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.     

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 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.     

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.     

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.     

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.     

Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon lowlands of Peru

In the Amazon lowlands of Peru, Aotus nancymai and A. vociferans were observed to use four different types of sleeping sites: (1) holes in the trunks and branches of dry or senescent trees; (2) concavities in polyaxial branching nodes of trees protected by dense entanglements of creepers, climbing plants, vines, and masses of diverse epiphytes; (3) complex sites among masses of epiphytes, climbers, and vines; and (4) simple sites among thickets and dense foliage. Each type is described. There was competition and sharing of sleeping holes between Aotus and other nocturnal arboreal mammals.     

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.     

Spontaneous rat bite fever in non-human primates: a review of two cases

Rat bite fever is a worldwide zoonotic, non-reportable disease. This entity encompasses similar, yet distinct, disease syndromes caused by Streptobacillus moniliformis or Spirillum minus. Naturally occurring rat bite fever has not been previously described in non-human primates. This report describes two cases of non-human primate rat bite fever caused by S. moniliformis; a rhesus macaque (Macaca mullata) with valvular endocarditis, and a titi monkey (Callicebus sp.) with septic arthritis. Potential sources of infection included direct contact, and ingestion of surface water or feed contaminated with rodent feces.     

Family composition and the characteristics of parental care during the nursing phase of captive common marmosets (Callithrix jacchus)

Cooperative care of the young by the father, older siblings, and unrelated group members is observed in a number of species, but inCallithrix jacchus parental care by the father is considered to be part of the reproductive behavior of the species. Nevertheless, the way the presence of potential helpers influences the costs of caring for the parents is not well understood. In this study we describe the suckling phase of youngC. jacchus, in families with and without older siblings, assessing the effect of siblings on the amount of care given by the father and mother. Six family groups were observed: three consisting of the mated pair and two newborn infants, and three with one or two additional sub-adult siblings. Our results suggest that the presence of older siblings as helpers affects the parents' participation in caregiving by altering maternal investment through the control of nursing and by reducing the costs of carrying for the father.     

Comparative chromosomal study of five taxa of genus Callithrix,group Jacchus (Platyrrhini,primates)

The karyotypes of four marmoset species of the Callithrix jacchus group (C. aurita, C. kuhlii, C. geoffroyi, and C. penicillata) were investigated. The patterns of G-, C-, and NOR-bands of these karyotypes were compared with those of C. jacchus, previously described, in order to clarify the taxonomic relationships of this species group. All species present 2n = 46, 14 uni- and 30 biarmed autosomes, a median size submetacentric X chromosome, and the same NOR-band patterns. No rearrangement or constitutive heterochromatic variation differentiate these species, which differ only in the morphology of the Y chromosome. The data obtained indicate that, from the chromosomal point stand, the marmoset species of C. jacchus group constitute a homogeneous clade. Am J Primatol 41:53–60, 1997. © 1997 Wiley-Liss, Inc.     

Species differences in adrenocortical activity of new world primates: Response to dexamethasone suppression

The effect of dexamethasone-induced alteration of adrenocortical activity was assessed in two species of New World primates: Saimiri sciureus and Callicebus moloch. Basal and stress levels of corticosteroids were determined following treatment with three doses of dexamethasone (0, 50, or 500 μg/kg). Saimiri showed substantially higher basal levels of corticosteroids than did Callicebus and a greater incremental corticosteroid response to physical restraint. Dexamethasone was found to reduce basal corticosteroids in both species, although this effect was greater for Callicebus than for Saimiri Moreover, the adrenocortical response to physical restraint was reduced by dexamethasone treatment in Callicebus but not in Saimiri. The pattern of results suggests that the species differ in the mechanisms mediating adrenocortical activity.     

Lighting requirements of nocturnal primates in captivity: A chronobiological approach

From the results of chronobiological studies in 11 Aotus lemurinus (trivirgatus) griseimembra, 3 Galago garnettii, 5 Galago senegalensis, and 6 Microcebus murinus, inferences can be made on the most suitable lighting conditions for nocturnal primates kept in captivity. In each species studied light controls the daily periodic course of activity in a dual way. First, the light-dark (LD) cycle acts as the main Zeitgeber, entraining the endogenous circadian timing system (CTS) to the environmental periodicity. Second, the prevailing light intensity has a direct species-specific inhibiting or enhancing effect, masking the level of activity predetermined by the CTS. Marked inhibition of activity is caused especially by low light intensities during dark-time (D-time), which can also lead to drastically reduced food intake (e.g., in Aotus). Therefore, high-amplitude LD cycles should be applied which guarantee a stable external and internal synchronization of the various circadian rhythms of the organism, with a D-illumination intensity high enough to prevent light-induced impairments of the behavior of the animals. Up to now LD cycles of 12:12 h (100–1,000:0.5–0.01 lx; ≥5,000°K) have proved to be most suitable. Only in Microcebus should the D-illumination be reduced to about 10^?4 lx. Moreover, it must be considered that species with a photoperiodically controlled reproduction cycle require specific alterations of the L-time:D-time ratio.     

Predator avoidance behaviour in the buffy-headed marmoset,Callithrix flaviceps

The predator avoidance behaviour of a free-ranging group of buffy-headed marmosets,Callithrix flaviceps, was recorded in detail during the course of a long-term study of behavioural ecology at the Fazenda Montes Claros, southeastern Brazil. Four distinct patterns of predator avoidance behaviour, each with specific vocalisations, were recognised and are described here. The selection and use of sleeping sites by the study group are also described. An analysis of the records indicates that these small monkeys are generally most vulnerable to predation by aerial raptors. Variations in the frequency of alarm calls also indicate that the marmosets tend to be more vigilant at higher levels in the forest and when the leaf cover is less extensive. The implications of group size and social structure for both the evolution and the efficacy of the anti-predator behaviour of marmosets are also discussed.