Selective signalling by cuttlefish to predators

Rather than simply escaping, prey animals often attempt to deter an attack by signalling to an approaching predator, but this is a risky strategy if it allows time for the predator to draw closer (especially when the signal is a bluff). Because prey are vulnerable to multiple predators, the hunting techniques of which vary widely, it could well be beneficial for a prey animal to discriminate predators and to signal only to those that are likely to be deterred. Higher vertebrates make alarm calls that can identify the type of predator to the signaller's conspecifics, and a recent study shows that squirrels direct an infrared deterrent signal specifically at infrared-sensitive pit-vipers and not at other snakes. We show here that na?ve juvenile cuttlefish (Sepia officinalis L.) use a visual signal selectively during encounters with different predatory species. We analysed sequences of defensive behaviours produced by cuttlefish, to control for effects of relative threat level (or 'response urgency'). This showed that a high contrast 'eyespot' signal, known as the deimatic display, was used before flight against visually oriented teleost fish, but not crabs and dogfish, which are chemosensory predators.     

Managing predators: The influence of kangaroo rat antipredator displays on sidewinder rattlesnake hunting behavior

Upon sensing predators in their vicinity, many prey species perform antipredator displays that are thought to provide information to the predator that deters it from attacking (predator‐deterrent signals). These displays can be complex, incorporating a variety of signaling elements as well as direct physical harassment of the predator. Although the display behaviors in these communication systems are often well characterized, evidence of the efficacy of these displays in deterring predators is limited due to the challenges associated with studying free‐ranging predators. Here, we examine how the anti‐snake signals of the desert kangaroo rat (Dipodomys deserti) influence the ambush hunting behaviors of sidewinder rattlesnakes (Crotalus cerastes). We found that, although desert kangaroo rats incorporate a number of signal elements into their antipredator display, only sand kicking behavior was a significant factor in motivating sidewinder rattlesnakes to cease hunting: high rates of sand kicking led to early abandonment of ambush coils. These results indicate that anti‐snake displays of small mammals may be especially effective at mitigating the threat posed by rattlesnakes when those displays incorporate physical harassment as well as signaling.     

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.     

Feeding Experience Modifies the Assessment of Ambush Sites by the Timber Rattlesnake, a Sit-and-Wait Predator

To effectively ambush prey, sit‐and‐wait predators must locate sites where profitable prey are likely to return. One means by which predators evaluate potential ambush sites is by recognizing high‐use areas through chemical cues deposited inadvertently by their prey. However, it is unknown whether ambush predators can use chemical cues associated with past prey items in the assessment of potential ambush sites. I examined selection of ambush sites by timber rattlesnakes (Crotalus horridus) exposed to trails made from chemical extracts of the integument of various prey species. I evaluated the role of feeding experience in ambush site selection by comparing the behavior of timber rattlesnakes before and after feeding experience with different sized prey items. Timber rattlesnakes are more likely to select ambush sites adjacent to chemical trails from prey with which they have had feeding experience, but only those fed relatively large prey showed an increase in responsiveness. Increased responsiveness after feeding experience was exhibited in experiments using integumentary extracts of mammals (the natural prey of timber rattlesnakes), but not in those using extracts of fish. These results indicate that ambush predators may learn to recognize chemicals on the integument of profitable food items, and use that experience when subsequently selecting ambush sites. Additionally, these findings provide evidence that size‐dependent predation by snakes may be, in some species, a result of active prey selection.     

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.     

Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

Prey‐driven behavioral habitat use in a low‐energy ambush predator

Food acquisition is an important modulator of animal behavior and habitat selection that can affect fitness. Optimal foraging theory predicts that predators should select habitat patches to maximize their foraging success and net energy gain, likely achieved by targeting areas with high prey availability. However, it is debated whether prey availability drives fine‐scale habitat selection for predators. We assessed whether an ambush predator, the timber rattlesnake (Crotalus horridus), exhibits optimal foraging site selection based on the spatial distribution and availability of prey. We used passive infrared camera trap detections of potential small mammal prey (Peromyscus spp., Tamias striatus, and Sciurus spp.) to generate variables of prey availability across the study area and used whether a snake was observed in a foraging location or not to model optimal foraging in timber rattlesnakes. Our models of small mammal spatial distributions broadly predicted that prey availability was greatest in mature deciduous forests, but T. striatus and Sciurus spp. exhibited greater spatial heterogeneity compared with Peromyscus spp. We found the spatial distribution of cumulative small mammal encounters (i.e., overall prey availability), rather than the distribution of any one species, to be highly predictive of snake foraging. Timber rattlesnakes appear to forage where the probability of encountering prey is greatest. Our study provides evidence for fine‐scale optimal foraging in a low‐energy, ambush predator and offers new insights into drivers of snake foraging and habitat selection.     

