Olfactory predator recognition in the brown mouse lemur (Microcebus rufus) in Ranomafana National Park,Madagascar

Predator odors such as urine and feces are known to elicit antipredator behaviors in prey including avoidance, fear, and curiosity. We measured how wild brown mouse lemurs (Microcebus rufus) responded to odors of mammalian, avian, and snake predators as well as nonpredator controls. The first experiment took place under controlled conditions in a laboratory where we recorded the occurrence of four behavioral categories (ignore, curiosity, alert, and fear) in response to a single odor. Subjects exhibited behavioral change significantly more often in response to the predator than to control stimuli, but did not distinguish between familiar and unfamiliar predators. Mammalian predator urine and feces were most likely to elicit behavioral change. The owl was the only predator to never elicit behavioral change, possibly because owls do not provide relevant odor cues. A second experiment employing live traps in the forest found that neither predator nor control odors affected the likelihood of capture. Due to their longevity, odors do not provide accurate information of spatial and temporal risk, and while mouse lemurs may have initially hesitated to enter a trap, in the absence of additional information about risk, they may have eventually ignored the stimuli. This study found that brown mouse lemurs are able to distinguish between predator and nonpredator odors, and that risk assessment may be affected by the experience, as well as predator and sensory stimulus quality.     

Potential risks of olfactory signaling: the effect of predators on scent marking by beavers

Mammals scent mark their territories to advertise occupancyand ownership. However, signaling with scent for territorialdefense can have a negative effect by advertising an individual'spresence and location to predators. In this study, we measuredresponses to a simulated territorial intrusion by conspecificadult male Eurasian beavers (Castor fiber) either in the localizedpresence or in the absence of odor of a predator to test thehypothesis that the territorial defense of free-living beaverswould be disrupted by the presence of predation risk in theirnatural environment. We predicted that beavers would significantlyreduce their willingness to countermark intruder's scent inthe presence of the scent of predators (wolf [Canis lupus] andlynx [Lynx lynx]), compared with a control (no odor), as responsesare in general stronger to predator scent marks than nonpredatorscent. Therefore, we also predicted that the effects of nonpredatorymammal scent (neophobic control) (eland [Taurotragus oryx] andhorse [Equus cabalus]) are to be expected somewhere in betweenthe effects of the predator odor and a control. Our resultssuggest that both predator and nonpredator scents reduce beaversresponse to a simulated intruder's scent mounds and thereforedisrupt their territorial defense. However, predator scent hada stronger effect than nonpredator scent. Beavers may thereforebe at great risk on territories with predators present becauseof the trade-off between predator avoidance and territorialdefense. Our study demonstrates the potential of predation riskas a powerful agent of counterselection on olfactory signalingbehavior.     

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

Predator–Primate Distribution,Activity, and Co-occurrence in Relation to Habitat and Human Activity Across Fragmented and Contiguous Forests in Northeastern Madagascar

Predator–primate interactions are understudied, yet predators have been shown to influence primate behavior, population dynamics, and spatial distribution. An understanding of these interactions is important for the successful management and conservation of these species. Novel approaches are needed to understand better the spatial relationships between predators and primates across changing landscapes. We combined photographic surveys of predators and humans with line-transect sampling of lemurs across contiguous and fragmented forests in Madagascar to 1) compare relative activity; 2) estimate probability of occupancy and detection; 3) estimate predator–primate and local people–primate co-occurrence; and 4) assess variables influencing these parameters across contiguous and fragmented forests. In fragmented (compared to contiguous) forest sites endemic predator and lemur activity were lower whereas introduced predator and local people activity were higher. Our two-species interaction occupancy models revealed a higher number of interactions among species across contiguous forest where predator and lemur occupancy were highest. Mouse lemurs show evidence of “avoidance” (SIF < 1.0) with all predator species (endemic and introduced) in contiguous forest whereas white-fronted brown lemurs show “attraction” (SIF > 1.0) with feral cats and local people in contiguous forest. Feral cats demonstrated the highest number of interactions with lemurs, despite their distribution being limited to only contiguous forest. Distance to forest edge and distance to nearby villages were important in predicting predator occupancy and detection. These results highlight the growing threat to endemic predators and lemurs as habitat loss and fragmentation increase throughout Madagascar. We demonstrate the effectiveness of a novel combination of techniques to investigate how predator species impact primate species across a gradient of forest fragmentation.     

