Brief communication: Noninvasive measuring of operational tongue length in callitrichids

Callitrichids use their tongue in various social, ecological, and hygienic contexts. Using a noninvasive measuring device, we obtained data on the operational tongue length (OTL) in seven species from the family Callitrichidae. OTL (defined as the maximum tongue extension into the device) varied significantly between species and the width of the device, but did not correlate with mandible length; it is smaller in relation to mandible length in Leontopithecus chrysomelas compared to species from the genera Saguinus and Callithrix. Current information does not allow concluding which of the various functions of the tongue is selecting for tongue length. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

The respiratory system of the genusCallithrix,the South American monkey

It has been described the cytology of the following parts of the respiratory system of some South American primates:Callithrix jacchus andCallithrix argentata melanura. The nasal cavities are divided into three parts: a vestibule, covered with a stratified nonkeratinized squamous epithelium; the respiratory portion, consisting of a pseudostratified columnar ciliated epithelium with goblet cells and the olfactory portion which is also covered with a high respiratory epithelium without goblet cells. The trachea is lined with a mucous membrane, whose epithelium is pseudostratified columnar ciliated with scarce goblet cells in the proximal portion unlike to the distal one. In the dorsal portion of the trachea, at the level of the gap between the two ends of incomplete cartilaginous rings, the epithelial lining is of transitional type. The incomplete hyaline cartilaginous rings present centers of calcification. The right and left lungs consist of two and three lobes respectively characteristic for these species, but they are not divided into lobules by connective tissue as in other ones. The bronchi, bronchioles and the respiratory portion, respiratory bronchioles, alveolar ducts, alveolar sacs, and alveoli present the typical respiratory structure with exception of their cartilaginous configuration; the cartilage continues as far as the respiratory bronchioles and alveolar ducts. These last structures are formed by a thin squamous epithelium, in which we observed two types of alveolar lining cells. This work was supported by grants from the Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET) and EHIGE program. Postgraduated fellow from CONICET. established Investigator and Director of EHIGE (Estudio Histológico comparado del Sistema de Glándulas Endócrinas) from CONICET.     

Dietary and dental adaptations in the Pitheciinae.

Since Mivart (1865), Cacajao, Chiropotes, and Pithecia have been grouped into a single taxon, which he called the subfamily Pitheciinae but which I, following Rosenberger (this issue), refer to as the living members of the tribe Pitheciini. While few today doubt the association of these three living genera, not all would place them together with Aotus and Callicebus in the subfamily Pitheciinae. This is an attempt to sort out the behavioral and morphological features of feeding and dental morphology in these taxa. Extant members of the tribe Pitheciini are adapted for sclerocarpic foraging, morphological evidence for which is found in the fossils of Soriacebus and Cebupithecia. Sclerocarpic foraging in living pitheciins is a two-stage process of seed predation involving 1) specialized features of the anterior dentition that allow removal of a hard pericarp that protects a seed or seeds, followed by 2) mastication by the posterior dentition having low cusp relief to triturate nutritious seeds of a relatively soft and uniformly pliable consistency. The dentitions of fossil pitheciins, Soriacebus and Cebupithecia, demonstrate that the hypertrophy of lower incisors plus the robustness and flaring of the canine precede development of low cusp relief on molars and premolars in the evolution of morphological features associated with sclerocarpic foraging. Features of sclerocarpic foraging are found less uniformly in the other two pitheciines, Callicebus and Aotus.     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

Diseases of the Callitrichidae: a review.

The Callitrichidae contains four genera that embrace up to 50 species and subspecies found in neotropical habitats. Certain members have either naturally occurring or induced conditions that serve as important models of human disease. They include viral, bacterial, and parasitic infections, nutritional deficiencies, neoplasia, and various other conditions. The spontaneous diseases of captive callitrichids and those to which these species are experimentally susceptible were reviewed.     

Flower and Fruit Visitors of Marcgravia longifolia in Amazonian Peru

Abstract: We recorded nectarivorous and frugivorous visitors of Marcgravia longifolia (Marcgraviaceae) at the Estación Biológica Quebrada Blanco in the northeastern Peruvian Amazonia. M. longifolia belongs to the subgenus Plagiothalamium, with downward facing flowers. A glossophagine bat, probably Anoura caudifer, was identified as a potential pollinator. Three primate species - Saguinus fuscicollis, Saguinus mystax and Callicebus cupreus - were recorded as potential seed dispersers. This is the first documentation of primate seed dispersal of a species from the family Marcgraviaceae.     

