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Comparative functional analysis of skull morphology of tree-gouging primates.

Many primates habitually feed on tree exudates such as gums and saps. Among these exudate feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate flow by biting into trees with their anterior dentition. We define this behavior as gouging. Beyond the recent publication by Dumont ([1997] Am J Phys Anthropol 102:187-202), there have been few attempts to address whether any aspect of skull form in gouging primates relates to this specialized feeding behavior. However, many researchers have proposed that tree gouging results in larger bite force, larger internal skull loads, and larger jaw gapes in comparison to other chewing and biting behaviors. If true, then we might expect primate gougers to exhibit skull modifications that provide increased abilities to produce bite forces at the incisors, withstand loads in the skull, and/or generate large gapes for gouging. We develop 13 morphological predictions based on the expectation that gouging involves relatively large jaw forces and/or jaw gapes. We compare skull shapes for P. furcifer to five cheirogaleid taxa, E. elegantulus to six galagid species, and C. jacchus to two tamarin species, so as to assess whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely, these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative to the toothrow at a given mandibular length in comparison with closely related, nongouging taxa. Lowering the height of the condyle relative to the mandibular toothrow should reduce the stretching of the masseters and medial pterygoids during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the lower incisors will follow a more vertical trajectory during both jaw opening and closing. We predict, based on these findings, that tree-gouging primates do not generate unusually large forces, but that they do use relatively large gapes during gouging. Of course, in vivo data on jaw forces and jaw gapes are required to reliably assess skull functions during gouging.

Anatomy, Comparative↗

Ontogenetic characteristics of the vomeronasal organ in Saguinus geoffroyi and Leontopithecus rosalia, with comparisons to other primates.

It has been suggested that the variability of the primate vomeronasal organ (VNO) may be greater than previously thought, especially among New World monkeys. It is not clear to what extent VNO variation reflects ontogenetic, functional, or phylogenetic differences among primates. The present study investigated VNO anatomy in an ontogenetic series of two genera of callitrichid primates, in order to assess recent attempts to develop VNO character states and to examine the evidence for VNO functionality at different life stages. A sample of six Leontopithecus rosalia, one L. chrysomelas, and six Saguinus geoffroyi was serially sectioned and stained using various methods. Two adult Callithrix jacchus were also sectioned for comparative purposes. The VNO of each primate was examined by light microscopy along its entire rostrocaudal extent. VNOs of the tamarins were described to determine whether they fit into 1 of 3 character states recently attributed to various New World monkeys. At birth, the two species of tamarins differed in the nature of communication between the VNO and nasopalatine duct (NPD). Two of 3 neonatal S. geoffroyi exhibited a fused VNO duct in a more dorsal position (adjacent to the nasal cavity) compared to that of L. rosalia. The VNO duct communicated with the NPD and was patent in neonatal L. rosalia. Both species appeared to have an age-related increase in the amount of sensory epithelium in the VNO. Subadult L. rosalia had caudal regions of the VNO that were exceptionally well-developed, similar to those of strepsirhine primates. Compared to subadults, all adult callitrichids appeared to have more ventral communications of the VNO duct directly into the NPD. Adult S. geoffroyi and L. chrysomelas both had VNO sensory epithelium separated by multiple patches of nonsensory epithelium. This contrasted with the VNOs of C. jacchus, which had a nearly continuous distribution of receptors on all surfaces of the VNO. The findings indicate that tamarins have delayed maturation of the VNO epithelium, and that some species have little or no perinatal function. These results also suggest that ontogenetic changes in craniofacial form may alter the position of the VNO in tamarins. The present study supports the use of at least two character states to categorize the VNO of various callitrichids, but it is suggested that one of these, previously called "reduced sensory epithelium" should be instead termed "interrupted sensory epithelium." The distribution of VNO sensory epithelium does not appear to reflect phylogenetic influences; it is more likely a functional characteristic that varies throughout postnatal life. Therefore, this chemosensory system has a high degree of plasticity relating to age and function, which in some instances can confound the use of characteristics as phylogenetic traits. Further study is needed to quantify VNO receptors in various species to determine if functional differences exist and if some species have more precocious VNO function than others.

Adaptation, Biological↗

New technique for studying reaction forces during primate behaviors on vertical substrates.