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.     

Anti-Predator Signals as Advertisements: Evidence in White-Throated Magpie-Jays

Calls and displays elicited by predators usually function as alarms or to inform predators of their detection. However, predator encounters may afford some individuals the opportunity to demonstrate quality or signal their availability. Here, I report on a class of vocal signals produced in predator-elicited displays that share many characteristics with sexually selected song. White-throated magpie-jays ( Calocitta formosa ) display at low-threat predators while producing 'loud display calls' (LDCs). I use this term because the calls occur primarily in two display contexts (see below) though occasionally in other contexts as well. Such calls and displays are primarily produced by males, and also occur in one other context, at dawn. Playback experiments showed that despite being elicited by predators, males were more likely than females to respond to LDCs, and more likely to respond when their mate was fertile. Over 134 different call types were produced in over 200 displays by 34 males; the largest minimum repertoire size was 67. Presentations of taxidermic raptor mounts elicited some LDCs, but fewer calls and lower diversity than at dawn or in predator approach displays. The male bias and high diversity suggest that LDCs are an outcome of intersexual selection, while their elicitation by predators suggests an alarm function. I propose that male magpie-jays use predator encounters as opportunities to advertise their presence and availability as mates; they use LDCs as songs. Such a communication system seems to have been favored by the unusual social system of magpie-jays, in which female groups defend territories and males have little opportunity to defend resources for mate attraction, forcing them to advertise when females are paying the most attention, during predator encounters.     

Anti‐Predator Signals in the Chaffinch Fringilla coelebs in Response to Habitat Structure and Different Predator Types

Many animals respond to the presence of predators with conspicuous signals such as alarm calling. These signals may aid the detection of the predator by conspecifics or may deter the predator from attack. The advantages of such signals may be dependent upon predator type and habitat type. We measured signalling behaviours (alarm calling and tail flicking) in foraging chaffinches in response to different predator models (hawk and pigeon control, cat and plastic box as control). In addition we measured responses to a cat model when chaffinches were foraging in different habitat structures (obstructed vs. open). There was no difference in the number of individual chaffinches alarm calling in obstructed vs. open habitat, but birds tail flicked more in open habitat, suggesting that tail flicking acts as a visual signal to the predator or conspecifics and therefore unlike auditory cues is influenced by habitat structure. Chaffinches were also more likely to tail flick in response to the cat model than the other three models. Our results are consistent with the idea that animals may respond to ground predators, which spend a large amount of time observing prey before attack, by using signalling behaviours, such as tail flicking and alarm calling. Further work on prey selection by predators is needed to separate the functions of signalling behaviour in response to predators.     

Once Bitten,Twice Shy: Does Previous Experience Influence Behavioural Decisions of Snakes in Encounters with Predators?

Injuries are common in animals of diverse taxa and are usually attributed to encounters with predators. Although often non‐lethal, injuries nevertheless represent effects of predators that can have negative consequences for demography and fitness (e.g. reproductive costs). However, encounters with predators also represent experience through which animals can learn and positively adapt their future behaviour, potentially mitigating, at least partly, the negative effects of prior exposure to predators. I predicted that injured grass snakes (Natrix natrix), which presumably had been handled previously by a predator, would be more likely to move before capture than uninjured snakes. This prediction was borne out. Snakes with injuries also had lower body condition than uninjured snakes, although the effect was non‐significant. Snakes that had been previously captured also were significantly more likely to move before capture than snakes that had never been caught before. These results provide strong evidence for the role of experience and learning in modifying the antipredator behaviour of snakes.     

Antipredator behaviour and predator recognition in Belding's ground squirrels

This study evaluates whether Belding's ground squirrels (Spermophilus beldingi) recognize predators under natural conditions. I observed these squirrels for 300 h during two consecutive summers, during which I described 1029 aerial and terrestrial interactions, including 299 interactions with animals known to prey on squirrels. Squirrels responded differentially to predators and non-predators, to predators that hunt differently, and to contextually different interactions with the same predator. Responses shown in encounters with predators included Trill and Chirp vocalizing, upright Posting, crouching, running to burrow entrances, entering burrows, Approaching or chasing predators, and doubling-back on pursuing predators. Ground squirrels appear to adjust their antipredator behaviour depending on the amount and kind of danger they face during an encounter.     