The costs of infant carrying in captive cotton-top tamarins

Marmosets and tamarins have a communal rearing system in which all group members help to care for the twin infants characteristic of this family of primates. Helpers are likely to incur time and energy costs by contributing to infant care. Predictions that cotton-top tamarin (Saguinus oedipus) helpers would change their behavior when carrying infants because of reduced mobility and/or a need for increased vigilance were tested in a captive colony. Tamarins carrying an infant spent significantly less time feeding, foraging, moving, or engaging in social activities such as grooming than they did when not carrying. Frequencies of scratching, autogrooming, and scent marking were significantly reduced in carriers, suggesting that their mobility was reduced. However, carriers were significantly less likely to be vigilant (measured by direction of gaze) than when not carrying. Further observations showed that carriers spent more time in concealed areas than they did when not carrying and were probably therefore adopting a cryptic strategy to reduce predation risks to themselves and to infants. These results demonstrate that tamarin helpers pay costs by carrying infants. Some possible compensating benefits are indicated.     

The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis)

Data collected during a 12-month field investigation of mixed species troops of Saguinus mystax and Saguinus fuscicollis in the Amazon Basin of north-eastern Peru indicate that callitrichid primates play an important role in tropical forest seed dispersal. Moustached and saddle-back tamarins were observed to ingest seeds from a variety of tree and liana species and pass them unharmed. These seeds tended to be large and heavy, and passed through the tamarin digestive tract in one to three hours. Experimental plantings of defecated seeds yielded a germination success rate of 70%. The specific gravity of these seeds (weight/volume) was inversely correlated with passage time and apparently had an indirect influence on the distance that seeds were dispersed from the parent tree. In the case of three preferred fruiting species, Leonia glycycarpa, Pourouma sp., and Hippocrateaceae #283, the present distribution of adult trees closely resembled the pattern of the seed shadow created by Saguinus. Moustached and saddle-back tamarins appeared to be reliable and high-quality dispersal agents for a number of tree and liana species. In this role, they are likely to exert an important influence on the composition, distribution, and regeneration patterns of Amazonian rain forest.     

The role of dilution and differential predation in brood adoptions of the Midas cichlid (<Emphasis Type="Italic">Amphilophus xiloaensis</Emphasis>)

Laboratory experiments were conducted to determine if the addition of conspecific foreign fry affects the survival of host fry in the Midas cichlid, Amphilophus xiloaensis. The study consisted of two separate experiments: (1) adoption treatments simulated by adding 75 foreign fry to a host brood containing 150 fry and parents (10 trials where host fry were larger, 10 trials where foreign fry were larger); (2) control treatments in which no foreign fry were added to a host brood containing 150 fry and parents (20 trials). Predation was imposed by introducing three bigmouth sleepers (Gobiomorus dormitor). No significant differences were found between the survival of host, foreign, and control fry after 24 h. Survival was significantly affected by fry size, leading to differential predation on smaller fry. Mean predation rate increased proportionally with brood size, therefore the addition of conspecific foreign fry did not result in dilution of the host brood.     

Radiographic evaluation of neonatal skeletal development in Callimico goeldii reveals closer similarity to Callithrix jacchus than to Saguinus oedipus

The phylogenetic affinities of the neotropical Goeldi's monkey (Callimico goeldii) have long been a matter of debate. Whereas most morphological evidence appears to place Callimico in a sister group position relative to the Callitrichidae, genetic studies place C. goeldii within the Callitrichidae and suggest that it is more closely related to marmosets than to tamarins. The present study presents the first radiographic analysis comparing the secondary limb bone ossification of newborn C. goeldii with representatives of the marmosets (Callithrix jacchus) and tamarins (Saguinus oedipus). The state of secondary ossification of the epiphysis and short bones is classified into three different ontogenetic stages. Our results reveal that in terms of the number of ossification centers, C. goeldii is significantly closer to C. jacchus than to S. oedipus. This is the first morphological study to support the findings of molecular studies, and the results suggest that C. goeldii is more closely related to marmosets than to tamarins.     

