Mirror-Directed Social Behaviors of Garnett's Greater Bush Baby (Otolemur garnettii)

Many diurnal anthropoid species direct social behaviors toward their own mirror-image as though viewing a conspecific. To determine whether a nocturnal prosimian species would behave similarly, we videotaped social responses of 45 Garnett's greater bush babies (Otolemur garnettii) observing mirror-images for the first time, scored them for frequency and duration, and compared them with the same behaviors directed elsewhere in the test apparatus. Males scentmarked more than females did, principally with the hindfoot, and most when in immediate proximity to the mirror. Bush babies displayed bipedal posture and threat gestures when oriented directly toward a mirror from a near position. Orientation toward the mirror also increased the frequency of arched-back postures; however, this behavior was not contingent on proximity to the mirror or visibility of the mirror-image. The differential expression of specific behaviors toward mirror-images by male and female bush babies supports the view that this nocturnal prosimian, thought to be dependent on olfaction and audition for communication, is capable of specific recognition by visual cues alone.     

Function of Head-Cocking in Garnett's Greater Bush Baby (Otolemur garnettii)

Head-cocking is rotation of the head about the rostrocaudal axis with a fixed direction of orientation. The behavior is a response to either visual or auditory stimuli according to species. Although head-cocking is prevalent in small primates, its functional significance is unclear. We studied head-cocking in response to a variety of novel visual and acoustic stimuli in Garnett's greater bush babies (Otolemur garnettii). We systematically varied stimulus type (animate vs. inanimate image) and mode of presentation (NON-VIDEO vs. VIDEO) to assess their effects on the head-cocking response. A higher incidence of head-cocking occurred with novel animal images and for NON-VIDEO presentations. Acoustic stimuli suppressed rather than facilitated head-cocking. Juveniles head-cocked much more than adults did. Clearly head-cocking in Otolemur garnettii is primarily involved in visual rather than auditory function. It does not serve simple sensory/perceptual functions such as depth perception or acuity. Instead, in consideration of the importance of novelty to the elicitation of the behavior, the higher incidence in younger animals, and the structure of the visual system, we propose that head-cocking is a motor strategy to encode the parameters of novel images in the process of form learning.     

Multiple measures of laterality in Garnett's bushbaby (Otolemur garnettii)

Behavioral laterality, a common measure of hemispheric specialization of the brain, has been examined in multiple tasks across several species of prosimian primates; however, there is inconsistency among findings between and within species that leaves many questions about laterality unanswered. Most studies have employed few measures of laterality, most commonly handedness. This study examined multiple measures of laterality within subjects in 17 captive‐born Garnett's bushbabies (Otolemur garnettii) to assess the consistency of lateralized behaviors and to examine possible influences such as age, posture, novelty, and arousal to elucidate the relations between direction and strength of laterality. We measured reaching, turning bias, scent marking, tail wrapping, leading foot, side‐of‐mouth preference, and hand use in prey capture. Because autonomic arousal has been invoked as a determinant of strength of lateralization, we included multiple tasks that would allow us to test this hypothesis. All subjects were significantly lateralized on simple reaching tasks (P<0.01) and tail wrapping (P<0.01). Moreover, the number of animals lateralized on turning (P<0.01), leading limb (P<0.05), mouth use (P<0.01), and prey capture (P<0.01) was greater than would be expected by chance alone. There was consistency in the strength and direction of hand biases across different postures. Tasks requiring hand use were more strongly lateralized than tasks not involving hand use (P<0.001). The data do not support the assumption that arousal (as subjectively categorized) or novelty strengthens lateralized responding. The results of this study are discussed in terms of the effects of arousal, posture, and age on lateralized behavior. Am. J. Primatol. 72:206–216, 2010. © 2009 Wiley‐Liss, Inc.     

