Inter-specific variation in anti-predator behavior in sympatric species of kangaroo rat

Kangaroo rats, Dipodomys, occupy desert habitats with little cover and thus are under high predation risk from diverse predators. The behavior used to assess predation risk or to escape capture is unknown. We therefore compared anti-predator behavior of two sympatric species of kangaroo rat of different sizes, D. merriami and D. spectabilis. We first examined whether kangaroo rats use olfaction as a first line of defense against snake predation and tested the rats for their responses to scent extracted from two species of snake that live sympatrically with the kangaroo rats, the Mojave rattlesnake (Crotalus scutulatus) and the gopher snake (Pitophis melanoleucus). We also tested for species differences in anti-predator behavior through 15-min interactions between the kangaroo rats and free-moving gopher snakes. We found that D. spectabilis actively approached the scent of both rattlesnakes and gopher snakes more than controls of vegetable oil and evaporated solvent (Fig. 1). In contrast, D. merriami did not differentiate snake odors from controls in the experimental arena, but they sniffed the sand where a free-moving snake had passed more than D. spectabilis. Both species successfully avoided predation in encounters with live snakes. Although total numbers of approaches and withdrawals were similar (Fig. 2), D. spectabilis spent significantly more time within striking distance of the snake than D. merriami. D. spectabilis approached the head of the snake in 93% of its approaches and often engaged in nose to snout contact with the snake. If the snake struck, D. spectabilis jumped directly backward to avoid a strike and footdrummed at a safe distance. In contrast, D. merriami oriented to the snake more than D. spectabilis, but approached the head in only 41% of the approaches and rarely engaged in nose-to-snout contact. The snakes struck, hissed and decreased predatory approaches with D. spectabilis but not with D. merriami (Fig. 3). These results show that kangaroo rats can behaviorally influence the risk of being preyed on by snakes. The two species differ, however, in how they react to snakes. The larger D. spectabilis confronts snakes while the smaller D. merriami monitors snakes from a safe distance and avoids them.     

Territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis): footdrumming and visual threats

Summary Footdrumming and visual displays associated with territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis) were studied in the field in Arizona. We predicted that foot-drumming functioned like bird song in territorial advertisement. Rats were tested in their territories for their responses to the presentation of four different stimuli: a playback of airborne footdrumming patterns (audio); a stuffed and mounted kangaroo rat in an aggressive posture (visual); a combination of both (audio-visual); and a playback of cricket stridulation as a control. Kangaroo rats investigated all experimental stimuli equally by becoming alert, approaching, and retreating (Fig. 2). Rats, therefore, seemed to assess the amount of threat and footdrummed at higher rates and sooner in response to the more threatening visual stumulus of a stuffed rat than to the apparently less threatening ones of a airborne footdrumming playback or cricket stridulation (Fig. 1). We conclude that rats footdrum at long ranges to repel a potential intruder and also at close ranges when territories are threatened by a persistent intruder. Chase and attack, as in territorial birds, are the final lines of defense.     

Territorial defense and advertisement by footdrumming in bannertail kangaroo rats (Dipodomys spectabilis) at high and low population densities

Summary Behaviors associated with territorial defense of large dirt mounds by bannertail kangaroo rats (Dipodomys spectabilis) at high and low population densities are reported. Rats were observed for 640 h during three summers and one spring from 1980–1982 in SE Arizona.Bannertail kangaroo rats defended their territories by footdrumming, as a long-distance warning signal, and chasing as a closer-distance threat. They footdrummed on or near their mounds spontaneosly during the night, in response to neighbors' footdrums, and durint mound challenges. There were no sexual differences in footdrumming, and juveniles frequently performed the behavior. The low frequency sounds were within the auditory sensitivities of the rats and footdrumming patterns differed somewhat between individuals. A playback experiment provided preliminary evidence that rats can differentiate between the footdrums of neighbors and strangers. When a bannertail visited the mound of another bannertail the mound owner actively defended its mound and immediately chased the visitor away. Fighting and mound challenges occurred infrequently, and the uniformly dispersed distribution of mounds suggested an effort by rats to avoid mutual interference.When population densities were high, dispersing juveniles built new mounds, consequently, distances between mounds decreased. Rats responded by tolerating closer neighbors, spending more time active on their mounds, and visiting neighboring mounds less. Adults increased footdrumming rates at high population densities, but juveniles footdrummed at high rates regardless of the population size.     