Effects of sibling-rearing experience on future reproductive success in two species of callitrichidae

The survival rate for offspring of mothers who either had or did not have previous experience rearing younger siblings was compared in two callitrichid species, Callithrix jacchus and Saguinus oedipus. Offspring of mothers with sibling-rearing experience had a higher survival percentage than offspring of inexperienced mothers in both species. While 50–60% of offspring of inexperienced C. jacchus mothers survived, no offspring of inexperienced S. oedipus mothers survived. The results suggest that sibling-rearing experience is necessary for adequate maternal behavior in S. oedipus, but not necessary to the development of maternal behavior in C. jacchus. Effects of previous sibling-rearing experience of S. oedipus fathers on offspring survival were also examined. Whether the father had rearing experience was not related to the survival of their offspring.     

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.     

Luteinizing hormone-releasing hormone in olfactory bulbs of primates

This immunohistochemical study of luteinizing hormone-releasing hormone (LHRH) in the olfactory bulbs in primates was undertaken in order to see whether there was an LHRH innervation in these species similar to that found in rodents. One old world (Macaca fascicularis) and two new world (Saimiri sciureus and Aotus trivirgatus) monkeys were studied. Aotus trivirgatus was of particular interest as it is noctural and so presumably more dependent upon olfactory cues. Animals were perfused with fixative, olfactory bulbs removed and sectioned, and tissues reacted immunocytochemically using LR1 (Benoit) antiserum to LHRH. Some LHRH innervation was found in the olfactory bulbs of all three species, comprising a few LHRH neurons and many fibers that ramified within the bulbs. The accessory bulb (not present as a distinct entity in old world primates) had more LHRH innervation than did the main olfactory bulb. Aotus trivirgatus had the greatest representation of LHRH of the three species. The layer of the olfactory bulb with the greatest number of LHRH fibers was the external plexiform layer. This is also true in rodents. There is evidence that LHRH has a role in the mediation of olfactory cues in reproductive behavior in rodents. It is not known how LHRH functions within the olfactory system in primates. However, the fact that it is distributed similarly in the two groups suggests that it may serve a similar function.     

Systematics of the Saguinus oedipus group of the bare-face tamarins: Evidence from facial morphology

The systematics of the Saguinus oedipus group within the bare-face tamarins remains open to question. Hershkovitz (Living New World Monkeys (Platyrrhini), Vol. 1. Chicago: University of Chicago Press, 1977) places the cotton-top and rufus-naped tamarins as subspecies of Saguinus oedipus (S. o. oedipus and S. o. geoffroyi, respectively). In contrast, several other authors have argued that these two taxa should be considered separate species (S. oedipus and S. geoffroyi). Phylogenetic relationships within the group are also disputed. Resolving these different interpretations has been difficult in part because no study of this group has included an objective measure of expected levels of specific vs. subspecific variation. We used facial measurements from 179 adult crania to address the systematics of this group and included a related species that is known to include multiple subspecies. Our sample included three taxa from the S. oedipus group of the bare-face tamarins (S. oedipus, S. geoffroyi, and S. leucopus) and six subspecies from the related hairy-face tamarin species S. fuscicollis. Comparisons to S. leucopus provided a relative measure of species-level differences. Analyses that included S. fuscicollis provided a measure of subspecific variation. There was no evidence of facial sexual dimorphism in any of these taxa. A variety of multivariate statistical analyses including discriminant function and cluster analysis suggest that S. oedipus and S. geoffroyi differ morphologically at a level consistent with species-level distinctions. The extent of differences between these taxa is large. The differences in their facial morphology was on the order of differences between S. oedipus or S. geoffroyi and S. leucopus rather than the extent of variation among S. fuscicollis subspecies. Furthermore, a comparison of collecting localities revealed that the variation we observed among S. oedipus and S. geoffroyi was not clinal but presented a large morphological discontinuity at the boundary between taxa. Our analyses also suggested that S. leucopus is more similar to S. oedipus than is either to S. geoffroyi. Finally, it may be that there are some distinct species within the S. fuscicollis group. However, this hypothesis, along with other phylogenetic relationships suggested by this study, will require more data and further study. © 1992 Wiley-Liss, Inc.     

