Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>) cathemeral?

Cathemerality, an activity pattern comprised of distinct periods of diurnal and nocturnal activity, is a trait found among several of the Malagasy strepsirhines and one species of Aotus. Because occasional anecdotal reports suggest that some diurnal primates can be active at night, I investigated the possibility of nocturnal ranging behavior in the ring-tailed lemur (Lemur catta) by using global positioning system (GPS) collars programmed to collect data across a 24-h period. Five individuals in a provisioned, free-ranging L. catta colony on St. Catherines Island, Georgia, USA, wore GPS collars across 1 week of the mating season. Results revealed that night ranging behavior occurred between the h of 1900 and 0530. An evaluation of the effect of moonlight on nocturnal activity showed that a greater rate of travel occurred during moonlit periods as opposed to periods when the moon had not yet risen. Distance travelled at night decreased across the deployment period, likely because of a decrease in available moonlight over time, as the lemurs were collared during a waning moon. Fewer mating opportunities over time may have also been responsible for the decrease in night ranging, because the number of females in estrus declined across the deployment period. Future research is needed to separate the effects of moonlight and mating activity on night ranging in this species, as well as to evaluate whether L. catta in Madagascar show night ranging similar to L. catta on SCI. These data raise the possibility that L. catta may be cathemeral, with an activity pattern fluctuating between diurnality and cathemerality in accordance with shifts in environmental conditions.     

Can captive-bred American bullfrogs learn to avoid a model avian predator?

Animals that are isolated from their natural predators may lose the ability to express antipredator behavior. The aim of this study was to test whether it would be possible to train captive-bred North American bullfrogs (Rana catesbeiana) to avoid a model avian predator and to measure their behavioral responses to this predator. We used 18 animals divided into two groups, trained (N?=?6) and control (N?=?12); these individuals were from a line that has been bred in captivity for at least 20 generations without predator contact. The trained group was exposed, individually, to 20 sequential antipredator training sessions, during which the presence of a model avian predator was paired with an aversive stimulus. The control group was exposed, individually, once only to the same model avian predator, but without the association of the aversive stimulus. Both groups were observed for 10 min after the presentation of the avian predator, during which their behavior was recorded using instantaneous recording of behavior. The results showed that, after only two training sessions, the trained bullfrogs started to express proper antipredator behavior: diving to the bottom of the tank, lying still, and eventually, learning to cover themselves in substrate (mud). However, continued training sessions provoked a varied response to antipredator training, which was undesirable as the effectiveness of their antipredator response varied. This study has shown that captive-bred bullfrogs were capable of learning antipredator behavior, despite having been bred for many generations in captivity with no predator contact.     

Wet and dry season diets of the Endangered Lemur catta (ring‐tailed lemur) in two mountainous rocky outcrop forest fragments in south‐central Madagascar

Lemur catta's ability to consume a wide variety of plant foods is a key to this species' survival in a time of ecological crisis across its geographic range. We examined seasonal diet variability of L. catta groups inhabiting two rocky outcrop fragments in south‐central Madagascar: Anja Reserve and Tsaranoro Valley forest. Leaves and fruit of Melia azedarach were a keystone resource for Anja lemurs in wet and dry seasons. At Tsaranoro, L. catta relied on M. azedarach and Ficus spp. in dry season, but during the wet season, neither was a dominant food resource. Top food species at both sites differed markedly from those consumed by L. catta in other habitats. At Tsaranoro, a greater proportion of lemurs engaged in feeding during the dry season compared with wet season. We attribute this to resource scarcity during dry season, when greater feeding effort is needed to maintain energy requirements. Because M. azedarach is ubiquitous throughout Anja Reserve, producing fruit and leaves year‐round, Anja lemurs can meet energy requirements with little seasonal adjustment in feeding activity. L. catta's IUCN status has been upgraded to Endangered, thus, greater insight into its diet flexibility and ability to survive on introduced plant species, can inform conservation plans in remaining wild habitats and ex situ programs.     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Multimodal signaling in wild Lemur catta: Economic design and territorial function of urine marking