Three-dimensional analysis of mandibular morphology in Otolemur

Euclidean distance matrix analysis (EDMA) of three-dimensional data is used here to examine mandibular morphology between two species of galagos. Otolemur crassicaudatus consumes primarily exudates, while O. garnettii is more frugivorous. Acquisition of exudates involves either gouging or scraping tree bark, and may involve different forces at the mandible than incising fruits. Previous studies of mandibular morphology in exudate-feeding primates produced mixed results, some suggesting that morphological specializations reflect adaptations for greater force at the anterior dentition, while others suggest specializations for producing a large gape. This study addresses these controversies by testing predictions associated with O. crassicaudatus generating greater force at the anterior dentition or producing a larger gape relative to O. garnettii. In addition, this study tests predictions associated with specializations of the anterior dentition in O. crassicaudatus as related to exudate-feeding. Crania and mandibles from 28 O. crassicaudatus and 17 O. garnettii were digitized in three dimensions, using 18 landmarks that summarize the shape of the jaw. Two-dimensional measurements were taken to assess incisor robusticity. All three-dimensional data were analyzed using EDMA, and bootstrap tests were executed to identify specific interlandmark differences that were driving any significant (P < 0.05) overall shape differences. Two-dimensional data were analyzed using Student's t-test for independent measures. Results revealed that there was a significant shape difference in mandibles between species, and that mandibles of O. crassicaudatus showed higher condyles, longer mandibles, decreased incisor procumbency, and greater incisor robusticity relative to O. garnettii. It is suggested that the results of the present study reflect adaptations for scraping in O. crassicaudatus rather than gouging.     

Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.)

The functional morphology of the primate craniomandibular complex and temporomandibular joint (TMJ) components is frequently discussed in terms of gross skeletal structure. At the histomorphologic level, however, the TMJ has only been studied in Old World anthropoids. The present study is designed to describe the microanatomy of the condylar cartilage of the TMJ in two closely related species of greater galago: the exudativorous Otolemur crassicaudatus and the frugivorous O. garnettii. TMJs with intact joint capsules were harvested from adult, cadaveric specimens of these species (four O. crassicaudatus and five O. garnettii). The samples were decalcified, processed for paraffin sectioning, and sectioned at 10-18 microm in the coronal plane. The samples were then stained with hematoxylin/eosin, Gomori trichrome, and Alcian blue, and examined with a photomicroscope. Generally, condylar cartilage in O. crassicaudatus was thickest both laterally and centrally, while O. garnettii had the relatively thickest cartilage laterally. Both species displayed a superficial articular zone, a middle proliferative zone, and a deeply located hypertrophic zone in the condylar cartilage. O. crassicaudatus typically had the greatest cell density in each of these zones. In addition, O. crassicaudatus had focal concentrations of Alcian blue laterally and centrally, while O. garnettii had the greatest reactivity in the central portion only. These results suggest that O. crassicaudatus may be specialized to resist greater compressive force at the TMJ condylar cartilage in specific regions of the mandibular condyle.     

Social organization of Galagos in Kenyan coastal forests: II. Galago garnettii

The social organization of Galago garnettii was studied for the first time and the study included data from two different sites in the coastal forests of Kenya. A combination of mark-recapture and radio-tracking techniques was used to investigate patterns of inter- and intrasexual home range overlap. Patterns of range use were established by radio tracking focal individuals. Adult females of different ages shared highly overlapping ranges, while like-aged females showed little range overlap. Females matured and had their first infants in their natal ranges. Adult males' ranges were larger than those of females and overlapped them extensively. Resident adult males showed little range overlap with each other, unless they were of different ages. Turnover of males was frequent in both populations. Males probably dispersed from their natal ranges. Adults rarely slept together. The social organization of G. garnettii is relatively similar to that of the closely related G. crassicaudatus of southern Africa but contrasts with that of its sympatric congener, G. zanzibaricus. The differences and similarities between these three species are discussed in relation to diet and body size.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Chimpanzees Differentially Produce Novel Vocalizations to Capture the Attention of a Human

Chimpanzees produce numerous species-atypical signals when raised in captivity. Here we report contextual elements of the use of two captivity-specific vocal signals, the "raspberry" and the extended grunt. Results demonstrate that these vocalizations are not elicited by the presence of food; rather the data suggest that these vocalizations function as attention-getting signals. These findings demonstrate a heretofore underappreciated category of animal signals: novel signals invented in novel environmental circumstances. The invention and use of species-atypical signals, considered in relation to group differences in signaling repertoires in apes in their natural habitats, may index a generative capacity in these hominoid species without obvious corollary in other primate species.     