Antipredator behavior of a social desert rodent: footdrumming and alarm calling in the great gerbil, Rhombomys opiums

We sought to understand why a social, desert rodent, the great gerbil, Rhombomys opimus, expends energy and possible risk of predation by footdrumming and vocalizing in the presence of a diversity of terrestrial predators: snakes, monitor lizards, polecats, foxes, and humans. Behavioral observations, human approaches, and experiments with tethered predators revealed that both male and female gerbils called and footdrummed in the presence of offspring, close relatives, and potential mates. Because adults called more often when pups were present, and solitary gerbils seldom gave an alarm, the alarm behavior probably warns conspecifics, especially vulnerable offspring, of potential danger. We also found that gerbils altered alarm behavior with the type of predator. They drummed more in the burrow when a dog that could not enter the burrow was present, and they drummed more out of the burrow in response to a snake that could enter the burrow. Gerbils vocalized and stood in an alert posture in response to all stimuli. The different footdrumming responses of gerbils to terrestrial predators seems related to the hunting style and type of risk posed by the predator, especially its ability to enter the burrow system. Received: 23 August 1999 / Received in revised form: 6 December 1999 / Accepted: 25 February 2000     

Use of different signaling modalities to communicate status by dominant and subordinate Heermann’s kangaroo rats (<Emphasis Type="Italic">Dipodomys heermanni</Emphasis>)

Dominance relationships in solitary species may be an important factor in the maintenance of long-term, stable relationships among territorial neighbors. We examined the mediation of intraspecific interactions in a solitary, territorial kangaroo rat, Dipodomys heermanni, and tested whether unfamiliar kangaroo rats establish a dominance hierarchy and then decrease aggression and increase communication (via footdrumming and sandbathing) after initial interactions and the establishment of a social structure. Results revealed that both dominance hierarchies and familiarization with particular individuals are likely to mediate social interactions. After only one pairing per dyad, an almost linear dominance hierarchy emerged, which became perfectly linear after a 90-min familiarization period. During the course of subsequent interactions between dyad partners, fighting decreased and non-agonistic communication increased. Dominant kangaroo rats sandbathed at higher rates than subordinates, possibly to deposit scent to advertise competitive ability, whereas subordinate kangaroo rats footdrummed from inside the burrow, which seemed to indicate an unwillingness to interact. We suggest the kangaroo rats use a conditional strategy when deciding to fight (be dominant) or withdraw (be subordinate) by employing different modes to communicate status and minimize the potential risk of injury during unnecessarily prolonged fights.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

Group-living in cliff swallows as an advantage in avoiding predators

Summary Cliff swallows (Hirundo pyrrhonota) in SW Nebraska, USA, nest in colonies and associate in groups away from their colonies. The degree to which group-living in this species affords advantages in the avoiding of predators was examined. The distance from the colony at which a snake predator was detected increased with colony size. In flocks away from the colonies, group vigilance increased, but the time that each individual spent vigilant decreased, with flock size. As a result, birds in large flocks had more time for preening and mud-gathering. Cliff swallows did not effectively mob predators and thus were unable to deter predators regardless of group size. Nesting within each colony was highly synchronous, but when the effects of ectoparasites on nesting success were removed, individuals nesting during the peak breeding period were no more successful than those nesting before or after the peak. This suggests that swamping of predators is unlikely in cliff swallow colonies. Nests at the edges of colonies were more likely to be preyed upon than nests nearer the center, suggesting that colonial nesting conferred some selfish herd benefits. Overall reproductive success did not vary with colony size. While cliff swallows receive some anti-predator benefits by living in groups, the avoidance of predators is probably not a major selective force for the evolution of coloniality in this species.     

Background level of risk determines the intensity of predator neophobia in juvenile convict cichlids

Behavioural ecology is rife with examples of prey animals that are able to adjust the intensity of their anti-predator response to match background risk levels. Often, preys need experience with predators before they will invest in costly anti-predator responses. This means that prey animals often fail to respond to predators during their first encounter. Recently, we have shown that prey raised under high-risk conditions may exhibit avoidance of potential predation cues independent of experience (neophobia). Such phenotypically plastic neophobic predator responses may reduce the initial costs of learning ecologically relevant threats while maintaining sufficient behavioural plasticity to respond to variation in local conditions. Here, we test if induced neophobia results in threat-sensitive behavioural trade-offs in response to a novel chemosensory cue. Our first experiment shows that while juvenile convict cichlids (Amatitlania nigrofasciata) pre-exposed to high (but not low) risk conditions exhibited predator avoidance to a novel odour (rainbow trout, Oncorhynchus mykiss), the response intensity was not influenced by the concentration of trout odour detected. Our second experiment demonstrated that the intensity of anti-predator response towards a novel predator cue was dependent upon the level of background risk. Convict cichlids pre-exposed to high-risk conditions showed stronger responses than those pre-exposed to low-risk conditions, while cichlids pre-exposed to intermediate-risk conditions exhibited intermediate response intensities. Together, these data demonstrate that background levels of risk and not the concentration of novel cues detected shape the induced neophobic response pattern of juvenile convict cichlids.     