Recording reaction forces from primates during behaviors on vertical substrates, such as leaping, climbing, or biting trees, typically requires the design and construction of customized recording devices or mounting commercially available force platforms in a vertical position. The technical difficulties imposed by either option have hindered in vivo research on the kinetics of primate behaviors on vertical substrates. We describe a simple, inexpensive apparatus for recording forces from primate behaviors on vertical substrates. The apparatus includes an instrumented beam fastened directly to a horizontal force platform and a surrounding vertical substrate that does not contact the instrumented beam or platform. The contact piece at the end of the instrumented beam is positioned flush with the noninstrumented vertical substrate, and reaction forces elicited on this instrumented section are directed to the force platform. Because most of the vertical substrate is not instrumented, we can isolate and record forces from a single limb or jaw during a behavior. Biewener and Full ([1992] Biomechanics Structures and Positions: A Practical Approach; New York: Oxford University press, p. 45-73) gave seven criteria to consider when designing a customized force-recording device. Where appropriate, we tested if our apparatus met their criteria. The apparatus accurately records forces in three orthogonal directions, has low cross-talk, maintains a high frequency response, exhibits a linear response up to at least 200 Newtons, and displays a uniform response to a given force across the instrumented contact piece. Our design does not easily facilitate the identification of the point of force application. Therefore, joint moments cannot be easily calculated. This limitation, however, does not affect the apparatus's ability to accurately record the magnitude and direction of a force (as shown by other tests). We developed this apparatus to measure jaw forces during tree gouging in common marmosets (Callithrix jacchus), but the general design can be readily modified to study a variety of primate behaviors on vertical substrates.

Animals↗

Evolution of feeding niches in New World monkeys.

The adaptive radiation of modern New World monkeys unfolded as the major lineages diversified within different dietary-adaptive zones predicated upon a fundamentally frugivorous habit. The broad outlines of this pattern can be seen in the fossil record, beginning in the early Miocene. Cebids are obligate frugivorous predators. The smallest forms (Cebuella, Callithrix) are specialized exudativores, and the largest (cebines) are seasonally flexible omnivores, feeding particularly on insects (Saimiri) or "hard" foods, such as pith and palm nuts (Cebus), when resources are scarce. The smaller-bodied atelids (Callicebus, Aotus) may use insects or leaves opportunistically, but pitheciins (saki-uakaris) specialize on seeds as their major protein source. The larger atelines (Alouatta, Brachyteles) depend on leaves or on ripe fruit (Ateles). Locomotion, body size, and dietary adaptations are linked: claws and small body size opened the canopy-subcanopy niche to callitrichines; climbing and hanging, the fine-branch setting to the atelines; large size and strength, semiprehensile tails, and grasping thumbs, the extractive insectivory of Cebus; deliberate quadrupedalism, the energy-saving transport of folivorous Alouatta. Body size increases and decreases occurred often and in parallel within guilds and lineages. Conventional dietary categories, particularly frugivory, are inadequate for organizing the behavioral and anatomical evidence pertinent to evolutionary adaptation. Related models of morphological evolution based on feeding frequencies tend to obfuscate the selective importance of "critical functions," responses to the biomechanically challenging components of diet that may be determined by a numerically small, or seasonal, dietary fraction. For fossils, body size is an unreliable indicator of diet in the absence of detailed morphological information. More attention needs to be given to developing techniques for identifying and quantifying mechanically significant aspects of dental form, the physical properties of primate foods, their mode of access, and the cycles of availability and nutritional value.

Adaptation, Physiological↗

"Giant" tamarin from the Miocene of Colombia.

