The biological function of snake mobbing by Siberian chipmunks: I. Does it function as a signal to other conspecifics?

The signal effect of mobbing of snakes (a signal effect alerts conspecifics of the presence of a predator) by Siberian chipmunkEutamias sibiricus asiaticus was examined. A pair of chipmunks, familiar with each other, were moved from their rearing pen into a test box, where they were kept undisturbed for acclimatization. Then the anterior portion (or head) of an anesthetized Japanese rat snake was exposed in a corner of the box. Several minutes later, one of the chipmunks discovered the snake and began mobbing it. This was followed by the discovery of the snake by the other chipmunk. Although the time span from the introduction of the snake to its discovery by the first chipmunk was quite different between trials, the time elasped from the snake discovery by the first chipmunk to that by the other chipmunk was relatively constant and significantly shorter than the former time span in all trials. These results strongly support the premise that the mobbing has a signal effect.     

An Analysis of Snake-Scent Application Behaviour in Siberian Chipmunks (Eutamias sibiricus asiaticus)

Some rodents assault live snakes by mobbing. Another snake-directed behaviour is shown by Siberian chipmunks, Eutamias sibiricus asiaticus, when encountering a dead snake. They approach the carcass cautiously, gnaw the snake skin, and chew and apply the gnawed bits to their body fur. We have termed this behaviour “Snake-Scent Application” (SSA). SSA behaviour is also elicited by snake urine and feces. Chemicals in snake skin and rectal and cloacal sacs release SSA. Snake urine applied to dead mice tends to suppress ingestion by snakes.     

Function of snake mobbing in spectral tarsiers

Numerous species are known for their tendency to approach and confront their predators as a group. This behavior is known as mobbing. Snakes seem to be one of the more consistent recipients of this type of predator-directed behavior. This paper explores individual differences (sex and age) in the mobbing behavior of the spectral tarsier toward live and model snakes. This study was conducted at Tangkoko Nature Reserve (Sulawesi, Indonesia) during 2003-2004. During this research, 11 natural mobbing events and 31 artificially induced mobbing events were observed. The mean number of individuals at a mobbing was 5.7. The duration of mobbing events was strongly correlated with the number of assembled mobbers. Adults were more likely than other age classes to participate in mobbings. Males were more likely than females to participate in mobbings. Mobbing groups often contained more than one adult male, despite the fact that no spectral tarsier group contains more than one adult male. No difference in body size between extragroup males and resident males was observed, refuting the "attract the mightier" hypothesis. The number of mobbers did not affect whether the tarsier or the snake retreated first, countering the "move-on" hypothesis. The "perception advertisement" hypothesis was tentatively supported, in that live snakes were rarely seen in the area following mobbing calls, in comparison to when tarsiers either ignored the snake or alarm call.     

Mobbing calls signal predator category in a kin group-living bird species

Many prey species gather together to approach and harass their predators despite the associated risks. While mobbing, prey usually utter calls and previous experiments have demonstrated that mobbing calls can convey information about risk to conspecifics. However, the risk posed by predators also differs between predator categories. The ability to communicate predator category would be adaptive because it would allow other mobbers to adjust their risk taking. I tested this idea in Siberian jays Perisoreus infaustus, a group-living bird species, by exposing jay groups to mounts of three hawk and three owl species of varying risks. Groups immediately approached to mob the mount and uttered up to 14 different call types. Jays gave more calls when mobbing a more dangerous predator and when in the presence of kin. Five call types were predator-category-specific and jays uttered two hawk-specific and three owl-specific call types. Thus, this is one of the first studies to demonstrate that mobbing calls can simultaneously encode information about both predator category and the risk posed by a predator. Since antipredator calls of Siberian jays are known to specifically aim at reducing the risk to relatives, kin-based sociality could be an important factor in facilitating the evolution of predator-category-specific mobbing calls.     

Exposure affects the risk of an owl being mobbed – experimental evidence

Mobbing is a widespread anti-predator strategy in birds, and predators are generally expected to avoid mobbing. For example, observational studies suggest that the cryptic roosting behaviour of nocturnal predators, such as many owls, may be a strategy to limit mobbing. In this paper, we present the results of the first experimental study investigating to what degree roost exposure influences the risk of being mobbed, and the intensity of a mobbing incidence once initiated. To determine these factors, we used an experimental setup with taxidermic mounts of tawny owls Strix aluco in Grib Skov forest, Denmark. The risk of an owl being mobbed during a 50 min morning survey period increased with the exposure of its roosting position, from 24% when hidden to 85% when openly exposed. The corresponding increase in the afternoon was from 6% to 36%. This suggests that an owl may minimize the mobbing rate by reducing the encounter rate with potential mobbers through its choice of roost. Once initiated, the duration of the mobbing (a proxy for the presumed cost of being mobbed) was independent of the roosting position of the mounted owl, but was positively correlated with the number of birds in the mob.     