Cheetah mothers' vigilance: looking out for prey or for predators?

Summary Free-living cheetah (Acinonyx jubatus) cubs are killed by a number of predators, thus vigilance in cheetah mothers may be a form of anti-predator behaviour as well as a means of locating prey. Mothers' vigilance during the day was closely associated with measures of hunting but not with measures of anti-predator behaviour. In contrast, mothers' vigilance at kills was not related to hunting but was related to anti-predator behaviour. Both forms of vigilance decreased as cubs grew older. Vigilance during the day increased with litter size which supports a model of shared parental investment (Lazarus and Inglis 1986) because after prey had been located and caught by mothers, cubs shared the prey between them. Vigilance at kills did not increase with litter size when cubs were young; in these situations predators stole cheetahs' prey and rarely chased cubs so, at most, only a single cub would be taken. Mothers' anti-predator behaviour away from kills did increase with litter size at young cub ages however; more cubs are killed in these circumstances the greater is the size of the litter. When cubs were older and could outrun predators, neither vigilance at kills nor anti-predator behaviour increased with litter size. These results strongly support two models of unshared investment (Lazarus and Inglis 1986) and demonstrate, not only that superficially similar behaviour has different functions in different contexts, but that parental investment is shaped by the type of benefits accrued from it.     

Experimental evaluation of aggregation behavior in the sea urchin Strongylocentrotus droebachiensis

Defensive aggregation by Strongylocentrotus droebachiensis has been invoked as the fulcrum for the transformation of macroalgal beds into coralline barrens in the northwest Atlantic. We critically examined some of the mechanisms contributing to aggregation behavior by experimentally manipulating sea urchins, purported predators and food during autumn 1983 and spring 1984 both in the laboratory and field. We utilized several approaches to examine a range of sea urchin responses to the presence of food, tethered predators, caged predators, crushed con-specifics in the field and predators in laboratory tanks. Some of the field cages had the property of allowing free passage to sea urchins while retaining lobsters; this allowed distinctions to be made between artifacts caused by cage walls or topographic barriers and unrestricted behavioral responses of sea urchins. The results falsified the hypothesis that aggregations of S. droebachiensis are elicited by predators. Except in the presence of algae, sea urchins always avoided decapod predators (but not sea stars) and fled from the vicinity of injured conspecifics. However, avoidance behavior was subordinate to feeding responses, demonstrated by mass migrations of sea urchins into cages (with lobsters) to feed on algae. We reaffirmed by observation and manipulation previous studies which showed that sea urchins aggregate only in the presence of food. Two types of sea urchin groupings were delineated: (1) surficial two dimensional associations, often caused by topographic or other features which inhibited dispersal and (2) cohesive three-dimensional aggregations induced by food.     

Case selection by a limnephilid caddisfly [Potamophylax latipennis (Curtis)] in response to different predators

Some organisms use morphological structures obtained by behavioural processes to lower mortality by predation. We test whether larvae of the limnephilid caddisfly Potamophylax latipennis (Curtis) vary their responses to the presence of different predators (dragonfly naiads, fire salamander larvae or brown trout) by choosing organic or mineral cases. We offered both case types to larvae, and simulated differences in predation risk using water conditioned with chemicals from the different predators. Our results show that Potamophylax larvae detect and discriminate predators using water-borne chemical cues and alter their choice of case type according to the perceived predation risk. Moreover, the distribution of larvae bearing cases of different anti-predator value matches the spatial variation in predation risk in the field.     

Threat-sensitive generalization of predator recognition by larval amphibians

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.     

