Olfactory Predator Research Articles

Contextual variation in the alarm call responses of dwarf mongooses, Helogale parvula

Alarm calling is a widespread antipredator behaviour, but it is not always a reliable indication of real danger. Individuals must decide when to respond to alarm calls as a function of the relative costs and benefits, but experiments investigating contextual influences are rare. We used playback experiments in conjunction with supplementary feeding and the presentation of direct predator cues to examine variation in receiver responses to alarm calls in a habituated population of wild dwarf mongooses. First, we investigated whether individuals adjust their response to alarm calls depending on their own satiation level and spatial position of the caller. Individuals were more likely to respond to alarm calls when they had received supplementary food, and hence could prioritize minimization of predation risk over starvation. There was also increased responsiveness to alarm calls given by individuals from elevated positions compared to those on the ground; sentinels (raised guards) are more likely to detect potential predators than foragers, and alarm calls from elevated positions are probably perceived as more reliable. When individuals did respond, they were more likely to flee following an alarm call given from ground level; foragers are likely to detect predators in closer proximity than sentinels, requiring more urgent escape responses. Second, we examined how individuals combine social information provided by alarm calls with personal information relating to predator presence. Receiver responses to terrestrial and aerial alarm calls did not differ when they followed interaction with an olfactory predator cue compared to an olfactory control cue. Following interaction with a terrestrial predator cue, however, latency to nonvigilance was significantly longer after hearing an aerial alarm call than after hearing a terrestrial alarm call, potentially because of social information novelty. Our results provide experimental evidence that receivers respond flexibly to alarm calls depending on receiver, signaller and external factors.

Increased olfactory search costs change foraging behaviour in an alien mustelid: a precursor to prey switching?

If generalist predators are to hunt efficiently, they must track the changing costs and benefits of multiple prey types. Decisions to switch from hunting preferred prey to alternate prey have been assumed to be driven by decreasing availability of preferred prey, with less regard for accessibility of alternate prey. Olfactory cues from prey provide information about prey availability and its location, and are exploited by many predators to reduce search costs. We show that stoats Mustela erminea, an alien olfactory predator in New Zealand, are sensitive to the search costs of hunting both their preferred rodent prey (mice) and a less desirable alternate prey (locust). We manipulated search costs for stoats using a novel form of olfactory camouflage of both prey, and found that stoats altered their foraging strategy depending on whether mice were camouflaged or conspicuous, but only when locusts were also camouflaged. Stoats gave up foraging four times more often when both prey were camouflaged, compared to when mice were conspicuous and locusts camouflaged. There were no differences in the foraging strategies used to hunt camouflaged or conspicuous mice when locusts were easy to find. Consequently, camouflaged mice survived longer than conspicuous mice when locusts were hard to find, but not when locusts were easy to find. Our results demonstrate that predators can integrate search costs from multiple prey types when making foraging decisions. Manipulating olfactory search costs to alter foraging strategies offers new methods for understanding the factors that foreshadow prey switching.

Prey aggregation is an effective olfactory predator avoidance strategy.

Predator–prey interactions have a major effect on species abundance and diversity, and aggregation is a well-known anti-predator behaviour. For immobile prey, the effectiveness of aggregation depends on two conditions: (a) the inability of the predator to consume all prey in a group and (b) detection of a single large group not being proportionally easier than that of several small groups. How prey aggregation influences predation rates when visual cues are restricted, such as in turbid water, has not been thoroughly investigated. We carried out foraging (predation) experiments using a fish predator and (dead) chironomid larvae as prey in both laboratory and field settings. In the laboratory, a reduction in visual cue availability (in turbid water) led to a delay in the location of aggregated prey compared to when visual cues were available. Aggregated prey suffered high mortality once discovered, leading to better survival of dispersed prey in the longer term. We attribute this to the inability of the dead prey to take evasive action. In the field (where prey were placed in feeding stations that allowed transmission of olfactory but not visual cues), aggregated (large groups) and semi-dispersed prey survived for longer than dispersed prey—including long term survival. Together, our results indicate that similar to systems where predators hunt using vision, aggregation is an effective anti-predator behaviour for prey avoiding olfactory predators.