Costs of infant‐carrying in the cotton‐top tamarin (Saguinus oedipus)

Infant‐carrying behavior among callitrichids seems to be a costly activity. Costs have been related to the physical efforts of carrying the weight of very heavy infants and to the resulting reduction in foraging efficiency. However, the costs of carrying in terms of the physical consequences for carriers have not previously been assessed. In this study, we have regarded weight loss in infant carriers as a measure of costs. We studied five families of cotton‐top tamarins (Saguinus oedipus) during the first 9 weeks following the birth of infants. Captive‐breeding conditions were required so that body weight could be measured frequently. To avoid inflicting undue stress on the subject animals, we used a noninvasive method for weighing the tamarins. Differences in carrying contribution were found amongst fathers and male and female helpers, with female helpers contributing less. We have found that carrying infants in the cotton‐top tamarins is an activity that produces a weight loss. Fathers and male helpers go through a maximal body weight loss. While carrying, the tamarins also decrease food intake. However, no relationship was found between contribution to carrying and feeding time or in energetic intake during feeding observations. Thus, it seems that a direct relation doesn't exist between the observations of feeding and weight loss. Fathers increase their contribution to carrying during mothers' periovulatory periods. In this period, male helpers and especially fathers go through a maximal body weight loss. We found body weight losses of up to 11.3% in one subadult male and 9.1percnt; in a father during the fifth week. No changes occurred in food intake in fathers or other male helpers during this period. During periovulatory periods, mothers carried less frequently but did increase their food intake. They gained weight from the second week after birth onward, especially during the periovulatory period. It seems that the infant‐carrying behavior of fathers and male helpers may contribute to the improvement of the mothers' physical condition after birth and therefore may support a consecutive pregnancy. Am. J. Primatol. 48:99–111, 1999. © 1999 Wiley‐Liss, Inc.     

Proposed chromosomal phylogeny for the South American primates of the Callitrichidae family (Platyrrhini)

Cytogenetic and cytotaxonomic studies (G, C, sequential G/C, and NOR banding) were performed on 110 specimens representing the four genera of South American primates of the family Callitrichidae: Cebuella (C. pygmaea), Callithrix, groups argentata (C. argentata, C. emiliae, C. chrysoleuca, C. humeralifera, C. mauesi), and jacchus (C. aurita, C. geoffroyi, C. jacchus, C. kuhli, C. penicillata), Leontopithecus (L. chrysomelas, L. rosalia), and Saguinus (S. midas midas, S. m. niger). Mitotic chromosomes are characterized, and the rearrangements distinguishing the karyotypes of the taxa are inferred from arm homologies. The results were then converted into numerical data and submitted to cladistic analysis. The following conclusions were achieved: 1) Five karyotypic classes were observed, which correspond to the five taxa studied. Differences between them are as follows: a) Cebuella (2n = 44, 10 acrocentrics, A + 32 bi‐armed autosomes, bi) and the argentata group (2n = 44, 10A + 32bi) are different from each other due to a reciprocal translocation; b) both can be distinguished from the jacchus group (2n = 46, 14A + 30bi) by a centric fusion/fission rearrangement and a paracentric inversion; c) Leontopithecus (2n = 46, 14A + 30bi) and Saguinus (2n = 46, 14A + 30bi) differ from the jacchus group by a reciprocal translocation and three paracentric inversions; and d) Saguinus is different from the others by one paracentric inversion and pericentric inversions in at least four pairs of acrocentric autosomes. 2) The cladistic analysis separates Cebus (used as an outgroup) from the Callitrichidae groups, which forms a clade. Among the Callitrichidae, marmosets (Cebuella and Callithrix) form a sub‐clade, Cebuella and the argentata group being more closely related to each other than both are to the jacchus group. Tamarins (Leontopithecus and Saguinus) are also quite close, so that if one was not derived from the other, they with the marmosets share a common ancestor. Among the tamarins, Leontopithecus is karyotypically closest to the marmosets, specifically to the jacchus group. 3) Based on the chromosome information and considering the possible direction of the evolutionary changes (primitivity or phyletic dwarfism hypothesis, previously advanced by other authors), it was possible to propose the ancestral karyotypes and to develop two alternatives for the origin, differentiation and dispersion of the callitrichid. Both proposals are plausible, but when the geographical distribution is considered, the phyletic dwarfism hypothesis seems to be the most probable. Am. J. Primatol. 49:133–152, 1999. © 1999 Wiley‐Liss, Inc.