Barn swallow mobbing: Self-defence,collateral kin defence,group defence,or parental care?

We presented stimuli (human and stuffed owl) to a marked population of barn swallows (Hirundo rustica) during the 1980–1982 breeding seasons at the Cranberry Lake Biological Station, Saint Lawrence County, New York. In experiment 1, we presented the stimuli at various distances from active nests during various stages of the reproductive cycle. Both the probability and intensity of mobbing varied during the breeding season, increasing with the probable reproductive value of young of the year and the degree of danger posed to them. Mobbing group sizes varied positively with local nest densities. In experiment 2, we analysed mobbing group structure in greater detail. Barn swallow mobbing groups usually contained active mobbers (those that emitted mobbing calls, and approached the stimulus closely, < 2 m, or even hit it) and passive mobbers (which were silent and flew in circles at greater distances, 2–10 m, from the stimulus). Passive mobbers were a random sample of the local population with respect to sex, age, nest location and reproductive status. This pattern is consistent with a hypothesis that passive mobbing, the less risky type, is a form of self-defence that reduces an actor's chance of being eaten, probably by providing information about the identity or probable behaviour of potential predators. Active mobbers were not a random sample of the source population. Mated birds and especially parents with nestlings were over-represented, while non-breeders, juveniles and incubators rarely mobbed actively. The seasonal changes in mobbing and the identity of active and passive mobbers are inconsistent with hypotheses that mobbing is a form of cooperative group defence or altruism conditioned by reciprocity or kin or group selection. These data are however consistent with other hypotheses, which propose that mobbing benefits the mate or the young. Even though active mobbers may be at risk, they benefit directly by increasing the personal component of their inclusive fitness, probably by alerting mates and young and defending them from predators. In this light the behavioural complex of mobbing appears to be a form of parental care (active) as well as self-defence (passive) and mate defence (active).     

Exposure affects the risk of an owl being mobbed – experimental evidence

Mobbing is a widespread anti‐predator strategy in birds, and predators are generally expected to avoid mobbing. For example, observational studies suggest that the cryptic roosting behaviour of nocturnal predators, such as many owls, may be a strategy to limit mobbing. In this paper, we present the results of the first experimental study investigating to what degree roost exposure influences the risk of being mobbed, and the intensity of a mobbing incidence once initiated. To determine these factors, we used an experimental setup with taxidermic mounts of tawny owls Strix aluco in Grib Skov forest, Denmark. The risk of an owl being mobbed during a 50 min morning survey period increased with the exposure of its roosting position, from 24% when hidden to 85% when openly exposed. The corresponding increase in the afternoon was from 6% to 36%. This suggests that an owl may minimize the mobbing rate by reducing the encounter rate with potential mobbers through its choice of roost. Once initiated, the duration of the mobbing (a proxy for the presumed cost of being mobbed) was independent of the roosting position of the mounted owl, but was positively correlated with the number of birds in the mob.     

Effects of avian mobbing on roost use and diet of powerful owls,Ninox strenua

We observed the species and numbers of mobbing birds and their effects on a large, nocturnal, bird-eating predator, the powerful owl, together with the pattern of owl predation on mobbing and non-mobbing species. Owls were mobbed on 35 occasions by seven of 44 species of forest birds at a site composed of open forest (88% by area) and rainforest (12%). The majority of bouts involved individuals of a single species, although mixed groups were observed on nine occasions. Regular mobbers were between 4 and 26% of the owls’ body weight. Owls abandoned their daytime roosts during 20% of bouts and responded by calling or actively monitoring mobbers during 54% of bouts. Mobbing appeared to explain why owls roosted in rainforest significantly more often than expected by its availability, mobbing being significantly less frequent in rainforest than in open forest. Only one mobbing species regularly occupied rainforest and the canopy of roosts in rainforest was denser than that in open forest, thus reducing the chances of an owl being detected by potential mobbers. Twelve species of forest birds were within the range of prey size of the powerful owl (75–800 g): six were mobbers and six non-mobbers. The frequency of owl predation on non-mobbers was 8.75 times that on mobbers. The species in this study took a high risk by mobbing a very large predator, but benefited by greatly reducing their chances of predation.     

