 d old pull down forage at the burrow entrance and later forage for food themselves and carry it to the burrow. This is the highest level of social and reproductive complexity described for beetles and the behavioural and ecological factors contributing to its evolution are discussed in the context of parental care known for other subsocial arthropods, especially coleopterans.     

Phylogeny of snake trypanosomes inferred by SSU rDNA sequences, their possible transmission by phlebotomines, and taxonomic appraisal by molecular, cross-infection and morphological analysis

Blood examination by microhaematocrit and haemoculture of 459 snakes belonging to 37 species revealed 2.4% trypanosome prevalence in species of Viperidae (Crotalus durissus and Bothrops jararaca) and Colubridae (Pseudoboa nigra). Trypanosome cultures from C. durissus and P. nigra were behaviourally and morphologically indistinguishable. In addition, the growth and morphological features of a trypanosome from the sand fly Viannamyia tuberculata were similar to those of snake isolates. Cross-infection experiments revealed a lack of host restriction, as snakes of 3 species were infected with the trypanosome from C. durissus. Phylogeny based on ribosomal sequences revealed that snake trypanosomes clustered together with the sand fly trypanosome, forming a new phylogenetic lineage within Trypanosoma closest to a clade of lizard trypanosomes transmitted by sand flies. The clade of trypanosomes from snakes and lizards suggests an association between the evolutionary histories of these trypanosomes and their squamate hosts. Moreover, data strongly indicated that these trypanosomes are transmitted by sand flies. The flaws of the current taxonomy of snake trypanosomes are discussed, and the need for molecular parameters to be adopted is emphasized. To our knowledge, this is the first molecular phylogenetic study of snake trypanosomes.     

Effects of Prey Movement and Prey Odor on Feeding in Garter Snakes

The role of prey movement in feeding behavior was investigated in 10 garter snakes (Thamnophis sirtalis) repeatedly presented with paired stationary and continuously rotating sections of earthworm (Lumbricus terrestris). Additionally, prey odor intensity and source were varied and the performance of a tongueless snake was compared to normal animals. Experiment 1 showed that garter snakes will selectively attack rotating over nonmoving sections of earthworm across a wide range of speeds (1–2048 rpm) with an optimum between 16 and 256 rpm. However, blocking the odor from the sections and presentation of speeds greater than 500 rpm decreased response to moving sections. Experiment 2 showed that at 22–32 rpm moving sections were selected over stationary sections when odor from both was blocked. Experiment 3 assessed the effects of varying ambient odor conditions upon selection of artificial moving and stationary prey. Ambient earthworm odor resulted in a sustained high rate of tongue-flicking while, with no odor present, snakes showed a gradually increasing rate of tongue-flicking that declined within a few minutes. Experiments 4 and 5 studied the effects of tongue removal upon the selection of moving and nonmoving prey. Gross changes in the feeding sequence were noted. A long-term tongue-less adult fed by opening her mouth and thrashing about her cage when presented with earthworm odor and only preferred moving prey at 32 rpm; a control showed the normal stalk-and-strike sequence. The tongueless snake was less attracted to the moving earthworm at a distance than were normal snakes and the use of vision seemed less integrated rather than compensably improved. The results are discussed in reference to the critical flicker-fusion frequency, klepto-parasitism, and escape tactics of prey.     

To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs

Risk-sensitive hatching is adaptive for species facing a trade-off between egg-stage and post-hatching risks, and environmental variation in one or both stages. Such plasticity has been found in amphibians, fishes, reptiles and spiders, with red-eyed treefrogs (Agalychnis callidryas) being the best-studied case. We assessed hatching plasticity and egg- and larval-stage risks in a closely related, syntopic species, the gliding leaf-frog (Agalychnis spurrelli). We found a lower hatching response to egg-eating snakes in A. spurrelli (9–28% of embryos escaped) than in A. callidryas (59–80% escaped). Levels of snake predation were similarly high for clutches of both species monitored at a pond in Costa Rica, and in fish predation experiments early-hatched A. spurrelli tadpoles were more vulnerable than later hatchlings, as has been shown for A. callidryas. A. spurrelli thus face a risk trade-off similar to A. callidryas, and likely would benefit from predator-induced hatching; their lower responsiveness to snakes appears nonadaptive. A. spurrelli embryos showed a stronger hatching response (57% hatched in 1 h) to submergence underwater than to snake attacks even though submergence is a less frequent risk. This suggests they have a greater capacity for early hatching than is expressed in the context of snake attacks, but have much lower sensitivity to snake cues than to flooding cues. Development in A. spurrelli is accelerated compared to syntopic A. callidryas, and spontaneous hatching is earlier and more synchronous. This is congruent with predictions based on selection by egg predators in the absence of a strong escape hatching response.