Fossils and phylogeny uncover the evolutionary history of a unique antipredator behaviour

Recently, two squirrel species (Spermophilus spp.) were discovered to anoint their bodies with rattlesnake scent as a means of concealing their odour from these chemosensory predators. In this study, we tested multiple species with predator scents (rattlesnake and weasel) to determine the prevalence of scent application across the squirrel phylogeny. We reconstructed the evolutionary history of the behaviour using a phylogenetic analysis and fossil records of historic predator co‐occurrence. Squirrels with historical and current rattlesnake co‐occurrence all applied rattlesnake scent, whereas no relationship existed between weasel scent application and either weasel or rattlesnake co‐occurrence. This was surprising because experimental tests confirmed rattlesnake and weasel scent were both effective at masking prey odour from hunting rattlesnakes (the primary predator of squirrels). Ancestral reconstructions and fossil data suggest predator scent application in squirrels is ancient in origin, arising before co‐occurrences with rattlesnakes or weasels in response to some other, now extinct, chemosensory predator.     

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.     

Size-dependent predation by snakes: selective foraging or differential prey vulnerability?

I staged replicate encounters between unrestrained lizards andsnakes in outdoor enclosures to examine size-dependent predationwithin the common garden skink (Lampropholis guichenoti). Yellow-facedwhip snakes (Demansia psammophis) forage widely for activeprey and most often consumed large skinks, whereas death adders(Acanthophis antarcticus) ambush active prey and most oftenconsumed small skinks. Small-eyed snakes (Rhinoplocephalusnigrescens) forage widely for inactive prey and consumed bothsmall and large skinks equally often. Differential predationmay reflect active choice by the predator, differential preyvulnerability, or both. To test for active choice, I presentedforaging snakes with an inert small lizard versus an inertlarge lizard. They did not actively select lizards of a particularbody size. To test for differential prey vulnerability, I quantifiedvariation between small and large lizards in behavior thatis important for determining the outcome of predator—prey interactions. Snakes did not differentiate between integumentarychemicals from small and large lizards. Large lizards tendto flee from approaching predators, thereby eliciting attackby the visually oriented whip snakes. Small lizards were moremobile than large lizards and therefore more likely to passby sedentary death adders. Additionally, small skinks were more effectively lured by this sit-and-wait species and less likelyto avoid its first capture attempt. In contrast, overnightretreat site selection (not body size) determined a lizard'schances of being detected by small-eyed snakes. Patterns ofsize-dependent predation by elapid snakes may arise not becauseof active choice but as a function of species-specific predatortactics and prey behavior.     

Do ‘Quiet’ Places Make Animals Placid? Island vs. Mainland Tiger Snakes

Most animals that possess potent venom display a wide variety of warning messages to discourage predators. Tiger snakes are large and highly venomous elapids that exhibit these anti‐predator behaviours. We compared the anti‐predator behaviours of two neighbouring and genetically indistinguishable populations in Western Australia (Herdsman Lake, HL and Carnac Island, CI). CI is free from human, native and feral predation. All of these factors represent a continual threat on HL situated on the mainland. Neither body size, nor sex influenced defensive behaviours. However, we observed a marked inter‐population difference among adults in the degree to which anti‐predator behaviours were displayed when snakes were continually aggravated: HL snakes exhibited a typical warning signal (flat‐neck) and bite, while CI snakes remained very docile. In stark contrast, neonates of both populations exhibited marked anti‐predator behaviours and both populations were indistinguishable in terms of the intensity of display. Neonates reared in captivity, hence regularly confronted by human predators, became more defensive in comparison with neonates exposed to natural conditions on CI; similarly several adult CI snakes kept in captivity became more defensive. Our results highlight the extreme behavioural plasticity of snakes. We also hypothesize that CI snakes may become more placid over time as they grow up in an environment free from predation.     