Anti‐Predator Behaviour in a Nocturnal Primate,the Grey Mouse Lemur (Microcebus murinus)

Although one‐third of all primates are nocturnal, their anti‐predator behaviour has rarely been studied. Because of their small body size, in combination with their solitary and nocturnal life style, it has been suggested that they mainly rely on crypsis to evade predators. However, recent studies revealed that nocturnal primates are not generally cryptic and that they exhibit predator‐specific escape strategies as well as alarm calls. In order to add to this new body of research, we studied anti‐predator strategies of nocturnal grey mouse lemurs experimentally. In order to elicit anti‐predator behaviour and alarm calls, we conducted experiments with a carnivore‐, snake‐ and raptor model. We also conducted playback experiments with mouse lemur alarm calls to characterize their function. In response to predator models, they exhibited a combination of anti‐predator strategies: in response to carnivore and snake models, mouse lemurs monitored the predator, probably to assess the potential risk that emanates from the predator. In response to raptor models they behaved cryptically and exhibited freezing behaviour. All mouse lemurs, except one individual, did not alarm call in response to predator models. In addition, during playback experiments with alarm calls, recorded during real predator encounters, mouse lemurs did not emit alarm calls nor did they show any escape behaviour. Thus, as in other nocturnal primates/mammals, mouse lemurs do not seem to rely on routinely warning of conspecifics against nearby predators.     

Predation and cathemerality. Comparing the impact of predators on the activity patterns of lemurids and ceboids

The removal, or absence, of predatory species could be a contributing proximate factor to the rise of primate cathemerality. But predators themselves can also be cathemeral, so cathemerality could well be an evolutionary stable strategy. From a comparative perspective, it appears that the effect of predatory species cannot provide a unitary explanation for cathemerality. Varying distributions and population densities of predators, especially raptors, may be key factors in owl monkey (Aotus) cathemerality, but temperature and lunar cycle variation have also been implicated. In Madagascar, while raptors are potential predators of lemur species, the cathemerality of Eulemur species coincides with that of the fossa (Cryptoprocta ferox), a major predatory threat to lemurs. Thus, lemurid cathemerality may be more parsimoniously explained as an evolutionary stable strategy.     

Can Paradise Fish (Macropodus opercularis,Anabantidae) Recognize a Natural Predator? An Ethological Analysis

Predator recognition and avoidance by paradise fish have been studied with allopatric species and model experiments. The effect of sympatric predators has not been investigated. Here I report that reactions of paradise fish towards a sympatric predator (Channa micropeltes) are quantitatively different from those shown towards an allopatric predator or different harmless species of fishes. I investigate the possible cues eliciting this differential response and show that visual as well as olfactory stimuli play roles. Olfactory stimuli from the sympatric predator alone elicit an elevated level of activity from paradise fish; the appearance of the sympatric predator (with or without olfactory stimuli) results in an exploratory and display reaction. I speculate what visual stimuli may play roles in predator recognition in paradise fish and I suggest that previously asserted key stimuli such as the eyes of the encountered heterospecific fish may not differentiate the harmful species from innocuous. I conclude that the antipredatory behavior of paradise fish may be affected by both genetic factors and learning and that the relative importance of the former or latter factor may vary depending on the situation.     

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

Failure of captive-born greater rheas (Rhea americana, Rheidae, Aves) to discriminate between predator and nonpredator models

The capacity to recognize and respond to predators can be lost by captive animals. Habituation to humans caused by the captive environment can be transferred to other stimuli, such as predators, a situation that conservation biologists wish to avoid. Greater rheas are threatened South American birds, for which there are plans for reintroduction programs in Brazil. The goal of this study was to evaluate the behavioral responses of captive-born greater rheas to different models of predators and nonpredators. Seventeen captive-born greater rheas, divided into four groups, from the Belo Horizonte Zoo, Brazil were studied. Three predator and three nonpredator models were presented to the birds and their behavioral responses recorded. Predators versus nonpredator models and the behavior of rheas in three experimental phases (baseline, models, and postmodels) were analyzed. Captive-born greater rheas modified their behaviors in the presence of both predator/nonpredator models, increasing alert and wary behaviors (alert, observing, and pacing behaviors: P?<?0.01), showing some degree of antipredator behavior persistence, but they were unable to discriminate between predator and nonpredator models (all behaviors: P?>?0.05). In conclusion, antipredator training should be implemented to develop the expression of this behavior before reintroductions are attempted.     

