Tail growth tracks the ontogeny of prehensile tail use in capuchin monkeys (Cebus albifrons and C. apella)

Physical anthropologists have devoted considerable attention to the structure and function of the primate prehensile tail. Nevertheless, previous morphological studies have concentrated solely on adults, despite behavioral evidence that among many primate taxa, including capuchin monkeys, infants and juveniles use their prehensile tails during a greater number and greater variety of positional behaviors than do adults. In this study, we track caudal vertebral growth in a mixed longitudinal sample of white-fronted and brown capuchin monkeys (Cebus albifrons and Cebus apella). We hypothesized that young capuchins would have relatively robust caudal vertebrae, affording them greater tail strength for more frequent tail-suspension behaviors. Our results supported this hypothesis. Caudal vertebral bending strength (measured as polar section modulus at midshaft) scaled to body mass with negative allometry, while craniocaudal length scaled to body mass with positive allometry, indicating that infant and juvenile capuchin monkeys are characterized by particularly strong caudal vertebrae for their body size. These findings complement previous results showing that long bone strength similarly scales with negative ontogenetic allometry in capuchin monkeys and add to a growing body of literature documenting the synergy between postcranial growth and the changing locomotor demands of maturing animals. Although expanded morphometric data on tail growth and behavioral data on locomotor development are required, the results of this study suggest that the adult capuchin prehensile-tail phenotype may be attributable, at least in part, to selection on juvenile performance, a possibility that deserves further attention.     

Carbonic anhydrase II in new world monkeys

Carbonic anhydrase II electrophoretic patterns were investigated in 3113 animals belonging to 12 genera and 24 species of New World primates. Polymorphism was detected in 13 species. A total of 24 different alleles was postulated to explain the variability found; the genusAotus showed the highest (eight) number of such alleles. Three genera of the family Callitrichidae (Callithrix, Saguinus, andCebuella) presented five alleles that were not found among the Cebidae. Important markers at the generic level were observed inCallicebus (CA2 ^*6 andCA2 ^*12),Cebus (CA2 ^*10, CA2^*16, andCA2 ^*21), andAotus (CA2^*3, CA2^*4, CA2^*5, CA2^*9, CA2^*15, CA2^*17, CA2^*22, CA2^*23). CA2^*13 seems to be the most common allele among the Cebidae; six genera of this family showed frequencies higher than 70% of it.     

Allomothering behaviour of new and old world monkeys

The holding or transferring of newborn infants at less than 1 month old by individuals other than the mothers was studied in 24 species of New and Old World monkeys under captive conditions. The observed monkey species could be divided into two types. Group A included eight species of three families where the mothers were tolerant to ‘infant transfer’ and readily retrieved their infants from other individuals, the frequency of infant transfer being high. The infant transfer of this group was termed allomothering behaviour. Group B included 16 species of two families where infant transfer did not occur at all or its frequency was very low and the mothers were possessive of their infants. Once transfer did occur, the infant could not be reclaimed with ease. The relationships between the two groups and taxonomic status, life forms and social types were evaluated in a total of 45 species from the present study and the literature. Correspondences were found with social type and taxonomic status. That is, species of Group A were seen only in the family or one-male type, except for one species, although none of this group appeared in the Cercopithecinae regardless of social types. The significance of infant transfer is discussed in relation to the participants' responses to it and the correlations between the two groups and social types.     

Life history patterns of new world monkeys

Allometric methods are used to investigate the life history patterns of New World monkeys. These patterns are compared to those found in other haplorhines and links with ecology are explored. The life history characteristics of the cebid monkeys suggest that these species are primarily slow breeding and slow developing for primates of their size. I suggest that these characteristics arose during a long period of adaptation to stable rainforest habitats. The capuchins and squirrel monkeys are a notable exception to the general rule that genera found outside primary forests will have a “fast” life history. In the marmosets and tamarins selection for small size and high birth rate has occurred, probably as a result of their adapting to more secondary habitats. It is this selection for rapid breeding, combined with the preadaptation of paternal care, that has probably led to twinning in these species. The evidence presented indicates that it is unlikely that twinning arose as a direct result of the mechanical constraints of small size but is more probably due to selection for increased reproductive output.     

Animal behaviour: old world monkeys build new world order

New experimental evidence shows that policing behaviour by dominant monkeys stabilizes and integrates macaque societies.     