Greater Sage-Grouse (Centrocercus urophasianus) select nest sites and brood sites away from avian predators

ABSTRACT. Greater Sage-Grouse (Centrocercus urophasianus) have declined in distribution and abundance in western North America over the past century. Depredation of nests and predation of chicks can be two of the most influential factors limiting their productivity. Prey species utilize antipredation behaviors, such as predator avoidance, to reduce the risk of predation. Birds in general balance the dual necessity of selecting cover to hide from visual and olfactory predators to enhance prospects of survival and reproductive success, which may also be achieved by selecting habitat with relatively fewer predators. We compared avian predator densities at Greater Sage-Grouse nests and brood locations with those at random locations within available sage-grouse habitat in Wyoming. This comparison allowed us to assess the species' ability to avoid avian predators during nesting and early brood rearing. During 2008–2010, we conducted 10-min point-count surveys at 218 nests, 249 brood locations from 83 broods, an...

Can predator avoidance training improve reintroduction outcomes for the greater bilby in arid Australia?

Many threatened species’ reintroductions in Australia fail because of predation by introduced cats and foxes. We attempted to improve reintroduction outcomes by training greater bilbies, Macrotis lagotis, to recognize cats as predators. The movement and behaviour of trained and control bilbies were compared in both a predator-free environment and in an area where cats and foxes were present. Trained bilbies within the predator-free environment moved significantly further, used more burrows with more entrances and changed burrows more frequently than untrained control animals. Trained bilbies also moved burrows when presented with olfactory predator stimuli while control bilbies did not. However, when bilbies were reintroduced to an area where predators were present, there was no difference in survival, movement or burrow use between trained and control bilbies. Both groups exhibited high survival rates in the first 6 months after release. In the presence of predators, both trained and control bilbies appeared to be more predator-aware possibly because of control bilbies learning from trained conspecifics or cohabiting rabbits or through inadvertent contamination of control animals during training. Results suggest that bilbies can be taught to recognize exotic predators but this may not necessarily translate into improved reintroduction success in the wild. Further investigation into cultural and filial transfer of antipredator behaviour is recommended.

Does Weather or Site Characteristics Influence the Ability of Scavengers to Locate Food?

AbstractOlfactory predators and scavengers rely on odors to locate food, and they forage primarily at night. We hypothesized that weather (e.g. wind speed, humidity, and temperature), vegetation, and landscape features affect the dissipation of odors in the atmosphere and, thus, impact the foraging efficiency of olfactory predators. We tested this hypothesis by assessing what conditions were correlated with the persistence of bait along the dike surrounding Willard Bay Reservoir, Utah. We distributed 124 chicken eggs and 199 dead European starlings (Sturnus vulgaris) as bait over 21 separate occasions spanning from May 21, 2009, to August 18, 2009. We used timers to record the time of consumption and cameras to identify which species ate the bait. Sixty‐six eggs and 87 dead European starlings were consumed. The bait was consumed mostly at night (83%) and by striped skunks (Mephitis mephitis), raccoons (Procyon lotor), and red foxes (Vulpes vulpes). We used nest survival models in program MARK to determine which covariates influenced bait persistence. We tested nine variables and found that bait persistence was influenced by section of the dike, time since study initiation, temperature, humidity, and wind speed but not bait type (egg or dead European starling), terrain, or visual cover. How quickly scavengers were able to locate food, which was inversely related to rates of bait persistence, decreased with higher temperatures and wind speeds and increased with higher humidity. Our results support the hypothesis that weather and micro‐habitat characteristics impact the ability of olfactory predators and scavengers to locate food.