Reversing Stimulus Timing in Visual Conditioning Leads to Memories with Opposite Valence in Drosophila

Animals need to associate different environmental stimuli with each other regardless of whether they temporally overlap or not. Drosophila melanogaster displays olfactory trace conditioning, where an odor is followed by electric shock reinforcement after a temporal gap, leading to conditioned odor avoidance. Reversing the stimulus timing in olfactory conditioning results in the reversal of memory valence such that an odor that follows shock is later on approached (i.e. relief conditioning). Here, we explored the effects of stimulus timing on memory in another sensory modality, using a visual conditioning paradigm. We found that flies form visual memories of opposite valence depending on stimulus timing and can associate a visual stimulus with reinforcement despite being presented with a temporal gap. These results suggest that associative memories with non-overlapping stimuli and the effect of stimulus timing on memory valence are shared across sensory modalities.     

Predator-induced plasticity in web-building behaviour

Many orb-web weaving spiders add conspicuous silken structures, called stabilimenta, to the hub of their webs, which are hypothesized to attract more prey. However, they may also attract predators. Orb spiders should therefore alter their web-building behaviour to minimize predation risk. We tested this hypothesis by experimentally examining web-building responses of the St Andrew cross spider, Argiope versicolor, to predation risk from one of its natural predators, the jumping spider Portia labiata. We randomly assigned A. versicolor juveniles to one of three treatments: (1) blank control (clean blotting paper: no odour from the predator or nonpredator); (2) predator odour cues from P. labiata; and (3) nonpredator control (odour cues from Leucauge decorata). Each individual of A. versicolor was monitored until it had built five consecutive webs (two webs before and three webs after the introduction of predator cues). When exposed to predator cues, the juveniles not only decreased the frequency of stabilimentum building but also refrained from increasing stabilimentum area, capture area and capture silk thread with subsequent webs compared with the blank control and the nonpredator control. Web-building traits, however, were not significantly different between the blank control and the nonpredator control. One plausible explanation is that A. versicolor juveniles can detect and discriminate between predators and nonpredators through olfactory cues and alter stabilimentum building and other web traits in response to the risk of predation. This is the first demonstration of an adaptive, plastic web-building behavioural response induced by chemical cues from a predator.     

High stimulus specificity characterizes anti-predator habituation under natural conditions

Habituation is one of the most fundamental learning processes that allow animals to adapt to dynamic environments. It is ubiquitous and often thought of as a simple form of non-associative learning. Very little is known, though, about the rules that govern habituation and their significance under natural conditions. Questions about how animals incorporate habituation into their daily behaviour and how they can assure only to habituate to non-relevant stimuli are still unanswered. Animals under threat of predation should be particularly selective about which stimuli they habituate to, since ignoring a real threat could be fatal. In this study, we tested the response of fiddler crabs, Uca vomeris, to repeatedly approaching dummy predators to find out whether these animals habituate to potential predators and to test the selectivity of the habituation process. The crabs habituated to model predators, even though they were confronted with real predators during the same habituation process. They showed remarkable selectivity towards the stimulus: a simple change in the approach distance of the stimulus led to a recovery in their responses. The results strongly indicate that in the context of predator avoidance, habituation under natural conditions is highly selective and a stimulus is not defined just by its current sensory signature, but also its spatio-temporal history.     

Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.     

Use of Vocal Fingerprinting for Specific Discrimination of Gray (Microcebus murinus) and Rufous Mouse Lemurs (Microcebus rufus)

Advertisement calls are often important noninvasive tools for discriminating cryptic species and for assessing specific diversity and speciation patterns in nature. We investigated the contribution of these calls to uncover specific diversity in nocturnal Malagasy lemurs. We compared sexual advertisement and predator advertisement calls of two mouse lemur species, western gray and eastern rufous mouse lemurs (Microcebus murinus and M. rufus, respectively) living in two contrasting habitats (dry deciduous vs. rain forest), and analyzed them statistically. Both species emitted several highly variable whistle calls in the context of predator-avoidance. Intrapopulation variation was high and overlapped interspecific variation. Sexual advertisement calls, given in the mating context, displayed a totally distinct, species-specific acoustic structure. Whereas gray mouse lemurs produced rapidly multifrequency modulated, long trill calls, rufous mouse lemurs gave slowly frequency-modulated short chirp calls. Our results suggest specific status for gray and rufous mouse lemurs and indicate the importance of predation and social needs in shaping vocal communication.     

