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.     

The biological function of snake mobbing by Siberian chipmunks: II. Functions beneficial for the mobbers themselves

The functions of snake mobbing by Siberian chipmunks were studied in the context of potencial benefit to the mobbers themselves. In experiment I, the threatening effect of the mobbing was examined, and following results were obtained. The snake retreated almost always into a shelter box when it was mobbed, and the time span from the beginning of the mobbing until the completion of the snake's retreat into the box was shorter when the snake was mobbed by 2 chipmunks than when mobbed by a single one. These results indicate that mobbing has a threatening effect against the snake that increases when more chipmunks mob. In experiment II, I examined whether chipmunks get information about the snake during the mobbing. The experiment showed that the chipmunks performed tail shakings after the mobbing more frequently at large snakes than at small ones, and also indicated that mobbing functions to obtain useful information about snakes. This study clarified that the snake mobbing by Siberian chipmunks provides benefits to the mobbers themselves.     

Allocare in a nocturnal primate: data on the spectral tarsier, Tarsius spectrum

Non-maternal infant care in many of the small-bodied New World primate species has been hypothesized by some researchers to be related to the high infant/adult weight ratio found in these species. The spectral tarsier, Tarsius spectrum, an Old World primate, has one of the highest infant/adult weight ratios of any primate, with infants weighing between 20-33% of adult weight at birth. On the basis of the hypothesized relationship between allocare and the infant/adult weight ratio, it is predicted that the spectral tarsier will also exhibit extensive allocaretaking behaviour. The results of this study indicate that although spectral tarsiers show care by male and female subadults as well as adult males, it is extremely limited compared to the extensive allocaretaking behavior observed in New World primate species such as Aotus and Callicebus. Spectral tarsier subadult females provide substantially more allocare to infants than do subadult males or adult males. Female subadults were observed sharing food, transporting, grooming, playing, alarm calling, baby-sitting and maintaining physical contact with infants more than other age/sex classes. Although the amount of allocare exhibited by adult males and subadult males was much less than that exhibited by female subadults, the data suggest that adult and subadult male spectral tarsiers do play a small part in the care and socialization of the infant. Adult males and subadult males were both observed occasionally engaging in allocaretaking behaviors such as grooming and playing, as well as frequently patrolling and defending the territory's boundaries. The results from this study suggest that although a high infant/adult weight ratio may be a prerequisite for selection to favor extensive allocare, it is not a causal factor. Additional research is needed in order to understand better the selective pressures involved and the costs and benefits of providing allocare to subadults and adult male spectral tarsiers.     

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.     

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.     

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.     

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.     

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).     

Is mobbing altruistic or selfish behaviour?

The hypotheses that try to explain mobbing behaviour can be divided into three main classes: altruistic behaviour, parental care and selfish behaviour. To try to distinguish between these hypotheses, I presented 12 Arabian babblers,Turdoides squamiceps , with a snake model, both alone and together with another babbler. Seven components of mobbing were compared in the two situations. Single babblers that were exposed to a snake model carried out mobbing-like behaviour. Mobbing in the absence of an audience or additional participants shows that it is basically a selfish behaviour, and suggests that it is an antipredator behaviour. No difference was found between males and females, and mobbing by two participants together was more intensive than mobbing by each of them on its own. These findings support the prey-predator communication hypothesis. However, the different hypotheses explaining mobbing are not exclusive, and this study does not exclude other hypotheses as secondary explanations. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

Condition explains individual variation in mobbing behavior

During mobbing, individuals approach predators with the apparent aim of reducing the risk of predation. The intensity of mobbing may depend on the costs and benefits of this behavior, which likely vary among individuals and between different social contexts. We studied whether Dark‐eyed junco male mobbing behavior is related to social environment, individual condition, and age during experimentally induced mobbing events. Based on risk‐taking theory, we predicted that individuals with high residual reproductive value—younger individuals and those in better condition—would show weaker mobbing behavior. We also expected to see weaker mobbing when the total number of individuals in the mobbing assemblage was small. All subjects were caught to assess condition and age. Focal males were then attracted to simulated mobbing events using heterospecific alarm calls. Social environment did not explain individual variation in mobbing behavior in focal juncos. Community‐wise, the relationship between the closest approach and group size was not significantly different from chance. Junco males in better condition approached the predator less closely and were less likely to give alarm calls. Age did not explain variation in mobbing. Both the mean approach and probability of giving alarm calls by junco males were repeatable, in contrast to the size and composition of mobbing assemblages in junco territories, which were inconsistent. Our results show that variation in mobbing can be linked to individual state, which likely affects the costs and benefits of mobbing.     

Sociality in the spectral tarsier, Tarsius spectrum

Recent studies indicate that many of the nocturnal prosimian primates are gregarious rather than solitary. This paper shows that the spectral tarsier is gregarious during its nightly activity period as well as in its sleeping tree. Using mist nets and radiotelemetry, focal follows were conducted on six groups at Tangkoko Nature Reserve in Sulawesi, Indonesia. During 442 focal follows, 1072 encounters between a focal adult group member and another adult were observed. The number of encounters ranged from as few as 0 to as many as 18 encounters per night. Intragroup encounters lasted from less than 1 min to as long as 3 hr 12 min. Nearly one-half of all social behavior occurred between adult females and males. There were also substantial rates of social interaction between the two adult females in one group, and between sub-adults of the opposite sex in neighboring groups.     