Intraspecific Variation in the Vocalizations and Hand Pad Morphology of Southern Lesser Bush Babies (Galago moholi): A Comparison with G. senegalensis

Previous studies have shown the taxonomic value of vocal repertoires and hand (volar) pad characteristics in the classification of cryptic nocturnal primates such as bush babies. However, no study included quantitative comparisons within the geographical range of any one species. We investigated levels of intraspecific variation in calls and hand pad characteristics of the southern lesser bush baby (Galago moholi), using the northern lesser bush baby (Galago senegalensis) for interspecific comparisons. Examination of calls recorded from different regions along a transect of 1500 km across southern Africa revealed low levels of intraspecific variation in Galago moholi, whereas comparisons with homologous call-types in G. senegalensis revealed them to be significantly different. Volar pad measurements across the ranges of both species also showed low levels of intraspecific variation and relatively high interspecific variation. These findings demonstrate that vocal and volar pad characteristics can be used as consistent measures of difference between species that look almost identical. These methods provide a practical means of distinguishing between cryptic species, whether in the field, in captivity, or, in the case of volar pads, of preserved specimens.     

Mitochondrial Sequences as Indicators of Genetic Classification in Bush Babies

Systematic relationships among the African bush babies are not well understood. Various generic designations are currently in use. Some authors refer all species to a single genus (Galago), while others recognize 4 genera. Phylogenetic reconstructions based on morphology, karyology, allozymes and vocal repertoires have generated inconsistent hypotheses of relationship. We analyzed partial sequences of three mitochondrial genes (270 bp from cytochrome b, 387 bp from 12S rRNA, and 241 bp from 16S rRNA, total 898 bp) to resolve some uncertainties. We sampled taxa from each of three genera: Galagoides alleni, G. demidoff and G. zanzibaricus; Galago senegalensis, G. gallarum and G. moholi; and Otolemur crassicaudatus and O. garnettii. Outgroup taxa were Asian lorises: Nycticebus coucang and Loris tardigradus. We analyzed sequences separately and in combination, and modeled phylogenies using maximum parsimony, weighted parsimony, neighbor-joining and maximum-likelihood. We obtained some variation in phylogenetic inference depending on sequence and analytical method, but the results also gave strong phylogenetic signals. The lesser bush babies invariably formed a clade, showing evidence of very recent radiation. The greater bush babies also formed a clade, marked by somewhat greater interspecific genetic distances, which was allied with Galagoides alleni in most instances. Galagoides demidoff and G. zanzibaricus are not closely related, though both diverged early in the history of the group. A genus comprising Galagoides alleni, G. demidoff and G. zanzibaricus is not supported by our data. The most likely alliance for Galagoides alleni is within the genus Otolemur. Of the three partial sequences employed in the study, 16S rRNA gave the most consistent results, while cytochrome b was least informative.     

Chuck Vocalizations of Wild Female Squirrel Monkeys (Saimiri sciureus) Contain Information on Caller Identity and Foraging Activity

Analysis of the acoustic signal of the chuck vocalizations of adult female squirrel monkeys (Saimiri sciureus) in Parque Nacional de Manu, Peru, revealed consistent differences within and between individuals. We quantified four peak frequency parameters: (a) the peak frequency of single chucks, (b) the first and (c) the second peak frequencies of double chucks, and (d) the peak difference: the difference between the first and the second double chuck peaks. One-way ANOVAs and a posteriori comparisons of these variables revealed that each distinguished more than 70% of all possible pairs of females. When all double chuck measures were included in a discriminant analysis, 57% of double chucks were correctly assigned to the caller. Another category of information potentially encoded in the acoustic structure of chuck vocalizations is foraging activity. When the chucks of squirrel monkeys during foraging and nonforaging activities were compared, the single chuck peak frequency, and the first peak frequency and the peak difference of double chucks, were significantly reduced during foraging contexts. Previously Boinski and Mitchell (1992) concluded that chucks facilitate group cohesion among widely dispersed troop members by providing information of the location of callers; the rate of chucks produced by an adult female increases as she becomes more spatially and visually separated from other adult females. The additional information potentially conveyed by chucks on caller identity and foraging activity documented in these new analyses further emphasizes the role chucks serve to enhance group coordination and cohesion.     

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.     

Sex differences in the acquisition of communicative competence by pigtail macaques (Macaca nemestrina)

Previous study of captive pigtail monkeys (Macaca nemestrina) revealed that victims of an attack by a group member employed one of four acoustically different recruitment calls (Gouzoules&Gouzoules: Animal Behaviour 37:383–401, 1989). The calls appear to provide allies with information pertinent to decisions about fight intervention. Each call was associated with an agonistic context distinguished by the relative rank of the opponent and the severity of the attack. Monkeys younger than 3 years of age were significantly less likely to use a contextually appropriate call than were older animals and their calls tended to be acoustically less like the prototype for a given context. Analyses reported on here revealed that, among juveniles, females were more proficient than males in both the proper contextual use and the production of these calls. These findings suggest parallels with human sex differences in the development of communicative competence. The evolutionary origins for these sex differences in macaque vocal development may be based in the different life history patterns males and females exhibit.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Geographic variation in the calls of wild chimpanzees: A reassessment