Anti-predatory performance in hatchery-reared red tilefish ( Branchiostegus japonicus) and behavioral characteristics of two predators: Acoustic telemetry, video observation and predation trials

The anti-predatory performance of hatchery-reared red tilefish ( Branchiostegus japonicus) using tube-shaped burrows was studied together with the behavioral characteristics of potential predators, the white spotted conger ( Conger myriaster) and the marbled rockfish ( Sebastiscus marmoratus). White spotted conger were released in Maizuru Bay (Kyoto, Japan) and tracked using acoustic telemetry; they were also observed in a tank using video recording. White spotted conger tended to remain inside shelters, but occasionally swam outside briefly at night. Attacking behavior of predators and predation avoidance behavior of red tilefish were also recorded in a tank. Red tilefish construct tube-shaped burrows into which they retreat to avoid attack. White spotted conger wandered around the tank, often invading the burrows to prey on red tilefish. Predation by white spotted conger occurred at night. Inside the burrows, red tilefish were not easily caught and were able to escape through the other entrance of the tube-shaped burrow. Marbled rockfish, on the other hand, pounced on red tilefish immediately after prey recognition, ambushing their prey near the burrow entrance. Predation by marbled rockfish was frequently observed around dusk and dawn, but some red tilefish that remained inside burrows survived. White spotted conger is nocturnal and probably an olfactory predator, whilst marbled rockfish is crepuscular and an ambush predator. For stock enhancement of red tilefish, the construction of tube-shaped burrows and their diurnal behavior around the burrows are desirable characteristics in reducing predation by both white spotted conger and marbled rockfish.

Experimental evidence for olfactory predator recognition in wild mouse lemurs

Although primates have remarkable olfactory capabilities, their ability for olfactory predator recognition is still understudied. We investigated this cognitive ability in wild gray and golden-brown mouse lemurs (Microcebus murinus and M. ravelobensis) that were confronted with four different olfactory stimuli, derived from two Malagasy predators (fossa and barn owl) and two local nonpredator species (brown lemur and sifaka). The predator response was tested (1) in a systematic cage setup and (2) in a two-way choice experiment with two Sherman traps on platforms in the forest (stimulus trap vs. nonstimulus trap). For part 1, the study animals were housed in cages during habituation and 5 days of experiments. One stimulus was tested per night and was presented underneath a drinking bottle. The changes in the time spent close to the stimulus and the drinking time at the bottle were used as indicators of predator recognition. A timidity score was established by classifying the strength of the antipredator response during the experiment. The study animals spent significantly less time drinking and less time in the stimulus area when confronted with fossa odor compared with the other stimuli. The timidity score was significantly higher during the fossa stimulus compared with the nonpredator and the control stimuli. The two-way choice experiments revealed a complete avoidance of the fossa odor, which was not found with the other stimuli. Thus, wild mouse lemurs showed clear signs of olfactory predator recognition in the case of the fossa in both experiments, but no signs of avoidance to the other presented stimuli. The lack of owl avoidance may be explained by less or no aversive metabolites in the owl stimulus or by lower significance for olfactory recognition of aerial predators. Furthermore, the results showed slight differences between the two mouse lemur species that may be linked to differences in their ecology.

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.

Greater Sage-Grouse Select Nest Sites to Avoid Visual Predators But not Olfactory Predators

Birds can hide from visual predators by locating nests where there is cover and from olfactory predators where habitat features create updrafts, high winds, and atmospheric turbulence, but sites optimal for hiding from visual and olfactory predators often differ. We examined how Greater Sage-Grouse (Centrocercus urophasianus) balance the dual needs of hiding from both visual and olfactory predators on Parker Mountain, Utah, where the Common Raven (Corvus corax) is the main visual predator and the striped skunk (Mephitis mephitis) and American badger (Taxidea taxus) are the main olfactory predators. By comparing nest sites to random sites during 2005 and 2006, we found that sage-grouse nest at sites where their nests were obscured from visual predators but were exposed to olfactory predators. To validate these findings, we replicated the study in southwest Wyoming during 2008. Again, we found that visual obscurity at nest sites was greater than at control sites but olfactory obscurity was less. Our results indicate that Greater Sage-Grouse select nest sites where they will be concealed from visual predators but at the cost of locating nests where they are exposed to olfactory predators. In southwest Wyoming, we found that olfactory predators (mammals) and visual predators (birds) depredated an equal number of nests. By selecting nest sites with visual obscurity, Greater Sage-Grouse have reduced the threat from visual predators to where it was similar to the threat posed by olfactory predators.