A nearly complete but badly crushed skull and mandible of Lagonimico conclucatus, gen. et sp. nov. is described from the La Victoria Formation, Colombia. The specimen is of middle Miocene age and dates from about 13.5 Ma. Features of the dentition suggest Lagonimico is a sister group to living Callitrichinae (Saguinus, Leontopithecus, Callithrix, and Cebuella). These features include having elongate compressed lower incisors, a reduced P2 lingual moiety, and the absence of upper molar hypocones. The new taxon also has autapomorphies, such as a relatively deep jaw, that rule it out of the direct ancestry of any living callitrichine. This animal is assigned to a new tribe of the callitrichine clade. The orbits of L. conclucatus are small, suggesting diurnal habits. Inflated, low-crowned (bunodont) cheek teeth with short, rounded shearing crests, as well as premolar simplification and M3 size reduction, suggest fruit- or gum-eating adaptations, as among many living callitrichines. Procumbent and slightly elongate lower incisors suggest this species could use its front teeth as a gouge, perhaps for harvesting tree gum. Estimates from jaw size suggest Lagonimico weighed about 1,200 g, about the size of Callicebus, the living titi monkey of South America. Judged from tooth size and jaw length, Lagonimico would have been slightly smaller than Callicebus, but still larger than Callimico or any living callitrichine. Therefore, many of the distinctive anatomical features of the callitrichine clade, sometimes explained by phyletic dwarfing, may have evolved at larger body size. Evolutionary size reduction may have occurred in parallel in callitrichines and Callimico.

Animals↗

Distribution of olfactory epithelium in the primate nasal cavity: are microsmia and macrosmia valid morphological concepts?

The terms "microsmatic" and "macrosmatic" are used to compare species with greater versus lesser olfactory capabilities, such as carnivores compared to certain primates. These categories have been morphologically defined based on the size of olfactory bulb and surface area of olfactory epithelium in the nasal fossa. The present study examines assumptions regarding the morphological relationship of bony elements to the olfactory mucosa, the utility of olfactory epithelial surface area as a comparative measurement, and the utility of the microsmatic concept. We examined the distribution of olfactory neuroepithelium (OE) across the anteroposterior length of the nasal fossa (from the first completely enclosed cross-section of the nasal fossa to the choanae) in the microsmatic marmoset (Callithrix jacchus) compared to four species of nocturnal strepsirrhines (Otolemur crassicaudatus, O. garnetti, Microcebus murinus, and Cheirogaleus medius). Adults of all species were examined and infant C. jacchus, O. crassicaudatus, M. murinus, and C. medius were also examined. All specimens were serially sectioned in the coronal plane and prepared for light microscopic study. Distribution of OE across all the turbinals, nasal septal surfaces, and accessory spaces of the nasal chamber was recorded for each specimen. The right nasal fossae of one adult C. jacchus and one neonatal M. murinus were also three-dimensionally reconstructed using Scion Image software to reveal OE distribution. Findings showed OE to be distributed relatively more anteriorly in adult C. jacchus compared to strepsirrhines. It was also distributed more anteriorly along the nasal septal walls and recesses in neonates than adults. Our findings also showed that OE surface area was not a reliable proxy for receptor neuron numbers due to differing OE thickness among species. Such results indicate that nasal cavity morphology must be carefully reconsidered regarding traditional functional roles (olfaction versus air conditioning) assigned to various nasal cavity structures. At present, the microsmatic concept itself lacks a basis in nasal chamber morphology, since OE may have varying patterns of distribution among different primates.

Adaptation, Physiological↗

Expression of neuron-specific markers by the vomeronasal neuroepithelium in six species of primates.

Vomeronasal organ (VNO) morphology varies markedly across primate taxa. Old World monkeys display no postnatal VNO. Humans and at least some apes retain a vestigial VNO during postnatal life, whereas the strepsirrhines and New World Monkeys present a morphologically well-defined VNO that, in many species, is presumed to function as an olfactory organ. Available microanatomical and behavioral studies suggest that VNO function in these species does not precisely duplicate that described in other mammalian taxa. The questions of which species retain a functional VNO and what functions they serve require inquiry along diverse lines but, to be functional, the vomeronasal epithelium must be neuronal and olfactory. We used immunohistochemistry to establish these criteria in six primate species. We compared the expression of two neuronal markers, neuron-specific beta-tubulin (BT) and protein gene product 9.5, and olfactory marker protein (OMP), a marker of mature olfactory sensory neurons, in paraffin-embedded VNO sections from two strepsirrhine and four haplorhine species, all of which retain morphologically well-defined VNOs during postnatal life. The infant Eulemur mongoz, adult Otolemur crassicaudatus, neonatal Leontopithicus rosalia, and adult Callithrix jacchus express all three proteins in their well-defined vomeronasal neuroepithelia. The infant Tarsius syrichta showed some BT and OMP immunoreactivity. We establish that two strepsirrhine species and at least some New World haplorhines have mature sensory neurons in the VNO. In contrast, at all ages examined, Saguinus geoffroyi VNO expresses these markers in only a few cells.