Urine marking has been neglected in prosimian primates. Captive studies showed that the Malagasy prosimian Lemur catta scent marks with urine, as well as via specialized depositions. L. catta urine mark, a multimodal signal, differs from simple urination in terms of different design features, including tail configuration: the tail is held up during marking (UT‐up) and down during urination (UT‐down). We explore economy and function of UT‐up in the female dominant L. catta. We collected 240 h of observations on one group at Berenty (south Madagascar) during the nonmating period via all occurrences sampling. We gathered behavioral bouts/contexts (marking, traveling, feeding, resting, and fights) and recorded 191 UT‐ups and 79 UT‐downs. Via Global Positioning System we established the location of the places frequented i) by extragroup individuals and ii) by group members, in this case recording also behavioral context and time spent in each place. We found that L. catta UT‐up is not an artifact of captivity. Moreover, UT‐up in the nonmating period plays a role in territorial defense, which is mostly performed by females in L. catta society. Female UT‐ups were the most investigated and UT‐ups were performed/investigated more by females. Finally, signal use is parsimonious, in that urine is economically placed where and when detection probability by competitors is higher. UT‐ups were performed in places most frequented by extragroup individuals and in presence of extragroup competitors (nonrandom topography and timing). In conclusion, we suggest that UT‐up is an economical signal with a primarily territorial function. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

Predator Generalization Decreases the Effect of Introduced Predators in the San Marcos Salamander,Eurycea nana

The introduction of novel predators into an environment can have detrimental consequences on prey species, especially if these species lack the ability to recognize these predators. One such species that may be negatively affected by introduced predators is the federally threatened San Marcos salamander (Eurycea nana). Previous research found that predator‐naïve (captive‐hatched) salamanders showed decreased activity in response to the chemical cues of both a native fish predator (Micropterus salmoides) and an introduced fish predator (Lepomis auritus), but not to a non‐predatory fish (Gambusia geiseri). We tested the hypothesis that E. nana recognized the introduced Lepomis (and other non‐native Lepomis) because they share chemical cues with other native congeneric Lepomis predators in the San Marcos River. We examined the antipredator response of predator‐naïve E. nana to chemical cues from (1) a sympatric native sunfish (Lepomis cyanellus; Perciformes: Centrarchidae); (2) a sympatric introduced sunfish (L. auritus); (3) an allopatric sunfish (Lepomis gibbosus); (4) a sympatric non‐native, non‐centrarchid cichlid (Herichthys cyanoguttatum; Perciformes: Cichlidae); and (5) a blank water control to determine whether individuals make generalizations about novel predators within a genus and across a family. Exposure to chemical cues from all fish predator treatments caused a reduction in salamander activity (antipredator response). Additionally, there were no differences in the antipredator responses to each predatory fish treatment. The similar responses to all sunfish treatments indicate that E. nana shows predator generalization in response to novel predators that are similar to recognized predators. Additionally, the antipredator response to H. cyanoguttatum indicates that predator generalization can occur among perciform families.     

Operant conditioning of scratching in lemurs

An adult femaleLemur catta and an adult femaleEulemur fulvus were given edible rewards for scratching. Both subjects learned to scratch in order to obtain the rewards, showed diminished rates of scratching during periods of extinction, and learned to scratch preferentially with one foot when required. TheLemur catta subject was more responsive to the changing experimental conditions than theEulemur fulvus. The conditionability of scratching in primates does not appear to be directly related to the widespread occurrence of scratching in simian social contexts.     