Nest predation in forest birds: influence of predator type and predator's habitat quality

We used the introduction of a generalist nest predator, the red squirrel Tamiasciurus hudsonicus, and of a large herbivore, the Sitka black-tailed deer Odocoileus hemionus sitkensis, to the islands of Haida Gwaii (Queen Charlotte Islands, British Columbia, Canada) to study how predator assemblage and habitat quality and structure influenced nest predation in forest birds. We compared losses of natural nests to predators on islands with and without squirrels. We selected nine islands with or without squirrel or deer and used 506 artificial nests put on the ground or in shrubs to further analyse variation of nest predation with predator assemblage and habitat quality for the predators. For both natural and artificial nests predation risk was higher in presence of squirrels. But predation risk varied within island categories. In presence of squirrels it was highest in stands with mature conifers where it fluctuated from year to year, in response to fluctuations in squirrel abundance. Vegetation cover around the nest had little effect on nest predation by squirrels. Where squirrels were absent, nest predation concentrated near predictable food sources for corvids, the main native predators, and increased with decreasing vegetation cover, suggesting that removal of the vegetation by deer increased the risk of predation by native avian nest predators that use visual cues. Predation risk in these forests therefore varies in space and time with predator composition and with quality of the habitat from the predators' perspective. This temporal and spatial variation in predation risk should promote trade-offs in the response of birds to nest predation, rather than fine-tuned adaptations to a given predation pattern.     

Stone banging by wild capuchin monkeys: an unusual auditory display

Primates often react to possible predators by using intimidation displays, although the occurrence of these displays is dependent on the risk of predation. Functional explanations for these kinds of displays range from sexual selection to predator deterrence. The ability to respond to different predators can be socially acquired, and social traditions could explain population differences in response to the same potential predator. Here I report wild groups of Cebus apella libidinosus banging stones to produce sound in a remarkable aggressive display. I observed this display in 6 wild groups and I suggest its primary function is a predator-deterrent behaviour. Although banging objects is an innate behaviour in capuchin monkeys, in all wild groups observed so far it has been observed only in a foraging context. Stone banging is a novel behavioural variant that is most likely learned socially. The absence of this display in other populations of capuchins, which have access to stones, suggests that stone banging could be a social tradition in the population studied.     

The impact of predation on burrow use by arctic ground squirrels in the boreal forest

In sedentary animals, the choice of a suitable home site is critical to survival and reproductive fitness. However, habitat suitability may vary with predation risk. We compared habitat use of Arctic ground squirrels (Spermophilus parryii plesius) living in the boreal forest under conditions of fluctuating predation pressure. In our study area, predators show ten-year cycles in numbers that track that of their primary prey, the snowshoe hare (Lepus americanus). In 1993, we compared burrows that continued to be occupied following the period of intense predation during the hare decline of 1990-1992 with those that became vacant, and with random locations. We contrasted these sites to those in a predator exclosure where predation pressure was minimized. Burrows on control sites were located on sloped sites with high visibility. Burrows that remained occupied during the period of intense predation were more likely to be in open areas with fewer fallen trees than burrows that became vacant. We used discriminant functions derived from the control sites and found that 89% of the burrows on the predator exclosure were classified as being similar to the random locations on control sites. We conclude that the distribution of Arctic ground squirrels in the boreal forest is a direct function of predator presence.     

Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis,Viperidae)

• 1.Do thermal factors influence foraging-site selection by ectothermic predators? Snake species that obtain their prey from ambush must remain immobile for long periods, precluding overt behavioural thermoregulation; and some “ambush” snakes use thermal cues to detect endothermic prey. Plausibly, alternative ambush sites might differ either in equilibrial body temperatures available to snakes, or in the thermal “background” against which prey items must be detected.
• 2.We examined this topic with field data on pit-vipers (Gloydius shedaoensis) on a small island in northeastern China. Adult snakes feed only on migrating passerine birds. The snakes ambush birds both from arboreal perches (branches of small trees) and from the ground.
• 3.Arboreal versus terrestrial ambush sites differed both in operative temperatures and thermal “backgrounds” available to the snakes. Operative temperatures inside copper models were lower in trees than on the ground (because of wind), and snakes in arboreal ambush sites were cooler than those in terrestrial sites. Thermal backgrounds from arboreal perches were cooler (and thus, provided more contrast against prey items) than did backgrounds available from terrestrial ambush-sites.
• 4.Thermal factors thus modify the suitability of alternative ambush locations for these pit-vipers, but with a trade-off: a snake in a tree can “see” its prey more clearly, but may not be warm enough (and hence, able to strike fast enough) to capture it. Further work is required to determine whether or not snakes actually use such thermal differences as criteria for the selection of ambush sites.