Mutualism,reciprocity, or kin selection? Cooperative rescue of a conspecific from a boa in a nocturnal solitary forager the gray mouse lemur

Predator mobbing is a widespread phenomenon in many taxa but the evolution of cooperative mobbing as an adaptive behavior is still subject to debate. Here, we report evidence for cooperative predator defense in a nocturnal solitarily foraging primate, the gray mouse lemur (Microcebus murinus). Several mouse lemurs mobbed a snake that held a non-related male conspecific until he could escape. Evolutionary hypotheses to explain cooperative mobbing include (1) by-product mutualism, when individuals defend others in the process of defending themselves; (2) reciprocity, where animals achieve a higher fitness when helping each other than when they do not cooperate; and (3) kin selection where animals help each other only if they share genes by common descent. Owing to the solitary activity of this species, reciprocity seems to be least likely to explain our observations. By-product mutualism cannot be ruled out entirely but, if costs of snake mobbing are relatively low, the available detailed socio-genetic information indicates that kin selection, rather than any of the other proposed mechanisms, is the primary evolutionary force behind the observed cooperative rescue.     

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.     

Group Mobbing Behaviour and Nest Defence in a Cooperatively Breeding Australian Bird

Cooperatively breeding noisy miners (Manorina melanocephala) are well known in Australia for their persistent and very vocal group mobbing of heterospecifics. Here I investigated the nature of this extraordinary behaviour, in particular its role in nest defence, in a colour banded population of noisy miners in south‐east Queensland, Australia. I focused on two questions. First, did the intensity of mobbing vary according to factors such as the threat to the nest, or the ‘value’ of a clutch? Secondly, what role did group mobbing play in the success of a nest? To answer these questions, I experimentally manipulated the nest defence behaviour by placing one of three stuffed models near active noisy miner nests. The response of noisy miners to intruders was not indiscriminate. However, I found that the number of birds that mobbed a model did not simply reflect the potential threat posed. The response of noisy miners to raptors and other potential nest predators may have reflected their rarity as well as the threat posed. The number of mobbers did not vary with the age or size of a brood. In this study, the fate of nests was independent of the number of mobbers or visitors at nests. Finally, up to 80% of mobbers were never seen to make any other type of contribution to a nest, and many could not be related to the brood that they were ‘defending’. Hence, for some noisy miner ‘helpers’ the benefits that they accrued were probably not wholly dependent on the survival of the broods. I suggest that, in this gregarious species, mobbing behaviour at the nest may be a display of social status or individual quality. This hypothesis warrants further investigation.     

Diurnal exposure as a risk sensitive behaviour in tawny owls Strix aluco?

Tawny owls Strix aluco generally roost in cryptic locations during the day. To test the hypothesis that this cryptic behaviour is an effort to avoid mobbers or avian predators, we measured diurnal behaviour and cause-specific mortality of radio-tagged birds. Non-breeding adults (assumed to be well fed individuals, optimising their own survival) roosted in less exposed locations than adults with young and newly independent juveniles. Parents roosted in the most exposed sites when their young were immature and vulnerable to depredation, probably to guard offspring. Newly independent juveniles apparently selected roosting sites in exposed places to get access to food, as this behaviour was associated with lower perching heights and higher prey abundance beneath their roosting sites. They also perched in more exposed sites, closer to the ground, in summers with low prey abundance compared to summers with high prey abundance. After previous encounters with goshawks Accipiter gentilis , dependent juveniles roosted in less exposed places compared to other young. The increased risk of being mobbed was highly significant with increasing roosting exposure. Once an owl was mobbed, the intensity of the mobbing correlated positively with the mass of the mobbers, but mobbing birds never killed any owls. In contrast, diurnal raptors caused 73% of natural owl deaths (n=15) and the depredation rate by raptors was 3.8 times higher in population classes that generally roosted in more exposed locations than did non-breeding adults. We therefore suggest that depredation by diurnal raptors is the main factor shaping the diurnal behaviour of tawny owls.     

Predator Mobbing in <Emphasis Type="Italic">Tarsius spectrum</Emphasis>

Whereas most animals make considerable effort to avoid their predators, numerous species tend to approach and to confront predators as a group: mobbing. Among the types of predators that elicit mobbing, snakes seem to be one of the more consistent recipients of it. I describe the mobbing behavior of spectral tarsiers toward live and model snakes. In particular, I explore individual differences—sex, age and reproductive status—in mobbing behavior at Tangkoko Nature Reserve, Sulawesi, Indonesia. In 1994–1995, I observed 11 groups for 18 mo, and in 1999, I observed 9 groups for 6 mo. Over all I recorded, 11 natural mobbing events and 9 artificially induced mobbing events. The mean number of individuals at a natural mobbing is 5.1 with an average duration of 33 min. The duration of a mobbing event is strongly correlated with the number of mobbers. Adults were more likely than other age classes to participate in mobbings. Males were more likely than females to participate in mobbings. Mobbing groups often contained > 1 adult male despite the fact that no spectral tarsier group contains > 1 adult male. Vis-à-vis Curios (1978) 9 hypotheses for the function of mobbing suggests that its primary function in spectral tarsiers may be perception advertisement or teaching snakes to move on.     

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.     