Aging↗

Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys.

Surprisingly little is known about the proportions of projections of different areas and regions of neocortex to the superior colliculus in primates. To obtain an overview of such projection patterns, we placed a total of 10 injections of retrograde tracers in the superior colliculus of three New World monkeys (Callithrix, Callicebus, and Aotus). Because cortex was flattened and cut parallel to the surface, labeled corticotectal neurons could be accurately located relative to architectonic boundaries and surface features. While there was variability across cases and injection sites, the summed results clearly support several conclusions. One, three well-defined visual areas, V1 (18%), V2 (14%), and MT (11%), contributed nearly half of the total of labeled cells. Two, several other visual areas (V3, DL, DM, and FST) that are early in the processing hierarchy provided another fifth of the total. Three, inferior temporal visual areas of the ventral stream provided only minor projections. Four, visuomotor fields (FEF, FV, cortex in the region of SEF, and posterior parietal cortex) contained less than 10% of the labeled neurons. Five, few labeled neurons were in auditory or somatosensory areas. The results indicate that cortical inputs to the superior colliculus originate predominantly from early visual areas rather than from multimodal or visuomotor areas.

Afferent Pathways↗

Distribution of two morphologically distinct subsets of serotoninergic axons in the cerebral cortex of the marmoset.

The serotoninergic innervation of the marmoset (New World monkey, Callithrix jacchus) cerebral cortex has been analyzed by using immunocytochemistry. The use of a sensitive monoclonal antibody against serotonin allowed the visualization of the fine morphology of individual axons. Two types of terminal axons were demonstrated: one has sparse, small, ovoid varicosities (dia. less than 1 micron), and the other has large, spheroidal varicosities (up to 5 microns in dia.), which are more densely clustered. The first type of axon is distributed through all cortical layers, with a characteristic laminar distribution that varies from area to area. The second type of axons was distributed sparsely in all regions but was markedly denser in the frontal and anterior parietal lobes, and in the hippocampal formation. Axons with large varicosities typically surrounded certain cell bodies and proximal dendrites, forming pericellular arrays, or baskets. These morphological specializations were most frequent in the frontal and anterior parietal cortex, where they were found around stellate and horizontal cells in layer I and around stellate and bipolar cells in layer II and III. Similar baskets were also found in the hippocampal formation, mainly along the border between the hilus and the granule cell layer of the dentate gyrus, across the CA4 field, and at each side of the pyramidal cell layer of the CA3 regions. The distribution and cellular morphology of the cell surrounded by the 5-HT basket fibres were suggestive of a subpopulation of interneurons, possibly GABAergic and/or peptidergic. In agreement with previous reports on the innervation of the cerebral cortex of other mammalian species, the marmoset cerebral cortex is innervated by two separate subsystems of serotoninergic axons. One of these may have a strong and specific influence on the cortical inhibitory circuitry, via relay through cortical interneurons.

Animals↗

Analysis of DR-like molecules on a marmoset Epstein-Barr virus-induced cell line using a monomorphic anti-human HLA-DR monoclonal antibody.

Mouse anti-HLA D region-related (DR) monoclonal antibodies have been found to cross-react with peripheral blood leukocytes from one primate species, the common marmoset (Callithrix jacchus). Immunoprecipitates of radioactively labeled cells extracted from a marmoset Epstein-Barr virus-induced cell line were analyzed by one- and two-dimensional gel electrophoresis and compared with the DR antigens of a human lymphoblastoid B cell line. Two chains of estimated molecular weights of 34 000 (alpha) and 28 000 (beta), similar to the human alpha and beta chains, have been observed in marmoset immunoprecipitates. Additionally, a set of spots located in the same area as the set of invariant spots found in human HLA-DR antigens is shown by two-dimensional gel electrophoresis. Thus, cross-reacting anti-human HLA-DR monoclonal antibodies could be used to analyze the expression and the structure of marmoset DR-like antigens.

Animals↗

The histochemical location of three diagnostic enzymes in the marmoset liver.

The histochemical locations of alkaline phosphate (ALP), leucine aminopeptidase (LAP) and gamma glutamyltransferase (GGT) were demonstrated in the liver of the marmoset (Callithrix jacchus). Although all three enzymes were located in cell membranes, the location of LAP was demonstrated by a chromogenic substrate, in the canalicular membrane. GGT was seen in a vascular network, provisionally identified as the peribiliary arterial plexus. Possible diagnostic applications in toxicology are discussed.