Do Sharp‐Tailed Grouse Select Loafing Sites to Avoid Visual or Olfactory Predators?

ABSTRACT Grouse should seek loafing sites hidden from predators; however, good hiding sites from predators that use vision to locate prey differ from good hiding sites from predators that use odor to locate prey. We compared characteristics of control sites to sites used for loafing by sharp‐tailed grouse (Tympanuchus phasianellus) to determine whether selection of loafing sites was more influenced by the need to hide from visual or olfactory predators. Sites used for loafing were similar to control sites in characteristics that would help hide a grouse from visual predators (i.e., visual obstruction, lateral visibility, visual obstruction, cover ht, and surface roughness), but loafing sites differed from control sites in characteristics that would help hide a grouse from olfactory predators (i.e., greater updrafts, wind velocities, and atmospheric turbulence).

Nest height, nest concealment, and predator type predict nest predation in superb fairy‐wrens (Malurus cyaneus)

AbstractThree factors and their interaction effects are increasingly recognized as important determinants of nest predation: nest concealment, nest height, and predator type. The risk of nest predation is predicted to vary across these variables because of nest detectability and accessibility. In general, however, few studies examine how these three variables interact in relation to nest predation, focusing instead on either nest concealment or nest height (whereby predator identity is usually not known). In this study, we examine the role of nest concealment and nest height for nest survival using both artificial and natural nests in the superb fairy‐wren (Malurus cyaneus). We indirectly identified potential predators through marks left on artificial eggs and footprints left on tracking tunnels. Predation level at artificial nests was lower than at natural nests, and this could be due to a failure of some nest predators to locate cryptic nests in the absence of cues provided by parental activity. Our results supported the prediction that exposed and concealed nests have different levels of nest predation, which can be explained by variation in predator type. Visual predators were only detected at exposed nests, and survival from visual predators was lower for high nests that were also exposed. However, olfactory predators were detected irrespective of nest height or nest concealment. Because rodents use olfaction to locate nests, this could explain the lack of association between nest concealment and predation outcome at low nests. In addition, rodent footmarks near nests were significantly associated with rodent tooth marks on eggs.

Olfactory Predator Discrimination in Yellow‐Bellied Marmots

AbstractThe mechanism underlying olfactory predator identification may be relatively experience‐independent, or it may rely on specific experience with predators. A mechanism by which prey might identify novel predators relies on the inevitable creation of sulfurous metabolites that are then excreted in the urine of carnivorous mammals. We tested whether free‐living, yellow‐bellied marmots (Marmota flaviventris) and mid‐sized herbivores that fall prey to a variety of carnivorous mammals could discriminate herbivore (elk—Cervus elephas) urine from predator (red fox—Vulpes vulpes, coyote—Canis latrans, mountain lion—Felis concolor, wolf—Canis lupus) urine, a novel herbivore (moose—Alces alces), and a distilled water control. We further asked how specific this assessment was by testing whether marmots responded differently to predators representing different levels of risk and to familiar vs. unfamiliar predators. We found that marmots responded more to urine from coyotes (a familiar predator on adults), mountain lions (a potentially unfamiliar predator that could kill adults) and wolves (a locally extinct predator that could kill adults) than to elk urine (a non‐predator). Red fox (a predator that poses a risk only to recently emerged marmot pups) urine elicited a less substantial (but not significantly so) response than coyote urine. Marmots can identify predators, even novel ones, using olfactory cues, suggesting that experience with a specific predator is not required to identify potential threats.