Effect of mobbing toward predators by the damselfishPomacentrus coelestis (Pisces: Pomacentridae)

Field observations on prey-predator interactions, focusing on mobbing behavior byPomacentrus coelestis, were made in the shallow water of Shirahama, Japan. Within the breeding colony of the damselfish, indirect group mobbing toward 6 ambushers and direct mobbing with physical contact only by nesting males toward a stalker were observed. The direct mobbing toward the stalker (moray eel) is suggested to have involved an element of egg-guarding. Group mobbing was usually released by large and quick attacking motion of the predator. Attack intervals of a predator were much longer after it was mobbed than when it was not mobbed, but there was no significant difference in success ratio of the next attack whether mobbing was elicited or not. Consequently, it is concluded that mobbing effectively reduced future predation risk of each mobber.     

The number of Great Tit mobbers influences the mobbing response of heterospecific birds

Many species mob predators to drive them away. Mobbing carries personal risk, but the risk of injury or death declines and the likelihood of repelling the predator increases in larger groups. The capacity to evaluate the number of mobbers before joining a mobbing group may be highly beneficial for individuals when deciding to join. Although recent studies have found that birds can use individual vocal discrimination to assess the number of conspecifics involved in initiating mobbing events, it is little known whether birds are able to evaluate the number of heterospecific mobbers. In this study, we investigated whether the number of heterospecifics responding to mobbing calls of Great Tits Parus major was influenced by the number of callers (a mix of Great Tit callers simulated by playbacks and live Great Tits attracted to playbacks, range one to seven callers). The total number of responding heterospecific individuals and species was positively influenced by the total number of callers, with heterospecifics responding more to larger than smaller Great Tit groups. However, these results may be driven by the total number of calls, call overlap and increased noise generated by the additional mobbers, and not the number per se. These findings therefore allow us to assess whether birds are more inclined to join a mobbing group when it consists of more heterospecific callers, but we cannot tell whether birds use individual vocal discrimination to assess the number of heterospecific callers.     

Behavioral responses to conspecific mobbing calls are predator‐specific in great tits (Parus major)

When facing a predator, animals need to perform an appropriate antipredator behavior such as escaping or mobbing to prevent predation. Many bird species exhibit distinct mobbing behaviors and vocalizations once a predator has been detected. In some species, mobbing calls transmit information about predator type, size, and threat, which can be assessed by conspecifics. We recently found that great tits (Parus major) produce longer D calls with more elements and longer intervals between elements when confronted with a sparrowhawk, a high‐threat predator, in comparison to calls produced in front of a less‐threatening tawny owl. In the present study, we conducted a playback experiment to investigate if these differences in mobbing calls elicit different behavioral responses in adult great tits. We found tits to have a longer latency time and to keep a greater distance to the speaker when sparrowhawk mobbing calls were broadcast. This suggests that tits are capable of decoding information about predator threat in conspecific mobbing calls. We further found a tendency for males to approach faster and closer than females, which indicates that males are willing to take higher risks in a mobbing context than females.     

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.     

Can Auditory Playback Condition Predator Mobbing in Captive-reared <Emphasis Type="Italic">Saguinus oedipus</Emphasis>?

Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus oedipus) did not differentiate between a snake and a rat, confirming previous research that naïve cotton-top tamarins do not fear snakes. Tamarins then viewed a living snake during playback of mobbing calls. In posttests, tamarins did not mob the snake. We then eliminated the pretest to avoid potential habituation and placed a stillborn tamarin with the snake in an attempt to heighten arousal. In posttests, tamarins again did not mob the snake, although they did increase their rates of calls, indicating mild arousal. Overall, none of 8 groups of cotton-top tamarins learned to mob a predator. Potential reasons for failure include conditioning multiple subjects at once and the lack of an experienced demonstrator. Observing a demonstrator was not necessary for birds to acquire mobbing, but may be necessary for tamarins.     

Behavioral Responses of Siberian Chipmunks toward Conspecifics Applied Snake Scent

Siberian chipmunks are known to gnaw snake-related objects such as skin, urine, feces and anal sac excretion, and apply the gnawed bits to their body fur repeatedly (SSA behavior). After SSA, chipmunks often rub their bodies on nearby wood stumps and branches. The SSA behavior is surmised to have function of information-spreading on snakes to neighboring chipmunks. In the present study, responses of the other chipmunks towards SSA individuals were experimentally analyzed to examine the possibility of this hypothesis. In the experiments, subject chipmunks were presented with 2 kinds of objects; (1) SSA-performed chipmunks in boxes and non-performed chipmunks in boxes, (2) wood boards to which the scent of SSA-performed chipmunks adhered and wood boards to which the scent of non-performed chipmunks adhered. In both cases of (1) and (2), subject chipmunks nosed significantly longer the scent from SSA-performed chipmunks and that they performed SSA only in the contact with the former.