Quantitative composition of the defensive secretion ofBledius species (Coleoptera: Staphylinidae: Oxytelinae) is adapted to naturally occurring predators

Summary The adaptation of defensive secretions to their target organisms was examined for the abdominal gland secretions ofBledius furcatus, B. spectabilis andB. arenarius. Therefore the target organisms of the secretion of theseBledius species (i.e. their predators) had to be identified. At the collection sites examined these were the earwigLabidura riparia, the antCataglyphis bicolor, the flyLispe candicans, different carabids of the generaPogonus, Dichirotrichus, Dyschirius, Bembidion andCalathus and the wading birdsHaematopus ostralegus andCalidris alba. The secretion of the abdominal glands contains the toxin ptoluquinone dissolved in either-dodecalactone and 1-undecene (B. furcatus andB. spectabilis) or in octanoic acid and octyloctanoate (B. arenarius). The ratio of these solvents is species-specific. Application experiments using some of the natural insect predators (L. riparia, C. bicolor, Pogonus, Di. gustavii, Dyschirius) revealed that these solvent ratios provided a more effective deterrent than other possible ratios. Thus by combining the solvents in certain ratios, the capability of cuticular penetration and therefore the effectiveness of the defensive secretions are adapted to their natural targets.     

Costs of reproduction in lizards: escape tactics and susceptibility to predation

Summary Increased basking and reduced agility in gravid female southern water skinks (Eulamprus tympanum) suggest that they will be more vulnerable to predators. However, gravid females shift their anti-predator tactics towards crypsis, by allowing potential predators (such as a human observer) to approach more closely than do males and non-gravid females. Gravid females were taken no more frequently than were non-gravid females or males when exposed to two types of natural predators, birds (kookaburra, Dacelo gigas) or snakes (common blacksnakes, Pseudechis porphyriacus) in field enclosures. Both these results suggest that the vulnerability of potential prey in this system is determined by the predator's probability of detecting a potential prey item, not its probability of capturing the prey item after detection. Hence, laboratory-based measures of performance demonstrating reduced escape speed may sometimes have little relevance to actual fitness under field conditions, if the probability that an animal will be taken by a predator depends primarily on whether or not it is seen, rather than on how quickly it can escape. Correspondence to: L. Schwarzkopf     

Resembling a Viper: Implications of Mimicry for Conservation of the Endangered Smooth Snake

The phenomenon of Batesian mimicry, where a palatable animal gains protection against predation by resembling an unpalatable model, has been a core interest of evolutionary biologists for 150 years. An extensive range of studies has focused on revealing mechanistic aspects of mimicry (shared education and generalization of predators) and the evolutionary dynamics of mimicry systems (co‐operation vs. conflict) and revealed that protective mimicry is widespread and is important for individual fitness. However, according to our knowledge, there are no case studies where mimicry theories have been applied to conservation of mimetic species. Theoretically, mimicry affects, for example, frequency dependency of predator avoidance learning and human induced mortality. We examined the case of the protected, endangered, nonvenomous smooth snake (Coronella austriaca) that mimics the nonprotected venomous adder (Vipera berus), both of which occur in the Åland archipelago, Finland. To quantify the added predation risk on smooth snakes caused by the rarity of vipers, we calculated risk estimates from experimental data. Resemblance of vipers enhances survival of smooth snakes against bird predation because many predators avoid touching venomous vipers. Mimetic resemblance is however disadvantageous against human predators, who kill venomous vipers and accidentally kill endangered, protected smooth snakes. We found that the effective population size of the adders in Åland is very low relative to its smooth snake mimic (28.93 and 41.35, respectively).Because Batesian mimicry is advantageous for the mimic only if model species exist in sufficiently high numbers, it is likely that the conservation program for smooth snakes will fail if adders continue to be destroyed. Understanding the population consequences of mimetic species may be crucial to the success of endangered species conservation. We suggest that when a Batesian mimic requires protection, conservation planners should not ignore the model species (or co‐mimic in Mullerian mimicry rings) even if it is not itself endangered. Implications of mimicry for Conservation of the endangered smooth snake     

Natal philopatry in bannertailed kangaroo rats

Summary I describe prolonged retention of offspring in natal home ranges, or natal philopatry, in the bannertailed kangaroo rat Dipodomys spectabilis. Though weaning occurs at about one month of age, offspring shared natal burrows with their mothers for three to seven months, and 39% of surviving offspring remained within natal home ranges through reproductive maturity. Males as well as females were philopatric. Data on the availability of burrows and on patterns of resettlement suggest that natal philopatry in this species may be a means of providing juveniles with access to essential resources, in this case food caches and large complex burrow systems, that are not readily available outside natal home ranges.     