Male chimpanzees produce a species‐typical call, the pant hoot, to communicate to conspecifics over long‐distances. Calls given by males from the well‐known Gombe and Mahale populations typically consist of four different phases: an introduction, build‐up, climax, and let‐down. Recent observations suggest that chimpanzees living in the Kibale National Park, Uganda, consistently give calls that lack a build‐up and are thus qualitatively distinguishable acoustically from those made by other East African conspecifics. We analyzed additional recordings from Mahale and Kibale to re‐examine geographic variation in chimpanzee calls. Results indicate that males from both sites produce pant hoots containing all four parts of the call. Calls made by chimpanzees from the two populations, however, differ in quantitative acoustic measures. Specifically, males at Kibale initiate their calls with significantly longer elements and build‐up over briefer periods at slower rates than individuals from Mahale. Kibale males also deliver acoustically less variable calls than chimpanzees at Mahale. Although climax elements do not differ between populations in any single acoustic feature, discriminant function analysis reveals that acoustic variables can be used in combination to assign calls to the correct population at rates higher than that expected by chance. Ecological factors related to differences in habitat acoustics, the sound environment of the local biota, and body size are likely to account for these observed macrogeographic variations in chimpanzee calls. Am. J. Primatol. 47:133–151, 1999. © 1999 Wiley‐Liss, Inc.     

The anatomy of vocal divergence in North American Elk and European red deer

Loud and frequent vocalizations play an important role in courtship behavior in Cervus species. European red deer (Cervus elaphus) produce low‐pitched calls, whereas North American elk (Cervus canadensis) produce high‐pitched calls, which is remarkable for one of the biggest land mammals. Both species engage their vocal organs in elaborate maneuvers but the precise mechanism is unknown. Vocal organs were compared by macroscopic and microscopic dissection. The larynx is sexually dimorphic in red deer but not in elk. The laryngeal lumen is more constricted in elk, and narrows further during ontogeny. Several elements of the hyoid skeleton and two of four vocal tract segments are longer in red deer than in elk allowing greater vocal tract expansion and elongation. We conclude that elk submit the larynx and vocal tract to much higher tension than red deer, whereby, enormously stressed vocal folds of reduced effective length create a high resistance glottal source. The narrow, high impedance laryngeal vestibulum matches glottal and vocal tract impedance allowing maximum power transfer. In red deer longer and relaxed vocal folds create a less resistant glottal source and a wider vestibulum matches the low glottal impedance to the vocal tract, thereby also ensuring maximum power transfer. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Evolution of Acoustic Communication Signals of Mammals: Friendly Close-Range Vocalizations in Felidae (Carnivora)

The distribution of the three friendly close-range vocalization types known in the Felidae was plotted on a recently published phylogeny of the cat family (Felidae) based on sequence comparisons of two mitochondrial DNA genes and other molecular and biochemical characters, with extrapolated divergence ages of its various lineages. It was found to be congruent with this phylogeny. One of the sound types is likely to be present in 30 species of the family (documented in 22 so far), another is present in 4, and the third in 2 species only; these sound types represent a phylogenetic transformation series. The latter two vocalization types also differ considerably from the first in the mode of sound production. From this, evolutionary conservatism over a long epoch for the one widespread vocalization type can be inferred, and less conservatism in the type present in four species, while the emergence of the least common type is evidence of relatively considerable and rapid evolutionary change. Thus, acoustic communication signals in a group of taxa can evolve at considerably different rates, and for a specific character this rate can differ between different lineages of that group. The ultimate causes of the evolutionary stability or of the subsequent relatively rapid change in sound structure and mode of sound production in these felid vocalizations are unknown.     

Temporal parameters of male—female sound communication in Leptophyes punctatissima

ABSTRACT. Quantitative information is presented about acoustic communication between the sexes of the speckled bush cricket Leptophyes punctatissima Bosc (Orthoptera: Tettigoniidae). The male song elicits an acoustic response from a receptive female with a net delay (excluding the travelling time of the sound) of about 25 ms depending upon ambient temperature. Only when the female responses fall within the narrow temporal window between 20 and 50 ms after the onset of his song does the male perform phonotaxis. The precise timing of this duet is described, and its advantages and disadvantages are discussed.