Predator-prey dynamics: the role of olfaction

Predator-prey dynamics: the role of olfaction

The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda)

We examined the trade-off between the behaviours associated with predator avoidance and mate acquisition in the mate-guarding amphipod crustacean Gammarus duebeni. We used laboratory experiments to investigate the impact of olfactory predator cues on activity, mate choice and mate-guarding behaviour of males and females. Pair formation declined under perceived risk of predation, reflecting reduced activity of both males and females and hence a reduced likelihood of encountering a mate. We also observed a reduction in the choosiness of both males and females. Under increased perceived predation risk, assessment of the female by the male was more likely to be followed by pair formation, and males showed a nonsignificant trend towards reduced discrimination in favour of large females and were less tenacious in their pair bond when they paired during exposure to predator cues. Females also showed less resistance behaviour, suggesting that both males and females trade off the costs of maximizing current reproductive success against the benefits of predator avoidance for survival and reproduction in the future. We discuss the implications of such context-dependent mating behaviours for ecological interactions between species and suggest that predators, via the effects of perceived predation risk on mate choice and mate guarding in the prey species, induce trait-mediated indirect effects with the potential to influence population dynamics and community structure.

Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus).

Olfactory cues of predators, such as feces, are known to elicit antipredator responses in animals (e.g., avoidance, activity). To date, however, there is little information on olfactory predator recognition in primates. We tested whether the odor of feces of different predator categories (historical Malagasy predators and introduced predators) and of Malagasy nonpredators (control) induces antipredator behavior in captive born, predator-naïve gray mouse lemurs. In an olfactory predator experiment a mouse lemur was exposed to a particular odor, fixed at a preferred location, where the animal was trained to get a reward. The behavior of the mouse lemur toward the respective stimulus category was videotaped and quantified. Results showed that mouse lemurs avoided the place of odor presentation when the odor belonged to a predator. They reacted with a significantly enhanced activity when exposed to odors of carnivores compared to those of nonpredatory controls. These findings are in favor of a genetic predisposition of olfactory predator recognition that might be based on the perception of metabolites from meat digestion.

Persistence of Alarm‐Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive‐Born Meerkats (Suricata Suricatta)

AbstractPerforming correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.

Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host’s appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.

CORRIDORS AND OLFACTORY PREDATOR CUES AFFECT SMALL MAMMAL BEHAVIOR

The behavior of prey individuals is influenced by a variety of factors including, but not limited to, habitat configuration, risk of predation, and availability of resources, and these habitat-dependent factors may have interactive effects. We studied the responses of mice to an increase in perceived predation risk in a patchy environment to understand how habitat corridors might affect interactions among species in a fragmented landscape. We used a replicated experiment to investigate corridor-mediated prey responses to predator cues in a network of open habitat patches surrounded by a matrix of planted pine forest. Some of the patches were connectedbycorridors.Weusedmark‐recapturetechniquesandforagingtraystomonitorthemovement,behavior, and abundance of small mammals. Predation threat was manipulated in one-half of the replicates by applying an olfactory predator cue. Corridors synchronized small mammal foraging activity among connected patches. Foraging also was inhibited in the presence of an olfactory predator cue but apparently increased in adjacent connected patches. Small mammal abundance did not change as a result of the predator manipulation and was not influenced by the presence of corridors. This study is among the 1st to indicate combined effects of landscape configuration and predation risk on prey behavior. These changes in prey behavior may, in turn, have cascading effects on community dynamics where corridors and differential predation risk influence movement and patch use.

Predator scent induces differing responses in two sympatric macropodids

When prey species encounter the scent of a predator they must make a decision on how to respond. This may be either to ignore, flee, hide or alarm call. While many species are able to derive detailed information from the chemical cues associated with predator scent, for some the decision to respond is often made without being able to identify the actual location and intentions of the predator. Depending on the sociality and ecology of the species, it may pay to flee or to engage in predator inspection where knowledge is impure. We tested for this in two sympatric marsupial macropodids, the parma wallaby (Macropus parma) and the red-necked pademelon (Thylogale thetis), as little is known of how these species detect and respond to olfactory cues of predation risk. We observed that, when presented with a synthetic predator scent mimicking dog urine, the social forager, T. thetis, tended to spend more time close to the predator odour, while the solitary forager, M. parma, exhibited an aversive response. The results suggest that social and ecological constraints on the sensory modalities used in predator detection may influence how macropodids respond to olfactory predator cues.