Role of the prehensile tail during ateline locomotion: experimental and osteological evidence

The dynamic role of the prehensile tail of atelines during locomotion is poorly understood. While some have viewed the tail of Ateles simply as a safety mechanism, others have suggested that the prehensile tail plays an active role by adjusting pendulum length or controlling lateral sway during bimanual suspensory locomotion. This study examines the bony and muscular anatomy of the prehensile tail as well as the kinematics of tail use during tail-assisted brachiation in two primates, Ateles and Lagothrix. These two platyrrhines differ in anatomy and in the frequency and kinematics of suspensory locomotion. Lagothrix is stockier, has shorter forelimbs, and spends more time traveling quadrupedally and less time using bimanual suspensory locomotion than does Ateles. In addition, previous studies showed that Ateles exhibits greater hyperextension of the tail, uses its tail to grip only on alternate handholds, and has a larger abductor caudae medialis muscle compared to Lagothrix. In order to investigate the relationship between anatomy and behavior concerning the prehensile tail, osteological data and kinematic data were collected for Ateles fusciceps and Lagothrix lagothricha. The results demonstrate that Ateles has more numerous and smaller caudal elements, particularly in the proximal tail region. In addition, transverse processes are relatively wider, and sacro-caudal articulation is more acute in Ateles compared to Lagothrix. These differences reflect the larger abductor muscle mass and greater hyperextension in Ateles. In addition, Ateles shows fewer side-to-side movements during tail-assisted brachiation than does Lagothrix. These data support the notion that the prehensile tail represents a critical dynamic element in the tail-assisted brachiation of Ateles, and may be useful in developing inferences concerning behavior in fossil primates.     

Model life tables for the smaller new world monkeys

Mortality statistics from five populations of small New World monkeys (includinsg Callithrix jaccus, Leontopithecus rosalia, Saguinus fuscicollis, and Saguinus oedipus) were combined to generate a standard model life table reflecting the mortality patterns of these primates. The model is applied to three individual populations to illustrate a strategy for smoothing and interpolating mortality statistics of varying completeness and quality. © 1993 Wiley-Liss, Inc.     

Adrenergic retinal neurons of some new world monkeys

Summary The retina of Aotes monkeys, Cebus monkeys, squirrel monkeys, and marmosets were investigated. Adrenergic perikarya were found in the innermost cell rows of the inner nuclear layer of all the investigated species. In addition, the Cebus monkey was found to have a special type of adrenergic neurons in the inner nuclear layer. This cell type was called the adrenergic pleomorph cell. Its processes ramify in the inner nuclear and inner plexiform layers. Adrenergic terminals occur in three more or less well developed sublayers of the inner plexiform layer, the layers being best developed in the Cebus monkey. Adrenergic terminals were also found around the cells of the inner nuclear layer and at the horizontal cells, where a scant sublayer is formed. More than one adrenergic sublayer of the inner plexiform layer has not been observed in primates previously, nor have the adrenergic terminals in the inner nuclear layer been observed previously in any species. The adrenergic pleomorph cells of the Cebus monkey also seem to be unique. The marked differences even between animals as closely related as some platyrhine monkeys call for caution when comparing the detailed function of the retina in different animals.This study was supported by grants from the Swedish Medical Research Council (B69-14X-2321-02) and the Faculty of Medicine, University of Lund, and was carried out within a research group sponsored by the Swedish Medical Research Council (projects No. B69-14X-56-05C and B69-14X-712-04C).     

Wing and tail myology of Tyto furcata (Aves,Tytonidae)

Barn Owls (Tytonidae) are nocturnal raptors with the largest geographical distribution among Strigiformes. Several osteological, morphometrical, and biomechanical studies of this species were performed by previous authors. Nevertheless, the myology of forelimb and tail of the Barn Owls is virtually unknown. This study is the first detailed myological study performed on the wing and tail of the American Barn Owl (Tyto furcata). A total of 11 specimens were dissected and their morphology and muscle masses were described. Although T. furcata has the wing and tail myological pattern present in other species of Strigiformes, some peculiarities were observed including a difference in the attachment of m. pectoralis propatagialis due to the lack of the os prominence, and the presence of an osseous arch in the radius that seems to widen the anchorage area of the mm. pronator profundus, extensor longus alulae, and extensor longus digiti majoris. Furthermore, the m. biceps brachii has an unusual extra belly that flexes the forearm. The interosseous muscles have a small size and lacks ossified tendons. This feature may be indicative of a lower specialization in the elevation and flexion of the digiti majoris. Forelimb and tail muscle mass account for 10.66 and 0.24% of the total body mass, respectively. Forelimb muscle mass value is similar to the nocturnal (Strigiformes) and diurnal (Falconidae and Accipitridae) raptors, while the tail value is lower than in the diurnal raptors (Falconidae and Accipitridae). The myological differences with other birds of prey are here interpreted in association with their “parachuting” hunting style. This work complements our knowledge of the axial musculature of the American Barn owls, and provides important information for future studies related to functional morphology and ecomorphology.     