PREDATOR‐DRIVEN TRAIT DIVERSIFICATION IN A DRAGONFLY GENUS: COVARIATION IN BEHAVIORAL AND MORPHOLOGICAL ANTIPREDATOR DEFENSE

Proof for predation as an agent shaping evolutionary trait diversification is accumulating, however, our understanding how multiple antipredator traits covary due to phenotypic differentiation is still scarce. Species of the dragonfly genus Leucorrhinia underwent shifts from lakes with fish as top predators to fishless lakes with large dragonfly predators. This move to fishless lakes was accompanied by a partial loss and reduction of larval spines. Here, we show that Leucorrhinia also reduced burst swimming speed and its associated energy fuelling machinery, arginine kinase activity, when invading fishless lakes. This results in patterns of positive phylogenetic trait covariation between behavioral and morphological antipredator defense (trait cospecialization) and between behavioral antipredator defense and physiological machinery (trait codependence). Across species patterns of trait covariation between spine status, burst swimming speed and arginine kinase activity also matched findings within the phenotypically plastic L. dubia. Our results highlight the importance of predation as a factor affecting patterns of multiple trait covariation during phenotypic diversification.     

Characterization of 21 microsatellite marker loci in the ring-tailed lemur (<Emphasis Type="Italic">Lemur catta</Emphasis>)

Ring-tailed lemur (Lemur catta) is the only species in the Genus Lemur, distributed in the deciduous and spiny forests of southwestern Madagascar. This species is listed as endangered due to the loss and fragmentation of its natural habitat, a consequence of deforestation. Twenty-one nuclear microsatellite loci were isolated from a genomic DNA derived from a free-ranging ring-tailed lemur population from the Tsimanampetsotsa National Park, Madagascar. We report various parameter estimates and measures to establish the utility of this marker suite as screened among individuals this single forest fragment.     

Antipredator Tactics of Amphibious Sea-Snakes (Serpentes, Laticaudidae)

Because the antipredator behavior that an animal displays depends upon the context in which it encounters the predator, apparent interspecific differences in antipredator tactics may result from ecological rather than behavioral differences among taxa. We approached 127 free-ranging laticaudid sea-snakes on small islands in Noumea Lagoon, New Caledonia, prodded the animals midbody, and recorded their responses. One species (Laticauda colubrina) usually remained immobile (relying on crypsis) whereas another (L. laticaudata) generally fled. However, multivariate analysis shows that the two species actually responded in very similar ways to any given stimulus; the species differed overall because colubrina was generally encountered on land during the day whereas laticaudata was more often encountered in the ocean at night. Thus, apparent interspecific differences in antipredator responses were secondary consequences of interspecific differences in the times and places that predators were encountered. Snakes were more likely to flee rather than remain immobile when rapid locomotion was possible (i.e. juveniles rather than adults; in water rather than on land) and pursuit by a predator was difficult (i.e. at night rather than during the day). These patterns suggest that snakes adjust their antipredator tactics in ways that maximize the chances of surviving the encounter, although the remarkable docility of these highly venomous snakes remains puzzling.     

Mother Cottonmouths (Agkistrodon piscivorus) Alter Their Antipredator Behavior in the Presence of Neonates

Neonate‐directed care is rare in non‐avian reptiles, but female pitvipers attend their young for a period of time after birth. One of the primary functions of parental care is the protection of offspring from predators, and parents of diverse taxa are able to modulate their antipredator behavior in the presence of offspring. To test the hypothesis that the antipredator behavior of post‐parturient pitvipers is altered during neonate attendance, we conducted behavioral trials on female cottonmouths (Agkistrodon piscivorus) in which we measured female response to a simulated predator encounter. Cottonmouths were divided into three treatment groups: (1) post‐parturient, attending neonates; (2) post‐parturient, not attending neonates; and (3) non‐reproductive. All females were subjected to a second trial approximately 3 wk later, when females in Group 1 were no longer attending neonates. When mothers were attending offspring, they were more hesitant to engage the predator and exhibited more warning than aggressive behaviors once they did, relative to non‐attending and non‐reproductive females. When these same mothers were no longer attending offspring, they significantly increased their antipredator behavior by engaging the predator quickly and displaying more aggressive than warning behaviors. This change in behavior was not observed in post‐parturient females who did not have neonates present during either trial, nor was it observed in non‐reproductive females, indicating that the presence of neonates directly affected the antipredator behavior of attending females. We discuss hypotheses concerning the possible adaptive value of reduced antipredator behavior in female pitvipers attending neonates.     