Hamsters Use Predator Odors as Indirect Cues of Predation Risk

Golden hamsters (Mesocricetus auratus) use olfactory cues to assess traits of conspecifics such as kinship, individual identity, and reproductive status. The environment, however, is full of a wide variety of other olfactory information such as signals emitted by some of the hamster’s primary predators. Given this, we hypothesized that hamsters use odors from predators as an indirect sign of increased predation risk in the environment. In addition, based on data that show that wild hamsters are diurnal while laboratory hamsters are nocturnal, we hypothesized that if golden hamsters did respond to the predator odors, perceived predator risk might influence daily activity patterns in hamsters. We tested male and female hamsters over 5 d with scent gland secretion from domestic ferrets (Mustela putorius furo) and compared their behavior to that observed when they were exposed to a clean arena. In response to the predator odor, subjects significantly decreased the amount of time active outside of their burrow, returned to their burrow more quickly, and spent less time near the predator odor than the clean control stimulus. These results strongly support our hypothesis that hamsters, like other species of small mammals, avoid predator odors. The results did not, however, support our second hypothesis that exposure to predator odors during the dark phase of the light cycle would elicit a switch to a more diurnal pattern of activity. More work is needed to understand how environmental cues and internal mechanisms interact to shape activity patterns.     

The behavioural responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels

• 1 Experiments were designed to determine the relative importance of chemical and visual stimuli in eliciting predator avoidance behaviour in juvenile freshwater crayfish Pacifastacus leniusculus (Dana).
• 2 Crayfish placed in visual and/or chemical contact with one of two predators exhibited marked avoidance behaviour, spending less time walking and climbing and more time within shelters.
• 3 The combined effects of both visual and chemical stimuli increased crayfish shelter use and reduced walking and climbing activity to a greater degree than either stimulus when presented alone.
• 4 Crayfish exhibited avoidance behaviour in response to chemical stimuli during periods of light and darkness. Visual detection of predators elicited avoidance behaviour during the day.
• 5 It is suggested that the behavioural response of P. leniusculus to chemical stimuli reduces the likelihood of being detected by visual predators, and that chemical stimuli lower the response threshold for avoidance behaviour in crayfish reacting to visual stimuli. The adaptiviry of using chemical cues to detect predators is emphasized.

     

Confusion Effect in a Reptilian and a Primate Predator

The confusion effect is claimed to be one benefit of group living with respect to predator avoidance: it is more difficult for predators to capture prey that is surrounded by other conspecifics than to capture an isolated individual. So far, the predictions of the confusion effect have been tested mainly in aquatic predators. As the confusion effect is seen to be a general problem for predators, terrestrial predators of two different vertebrate classes were used to test it. The prey (mealworms and black beetles, Tenebrio molitor ) was harmless and had no chance of predator avoidance. Thus, confounding effects of group defence and enhanced vigilance were controlled. Both leopard geckos ( Eublepharis macularius ) and common marmosets ( Callithrix jacchus ) took longer to catch one out of several prey compared to one single prey. Leopard geckos showed more fixations (changing of head position) when confronted with 20 mealworms than when confronted with only one mealworm, thus showing indications of being 'confused'.     

Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.)

We report the development of 13 new microsatellite markers for mouse lemurs (Microcebus sp.). Two markers were isolated from the fat tailed dwarf lemur (Cheirogaleus medius) and 11 from the grey mouse lemur (Microcebus murinus). A total of 561 individuals from four different species of mouse lemurs was genotyped with the newly developed markers. All markers showed Mendelian inheritance in 21 families of mouse lemurs. All markers show polymorphism in several species of mouse lemurs and seven amplified in C. medius. Among these new markers are the first 10 published for M. berthae and the first 11 for M. griseorufus.     

Submaximal leaping in the grey mouse lemur

In arboreal animals such as the grey mouse lemur (Microcebus murinus Miller, 1777), leaping is the most frequent strategy for predator avoidance. The aim of this study was to characterise the locomotor adaptation in response to the structural constraint of the habitat (i.e., position of the landing substrate). Thus, we characterised the push-off phase by inducing the lemurs to leap up to a range of heights from horizontal to their own individual highest performance. Using uniplanar high-frequency cineradiographs collected in a sagittal plane, the relative contributions of the centre of mass (CoM) velocity vector magnitude and orientation to leaping performance were evaluated. The kinematics of the push-off phase showed that for low landing heights, leaping performance was essentially due to hip and knee extensions. Higher leaps seemed to be related to an increase in ankle contribution. At all leaping heights, the proximal-to-distal sequence of the hind limb joints controlled the orientation and magnitude of the M. murinus CoM velocity vector while pushing off. Finally, the analysis of the velocity vector at the onset of take-off suggested that the optimal solution for predator avoidance was to leap for horizontal distance and not for vertical distance.