Comparative microcomputed tomography and histological study of maxillary pneumatization in four species of new world monkeys: the perinatal period

In anthropoid primates, it has been hypothesized that the magnitude of maxillary sinus growth is influenced by adjacent dental and soft tissue matrices. Relatively, little comparative evidence exists for the perinatal period when secondary pneumatization is at its earliest stages in some primates. Here, dental and midfacial variables were studied in a perinatal sample of four anthropoid primates, including three callitrichines (Leontopithecus, Saguinus, and Callithrix) and Saimiri boliviensis. In the latter species, the maxillary recess (the ontogenetic precursor to a "true" maxillary sinus) does not undergo secondary pneumatization. Using histological methods and micro-computed tomography, midfacial and dental dimensions and radiographic hydroxyapatite density of tooth cusps were measured. The distribution of osteoclasts and osteoblasts was also documented. Kruskal-Wallis's one-way analysis of variance tests indicates significant (P < 0.05) differences among groups for dental and midfacial measurements. In particular, the posterior maxillary dentition is relatively larger and more mineralized in Saimiri compared to the callitrichines. At posterior dental levels, Saimiri has the lowest palatonasal index [interdental (palatal) width/width of the nasal cavity] and highest bizygomatic-interorbital index. Distribution of osteoclasts indicates that the inferomedial surfaces of the orbits are resorptive in perinatal Saimiri, whereas, in all callitrichines, these surfaces are depository. Taken together, these findings suggest that pneumatization in Saimiri is suppressed by an inward growth trajectory of the orbits, relatively large posterior dentition, and a correspondingly compressed nasal region.     

Chromosome evolution in new world monkeys (platyrrhini)

During the last decades, New World monkey (NWM, Platyrrhini, Anthropoideae) comparative cytogenetics has shed light on many fundamental aspects of genome organisation and evolution in this fascinating, but also highly endangered group of neotropical primates. In this review, we first provide an overview about the evolutionary origin of the inferred ancestral NWM karyotype of 2n = 54 chromosomes and about the lineage-specific chromosome rearrangements resulting in the highly divergent karyotypes of extant NWM species, ranging from 2n = 16 in a titi monkey to 2n = 62 in a woolly monkey. Next, we discuss the available data on the chromosome phylogeny of NWM in the context of recent molecular phylogenetic analyses. In the last part, we highlight some recent research on the molecular mechanisms responsible for the large-scale evolutionary genomic changes in platyrrhine monkeys.     

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.     

Degrees of sexual dimorphism in Cebus and other new world monkeys

Sexual dimorphism in primate species expresses the effects of phylogeny, life history, behavior, and ontogeny. The causes and implications of sexual dimorphism have been studied in several different primates using a variety of morphological databases such as body weight, canine length, and coat color and ornamentation. In addition to these different patterns of dimorphism, the degree to which a species is dimorphic results from a variety of possible causes. In this study we test the general hypothesis that a species highly dimorphic for one size-based index of dimorphism will be equally dimorphic (relative to other species) for other size-based indices. Specifically, the degree and pattern of sexual dimorphism in Cebus and several other New World monkey species is measured using craniometric data as a substitute for the troublesome range of variation in body weight estimates. In general, the rank ordering of species for dimorphism ratios differs considerably across neural vs. non-neural functional domains of the cranium. The relative degree of sexual dimorphism in different functional regions of the cranium is affected by the independent action of natural selection on those regions. Regions of the cranium upon which natural selection is presumed to have acted within a species show greater degrees of dimorphism than do the same regions in closely related taxa. Within Cebus, C. apella is consistently more dimorphic than other Cebus species for facial measurements, but not for neural or body weight measurements. The pattern in C. apella indicates no single best measurement of the degree of dimorphism in a species; rather, the relative degree of dimorphism applies only to the region being measured and may be enhanced by other selective pressures on morphology. Am J Phys Anthropol 107:243–256, 1998. © 1998 Wiley-Liss, Inc.     