Reactions to Potential Predators in Captive-Born Marmosets (Callithrix penicillata)

We describe the behavioral repertoire of captive-born black tufted-eared marmosets (Callithrix penicillata) elicited by brief exposures to three potential mounted taxidermized predators (caracara hawk, Polyborus plancus; rattlesnake, Crotalus durissus; oncilla, Leopardus tigrina), and a stuffed toy. For each of the four stimuli, we submitted the subjects to a 9-min trial divided into three consecutive intervals: a 4-min pre-exposure baseline observation, a 1-min stimulus exposure, and a 4-min postexposure observation period. We positioned stimuli in front of each subject's home cage, and video-taped trials for behavioral analysis. During exposures to the potential taxidermized predators, we heard tsik-tsik vocalization and alarm behavior. After exposures, only the cat induced these reactions. All stimuli elicited observational reaction, albeit only during exposure intervals. Further comparisons between the three trial intervals indicated a decrease in the time spent in proximity to the cat during exposures, while an increase in proximity occurred when subjects were exposed to either the hawk or snake for the same period. Taken together, the behavioral responses during and after exposures to the taxidermized oncilla suggest that this stimulus is capable of inducing strong and persistent emotional reactions in Callithrix penicillata.     

The ranging behavior of Lemur catta in the region of Cap Sainte‐Marie,Madagascar

Large home ranges and extreme flexibility in ranging behaviors characterize most subarid dwelling haplorhines. However, the most comparable extant strepsirhine, Lemur catta, is characterized as having small home ranges with consistent boundaries. Since ranging studies on this species have been limited to gallery forest habitat, the author's goal is to identify ecological factors that affect range use of L. catta in one of the most resource‐limited environments of its distribution. To conduct this study, ranging and behavioral data were collected on two nonoverlapping groups through all‐day follows in the semidesert scrub environment of Cap Sainte‐Marie (CSM), Madagascar. Data were collected from August 2007 through July 2008. Home range areas and day range lengths were generated using ArcGIS® 9.3. Other variables measured were habitat composition, diet richness, daily activity, and microclimate. Home range areas of CSM L. catta were very large relative to those of gallery forest L. catta, and there was great monthly variation. In contrast, day range lengths at CSM were either smaller than or approximated the size of comparative gallery forest groups. Temperature, sunning, and diet richness were associated with day range length for one but not for both groups and appear to be related to energy management needs. Based on these findings, the author suggests that L. catta is capable of extensive behavioral and ranging flexibility in the extremes of its environment. However, physiological constraints impose limitations that can interfere with its ability to adapt to even seemingly minor variations in microclimate and habitat structure within the same site. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Do predators limit the abundance of alternative prey? Experiments with vole‐eating avian and mammalian predators