Alkaline Phosphatase↗

Comparative and functional myology of the prehensile tail in New World monkeys.

The caudal myology of prehensile-tailed monkeys (Cebus apella, Alouatta palliata, Alouatta seniculus, Lagothrix lagotricha, and Ateles paniscus) and nonprehensile-tailed primates (Eulemur fulvus, Aotus trivirgatus, Callithrix jacchus, Pithecia pithecia, Saimiri sciureus, Macaca fascicularis, and Cercopithecus aethiops) was examined and compared in order to identify muscular differences that correlate with osteological features diagnostic of tail prehensility. In addition, electrophysiological stimulation was carried out on different segments of the intertransversarii caudae muscle of an adult spider monkey (Ateles geoffroyi) to assess their action on the prehensile tail. Several important muscular differences characterize the prehensile tail of New World monkeys compared to the nonprehensile tail of other primates. In atelines and Cebus, the mass of extensor caudae lateralis and flexor caudae longus muscles is more uniform along the tail, and their long tendons cross a small number of vertebrae before insertion. Also, prehensile-tailed monkeys, especially atelines, are characterized by well-developed flexor and intertransversarii caudae muscles compared to nonprehensile-tailed primates. Finally, Ateles possesses a bulkier abductor caudae medialis and a more cranial origin for the first segment of intertransversarii caudae than do other prehensile-tailed platyrrhines. These myological differences between nonprehensile-tailed and prehensile-tailed primates, and among prehensile-tailed monkeys, agree with published osteological and behavioral data. Caudal myological similarities and differences found in Cebus and atelines, combined with tail-use data from the literature, support the hypothesis that prehensile tails evolved in parallel in Cebus and atelines.

Animals↗

Group size and aggression: 'recruitment incentives' in a cooperatively breeding primate

In many cooperatively breeding birds and mammals, group size is positively correlated with reproductive success. In marmoset and tamarin monkeys, species that display cooperative breeding, the presence of helpers appears to be critical for offspring survival, and breeders might be expected to display social strategies that would regulate group size. This study investigated the association between group size and aggression towards strangers in Wied's black tufted-ear marmosets, Callithrix kuhlifrom small groups (with no helpers present) and large groups (with helpers present). Residents were exposed to multiple presentations of male and female strangers. Breeding females from large groups spent more time in close proximity to strangers, showed higher levels of agonistic displays and engaged in higher levels of aggressive behaviour towards intruders than did breeding females from small groups. Breeding male behaviour did not dramatically differ as a function of group size. After the removal of the intruder, female breeders from large groups showed higher levels of scent-marking relative to baseline observations, and time spent in close proximity to the partner increased after exposure to female intruders in large, but not small, groups. The results reveal that breeders from small groups are tolerant of strangers, which may facilitate the recruitment of additional group members, whereas breeders from large groups, particularly females, are intolerant of strangers, which may inhibit immigration. These findings have implications for understanding mechanisms that regulate immigration in cooperatively breeding animals, and suggest of how breeders from small groups might reconcile the serious limitation of having few or no helpers.

Journal Article↗

Push or pull: an experimental study on imitation in marmosets

A laboratory experiment was conducted in order to explore the possibility of imitation, that is, response learning by observation, in marmosets, Callithrix jacchusInexperienced individuals were allowed to observe a skilful model that demonstrated one of two possible techniques (pushing or pulling a pendulum-door) to get food from inside a wooden box. Their initial manipulative actions, performed when exposed to the box in a subsequent test, were compared with those of naive control subjects (non-observers). The observers showed less exploratory behaviour than the non-observers and, more importantly, some showed a strong tendency to use the demonstrated opening technique in the initial test phase. This initial preference disappeared in the course of five test sessions and the observers converged towards the simpler, alternative solution that was generally preferred by the non-observers. Despite fundamental individual differences in the observer group and the failure to find a significant group effect, the results indicate that marmosets are capable of learning simple motor skills through conspecific observation.Copyright 1997 The Association for the Study of Animal Behaviour1997The Association for the Study of Animal Behaviour

Journal Article↗

Social determinants of reproductive failure in male common marmosets housed with their natal family.