Associations between adult spectral tarsiers

While anecdotal observations of gregarious behavior in nocturnal prosimian primates are common, most anthropologists continue to refer to them as solitary, perhaps based on the assumption that the occasional social interactions observed via ad libitum methods represent random chance encounters and not patterned social interactions. In this paper, I test the null hypothesis that nocturnal encounters between spectral tarsier (Tarsius spectrum) group members, outside of the sleeping tree, are the result of chance. Three male‐female pairs were radio‐collared and observed over a 4‐month period, using continuous focal animal sampling at the Tangkoko Nature Reserve (Sulawesi, Indonesia). Using Waser's random gas model, I found that spectral tarsiers spent more time in proximity to other group members than expected by chance, given the size of their home range and nightly path length. Adult group members spent 11% of the night in physical contact and an additional 17% of the night within a 10‐m radius of one another. Spectral tarsiers were also observed to significantly increase the amount of time spent foraging when located less than 10 m from another group member. Individuals foraging in proximity to another adult group member had lower insect capture rates compared to individuals who were not foraging in proximity to another adult group member. If living in a group is costly to these tarsiers' foraging efficiency, then why don't they actively avoid one another when foraging? One situation in which it might benefit tarsiers to be gregarious is high predation pressure. Preliminary results suggest that predation pressure by snakes may be the most likely factor selecting for the tarsiers to forage in proximity. Am J Phys Anthropol 128:74‐83, 2005. © 2005 Wiley‐Liss, Inc.     

The emerging phylogenetic pattern of parthenogenesis in snakes

Parthenogenesis occurs across a variety of vertebrate taxa. Within squamate reptiles (lizards and snakes), a group for which the largest number of cases has been documented, both obligate and facultative types of parthenogenesis exists, although the obligate form in snakes appears to be restricted to a single basal species of blind snake, Indotyphlops braminus. By contrast, a number of snake species that otherwise reproduce sexually have been found capable of facultative parthenogenesis. Because the original documentation of this phenomenon was restricted to subjects held in captivity and isolated from males, facultative parthenogenesis was attributed as a captive syndrome. However, its recent discovery in nature shifts the paradigm and identifies this form of reproduction as a potentially important feature of vertebrate evolution. In light of the growing number of documented cases of parthenogenesis, it is now possible to review the phylogenetic distribution in snakes and thus identify subtle variations and commonalities that may exist through the characterization of its emerging properties. Based on our findings, we propose partitioning facultative parthenogenesis in snakes into two categories, type A and type B, based on the sex of the progeny produced, their viability, sex chromosome morphology, and ploidy, as well as their phylogenetic position. Furthermore, we introduce a hypothesis (directionality of heterogamety hypothesis) to explain the production of female‐only parthenogens in basal alethinophidian snakes and male‐only parthenogens in caenophidian (advanced) snakes.     

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.     

Laughing Falcon (Herpetotheres cachinnans) Predation on Coral Snakes (Micrurus nigrocinctus)1

Laughing falcon (Herpetotheres cachinnans) predation on coral snakes (Micrurus nigrocinctus) was recorded in two incidents that illustrate previously unreported variation in predatory behavior. In the first, the falcon held a live coral snake by the posterior end for an extended period of time, rather than decapitating it immediately. In the second, the falcon left a decapitated coral snake in a tree for more than 2 h before returning to recover its prey. A variety of behavioral adaptations may protect laughing falcons from coral snake venom.     

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.     

Hormonal independence of courtship behavior in the male garter snake

Garter snakes exhibit a dissociated reproductive tactic in which gonadal activity is minimal at the time of mating, increasing only after the breeding season has ended. Experiments are presented demonstrating that neither short-term nor longterm castration affects courtship behavior in adult male red-sided garter snakes (Thamnophis sirtalis parietalis). So long as males have passed through a low-temperature dormancy period (hibernation), castration either shortly after emergence in the spring, or before entering winter dormancy in the fall, does not prevent the display of intense courtship behavior on emergence. Similarly, males castrated during mating activity the previous spring prior to the annual testicular growth phase actively courted females on emergence from hibernation. Males adrenalectomized and castrated during low-temperature dormancy also courted females on emergence. Hypophysectomy during or before low-temperature dormancy did not prevent males from displaying high-intensity courtship behavior on emergence from hibernation. Treatment with sex steroid hormones, as well as hypothalamic and pituitary hormones, and a variety of neural and metabolic affectors also fails to elicit courtship behavior in noncourting males during the summer. It was concluded that causal mechanisms controlling courtship behavior in the red-sided garter snake are fundamentally different, at least at the physiological level, from those mechanisms described for many laboratory and domesticated species.     

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.     

Predation by grass snakes (Natrix natrix) at a site in southern England

The prey and feeding frequency in free-living grass snakes was studied during 1993 and 1994 at a site in southern England. Individual snakes and common toads were recognized using PIT tags and a small number of adult snakes were radio-tracked over long periods to determine predation rates.
Grass snakes fed, almost exclusively, on common toads (adult, juvenile, and tadpoles). A positive correlation was found between prey size and snake size. Large snakes did not appear to prey upon small toads, although clearly capable of doing so.
Male and female snakes ate large meals (toads) approximately every 20 days between May and September, with females fasting for a period of about 45 days during gestation and egg-laying. After allowing for differences in the number and size of toads predated by male and female snakes, the mean amount of food consumed per day was estimated to be 2.3% and 1.6% of body weight.