Functional morphology of ventral tail bending and prehensile abilities of the seahorse,Hippocampus kuda

Unlike most teleosts, the seahorse (genus Hippocampus) is able to bend its tail ventrally, uses its tail in a postural role as a grasping and holding appendage, and possesses heavy body plates instead of scales. To investigate seahorse axial bending mechanisms and the role of plating in those mechanisms, observations were made on seahorses curling their tails ventrally and holding a support and components of the mechanical system used for axial bending, including dermal plates, vertebrae, and axial muscles, were examined. Anatomical modifications involved in ventral tail bending include hypertrophy of the ventral region of the hypaxial muscle, ventrolateral attachment of the myomeres to plates, and modification of the infracarinalis posterior muscles so that they act in axial bending rather than in fin movement as has previously been hypothesized (Harder, '75) for other fishes. Modifications for prehension include the presence of fibers histochemically characterized as tonic in the median ventral muscles (the modified infracarinalis muscle) and in portions of the myomeres. Dermal plates are an important part of the force transmission system used in seahorse tail bending. They transmit forces from the hypaxial myomeres to bend the tail both laterally and ventrally. This study expands our understanding of axial bending in fishes by examining extreme modifications of the musculoskeletal system associated with the evolution of unique functional capabilities within teleosts. © 1996 Wiley-Liss, Inc.     

Forelimb anatomy of New World monkeys: myology and the interpretation of primitive anthropoid models

The forelimbs of 12 genera of New World monkeys, two genera of Old World monkeys, and a gibbon were dissected. Of the 54 muscles examined, 19 exhibited significant intergeneric variation. We present arguments for which morphologies are primitive and which are derived within platyrrhines and within anthropoids. We conclude that the forelimbs of Cebus apella and Callicebus moloch represent good models of the ancestral anthropoid morphology. Thus among living anthropoids they are most appropriate for comparisons with early fossil anthropoids. They are also useful for determining whether myological anomalies of human aneuploids are atavistic. Wagner tree analyses were conducted to assess the value of these myological characters in phylogenetic studies of platyrrhines. In most respects the Wagner trees were consonant with phylogenies previously proposed, although some hypothesized trees are less parsimonious than others in explaining our data. There is an unexpected number of derived features shared by Aotus and the Atelines. There are marked dissimilarities in forelimb musculature between Aotus and Callicebus.     

Comparative myology of the forelimb of squirrels (Sciuridae)

The musculature of the shoulder, arm, and forearm was studied in 19 genera of squirrels, representing the Pteromyinae (flying squirrels) and all 7 tribes of the Sciurinae (tree and ground squirrels). The objective was to locate derived anatomical features of functional or phylogenetic significance and to determine how much morphological variation underlies the diverse locomotor behavior of squirrels, which includes terrestrial and arboreal bounding, climbing, digging, and gliding. The fossil evidence suggests that arboreality is primitive for squirrels, and in fact tree squirrels appear to represent the primitive sciurid morphology. Ground squirrels are less uniform and exhibit a few derived features, including a clavobrachialis muscle not seen in other squirrels. Pygmy tree squirrels, which have evolved independently in three tribes, exhibit convergence of forelimb anatomy, including the loss or reduction of several muscles in the shoulder and forearm. The forelimb anatomy of flying squirrels is the most derived and differs from that of tree squirrels in details of shoulder, arm, and forearm musculature. Some of these muscular differences among squirrels have phylogenetic significance, being shared by closely related genera, but none has significance above the tribal level. Many of the differences suggest a variety of changes in function that are amenable to further study. J. Morphol. 234:155–182, 1997. © 1997 Wiley-Liss, Inc.     

Comparative limb myology of two opossums,Didelphis and Chironectes

A comparative study of limb morphology indicates that the osteological and myological differences between Didelphis virginiana, the Virginia opossum, and Chironectes minimus, the water opossum, may be associated in Chironectes with decreased resistance to water and increased mechanical advantage of its muscles for increased force. Limb myology is described and a synonymy of terms is applied to the musculature of these two opossums.