Predation has been invoked as a factor synchronizing the population oscillations of sympatric prey species, either because predators kill prey unselectively (the Shared Predation Hypothesis; hereafter SPH), or because predators switch to alternative prey after a density decline in their main prey (the Alternative Prey Hypothesis; APH). A basic assumption of the APH is that the impact of predators on alternative prey depends more on the density of main prey than on the predator/alternative prey ratio. Both SPH and APH assume that the impact of predators on alternative prey is at least periodically strong enough to depress prey populations. To examine these assumptions, we utilized data from replicated field experiments in large areas where we reduced the breeding densities of avian predators during three years and the numbers of least weasels (Mustela nivalis) in two years when vole populations declined. In addition, we reduced the breeding densities of avian predators in two years when vole populations were high. The reduction of least weasels increased the abundance of their alternative prey, small birds breeding on the ground, but did not affect the abundance of common shrews (Sorex araneus). In years when vole populations declined, the reduction of avian predators increased the abundance of their alternative prey, common shrews and small birds. Therefore, vole‐eating predators do at least periodically depress the abundance of their alternative prey. At high vole densities, the reduction of avian predators did not increase the abundance of common shrews, although the ratio of avian predators to alternative prey was similar to years when vole populations declined, which supported APH. In contrast, the abundance of small birds increased after the reduction of avian predators also at high vole densities, which supported SPH. The manipulations had no obvious effect on the number of game birds, which are only occasionally killed by these small‐sized predators. We conclude that in communities where most predators are small or specialize on a single prey type, the synchronizing impact of predation is restricted to a few similar‐sized species.     

Isolation from mammalian predators differentially affects two congeners

Evolutionary isolation from predators can profoundly influencethe morphology, physiology, and behavior of prey, but littleis known about how species respond to the loss of only someof their predators. We studied antipredator behavior of tammarwallabies (Macropus eugenii) and western gray kangaroos (Macropusfuliginosus) on Kangaroo Island (KI), South Australia, andat Tutanning Nature Reserve on the mainland of western Australia.Both species on KI have been isolated from native mammalian predators for several thousand years. On KI, wallabies (becauseof their size) are vulnerable to diurnal aerial predators.In contrast, on the mainland both species have been exposedcontinuously to native and introduced mammalian and avian predators.At both locations, wallabies modified the amount of time they allocated to vigilance and foraging in response to group size,whereas kangaroos did so only at the higher risk Tutanningsite. Both species modified overall time budgets (they werewarier at the higher risk site), and both species modifiedspace-use patterns as a function of risk. At the higher risk site, tammars were closer to cover, whereas kangaroos were,on average, farther from cover. We hypothesize that the presenceof a single predator, even if it is active at a different timeof day, may profoundly affect the way a species responds tothe loss of other predators by maintaining certain antipredatorbehaviors. Such an effect of ancestral predators may be expected as long as species encounter some predators.     

Face to face with the woolly spider monkey. Review of faces in the forest: The Endangered Muriqui Monkeys of Brazil,by Karen B. Strier. New York,Oxford University Press,Inc., 1992, 138 pp, $49.50

During an intertroop encounter, an infanticide was observed in a population of ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. The killer was a male that had not been previously observed to mate with any females in the infant's troop. This observation, combined with other observations of infanticidal behavior by males at Berenty Reserve and the Duke University Primate Center, is consistent with the hypothesis that infanticide is a reproductive tactic for some male ringtailed lemurs. © 1994 Wiley-Liss, Inc.     

Body mass of wild ring-tailed lemurs in Berenty Reserve,Madagascar, with reference to tick infestation: a preliminary analysis

In 1999, we measured the body mass of 101 wild ring-tailed lemurs (Lemur catta) inhabiting the Berenty Reserve, Madagascar. In addition, we counted the number of ticks [Haemaphysalis (Rhipistoma) lemuris Hoogstraal, 1953] infesting their facial skin and external auditory meatuses. For both males and females, the body mass appeared to increase until the age of 3 years. With the apparent exception of infants, there were no sexual differences in body mass. Within a group, higher-ranked adult males tended to be heavier than lower-ranked males. In contrast, there was no consistent correlation between the body mass of females and their ranks. Among the study groups, there was a small difference in body mass and significant difference in the number of ticks infesting the facial skin and external auditory meatuses. In particular, lemurs of a group who inhabited an area of gallery forest in the study area exhibited the smallest values of body mass and were severely infested with ticks. Such group variations were not consistently correlated with the reproductive parameters of the study groups. In three groups moderately infested with ticks, ticks infested adult males and subadults more heavily than adult females, juveniles, and infants.