Does information of predators influence general wariness?

Antipredator behavior includes several qualitatively distinct activities, but few studies have determined the degree to which these activities are independent. If behaviors are not independent, then the nature of the relationship would illustrate potential performance constraints. We studied crimson rosellas (Platycercus elegans) and first focused on acoustic predator discrimination. We measured time allocation before and after playback of one of three experimental treatments (peregrine falcons—Falco peregrinus, wedge-tailed eagles—Aquila audax, and crimson rosellas) to determine whether or not rosellas discriminated predators from non-predators, and specifically whether or not they discriminated large from small predators. We then focused on the decision to flee. We experimentally approached subjects and measured the distance at which they oriented to us (alert distance) and the distance at which they fled (flight initiation distance; FID). We found that rosellas could distinguish among predators; however, there was no effect on general wariness as measured by FID. These two processes of antipredator behavior may, thus, be independent.     

Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows

According to the threat-sensitive predator avoidance hypothesis, selection favors prey that accurately assess the degree of threat posed by a predator and adjust their anti-predator response to match the level of risk. Many species of animals rely on chemical cues to estimate predation risk; however, the information content conveyed in these chemical signatures is not well understood. We tested the threat-sensitive predator avoidance hypothesis by determining the specificity of the information conveyed to prey in the chemical signature of their predator. We found that fathead minnows (Pimephales promelas) could determine the degree of threat posed by northern pike (Esox lucius) based on the concentration of chemical cues used. The proportion of minnows that exhibited an anti-predator response when exposed to a predator cue increased as the concentration of the pike cue used increased. More surprisingly, the prey could also distinguish large pike from small pike based on their odor alone. The minnows responded more intensely to cues of small pike than to cues of large pike. In this predator–prey system small pike likely represent a greater threat than large pike.Communicated by A. Mathis     

Influences of divergent behavioral strategies upon risk allocation in juvenile flatfishes

Animals balance feeding and anti-predator behaviors at various temporal scales. When risk is infrequent or brief, prey can postpone feeding in the short term and temporally allocate feeding behavior to less risky periods. If risk is frequent or lengthy, however, prey must eventually resume feeding to avoid fitness consequences. Species may exhibit different behavioral strategies, depending on the fitness tradeoffs that exist in their environment or across their life histories. North Pacific flatfishes that share juvenile rearing habitat exhibit a variety of responses to predation risk, but their response to risk frequency has not been examined. We observed the feeding and anti-predator behaviors of young-of-the-year English sole (Parophrys vetulus), northern rock sole (Lepidopsetta polyxystra), and Pacific halibut (Hippoglossus stenolepis)—three species that exhibit divergent anti-predator strategies—following exposure to three levels of predation risk: no risk, infrequent (two exposures/day), and frequent (five exposures/day). The English sole responded to the frequent risk treatment with higher feeding rates than during infrequent risk, following a pattern of behavioral response that is predicted by the risk allocation hypothesis; rock sole and halibut did not follow the predicted pattern, but this may be due to the limited range of treatments. Our observations of unique anti-predator strategies, along with differences in foraging and species-specific ecologies, suggest divergent trajectories of risk allocation for the three species.     

Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi)

Predator–prey relationships provide an excellent opportunity to study coevolved adaptations. Decades of theoretical and empirical research have illuminated the various behavioral adaptations exhibited by prey animals to avoid detection and capture, and recent work has begun to characterize physiological adaptations, such as immune reactions, metabolic changes, and hormonal responses to predators or their cues. A 2-year study quantified the activity budgets and antipredator responses of adult Belding’s ground squirrels (Spermophilus beldingi) living in three different California habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed and predators and escape burrows are difficult to see, animals responding to alarm calls remain alert longer and show more exaggerated responses than adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than adults at the other two sites. A 4-year study using noninvasive fecal sampling of cortisol metabolites revealed that S. beldingi living in the closed site also have lower corticoid levels than adults at the other two sites. The lower corticoids likely reflect that predation risk at this closed site is predictable, and might allow animals to mount large acute cortisol responses, facilitating escape from predators and enhanced vigilance while also promoting glucose storage for the approaching hibernation. Collectively, these data demonstrate that local environments and perceived predation risk influence not only foraging, vigilance, and antipredator behaviors, but adrenal functioning as well, which may be especially important for obligate hibernators that face competing demands on glucose storage and mobilization.