Postpubertal male common marmosets, Callithrix jacchus, engage in little or no sexual behaviour while living with their natal families. The social mechanisms underlying this phenomenon have not been identified but have been assumed to include reproductive suppression by dominant males and/or avoidance of mating with closely related females. We evaluated these two possible components of male reproductive failure. Seven postpubertal males and their fathers underwent a series of 45-min sex tests, in which the son, the father, or the son and father together were allowed to interact freely with the mother/mate or with an unfamiliar, unrelated adult female. We measured testosterone, luteinizing hormone and cortisol concentrations in blood samples collected from males immediately following each test, and in basal blood samples collected on three different occasions. Sons, but not fathers, engaged in very low rates of sexual behaviour when tested with the mother/mate. When tested with unrelated females, however, sons engaged in significantly more sexual behaviour than they had when tested with their mothers and showed no differences from their fathers. When sons and fathers were tested together, both males performed significantly less sexual behaviour than when tested alone with a female; however, they showed no overt competition for females and engaged in little agonism. Hormone levels did not differ significantly between fathers and sons. These results indicate that avoidance of mating with familiar females and possibly father-son competition, but not specific, rank-related suppression, contribute to reproductive failure among postpubertal male marmosets living with their natal family. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

True imitation in marmosets.

Marmosets, Callithrix jacchus, observed a demonstrator removing the lids from a series of plastic canisters to obtain a mealworm. When subsequently allowed access to the canisters, marmosets that observed a demonstrator using its hands to remove the lids used only their hands. In contrast, marmosets that observed a demonstrator using its mouth also used their mouth to remove the lids. Since hand and mouth demonstrators brought about identical changes in the canisters, the differential test behaviour of the observer groups suggests that they learned about the demonstrator's behaviour. Furthermore, marmosets that had not been given the opportunity to observe a demonstrator prior to testing had a low probability of mouth opening, even if the canisters were previously opened by a mouth-opening demonstrator in an olfactory control experiment. Corroborating Bugnyar & Huber's (1997, Animal Behaviour, 54, 817-831) earlier findings, our results provide further evidence that marmosets can imitate. Copyright 2000 The Association for the Study of Animal Behaviour.

Journal Article↗

The nucleotide sequences of the parathyroid gene in primates (suborder Anthropoidea).

Nucleotide sequences of the parathyroid (PTH) gene of 12 species of primates belonging to suborder Anthropoidea were examined. The PTH gene contains one intron that separates two exons that code the sequence of prepro and PTH, respectively. The intron of the PTH gene in Cebus apella, Callithrix jacchus, and Saguinus oedipus was 102 bp long, whereas a 103-bp intron was observed in the remaining species. Phylogenetic analysis using the nucleotide sequences of PTH revealed that these 12 species of primates of suborder Anthropoidea could be divided into two groups of the infraorder Platyrrhini (C. apella, C. jacchus, and S. oedipus) and the infraorder Catarrhini (Macaca fascicularis, Macaca fuscata, Cercopithecus aethiops, Papio hamadryas, Presbytes obscura, Hylobates lar, Pongo pygmaeus, Pan troglodytes, and Pan paniscus). The latter infraorder could be further subdivided into two subgroups belonging to the superfamily Cercopithecoidea (M. fascicularis, M. fuscata, C. aethiops, P. hamadryas, and P. obscura) and the superfamily Hominoidea (H. lar, P. pygmaeus, P. troglodytes, and P. paniscus). The deduced amino acid sequences of PTH gene between 12 species of nonhuman primates and human revealed no amino acid substitution in mature PTH among orangutans, chimpanzees, and humans. The results indicated that the PTH gene is very conserved among primates, especially between great apes and humans. The apes are the most suitable animals to be used for studying the bone metabolism and applying the knowledge to clinical use in humans.

Amino Acid Sequence↗

Hand specialization, sympatry, and mixed-species associations in callitrichines.

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands of Leontopithecus differ in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands of Saguinus fuscicollis adapted to manipulative foraging, and are they functionally similar to Leontopithecus' hands? 3. Is hand morphology in S. fuscicollis more similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollis and S. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, and S. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, and Callimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands of Leontopithecus are adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands of S. fuscicollis, S. tripartitus and S. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.

Animals↗