Experimental protein malnutrition during gestation and breeding performance of squirrel monkeys,Saimiri sciureus

The report summarizes our four year experience with the breeding of squirrel monkeys, a New World species used widely in experimental research. Breeding squirrel monkeys in captivity has hitherto been considered capricious, with success in most instances not exceeding 50%. By a combination of hand picking the animals, housing in a harem-type situation with one male to several females, and sound nutrition, a success rate of 85–91% live births to number of pregnancies has been achieved. The rate of stillbirths and abortions in the group maintained on a well-balanced diet did not exceed 10% of the total pregnancies. This compares favorably with any successful breeding program with Old World monkeys, whose reproductive physiology is relatively well understood. It is clear from our studies that adequate quantities of proteins are essential for optimum reproduction. Among the pregnant animals maintained on a diet containing about 50% of their normal requirements of protein (8% calories from a protein source), the incidence of abortions increases significantly. In this group, the rate of abortions to total pregnancies ranges from 40.5 to 61.5%. The females maintained on a protein deficient diet during pregnancy are so protein hungry that an extruded fetus is a welcome food and no time is lost in devouring all of the placenta and the fetus. This type of cannibalism has never been observed among the mothers maintained on a high protein regimen.     

Experimental Plasmodium falciparum cerebral malaria in the squirrel monkey Saimiri sciureus.

Infection of the squirrel monkey, Saimiri sciureus, with several strains of Plasmodium falciparum leads in a proportion of animals to neurological symptoms with a fatal outcome. This first simian model for human cerebral malaria was studied with three strains of parasites, the uncloned Palo Alto(FUP-1) strain, the Palo AltoPLF3 clone MHB11, and the recently monkey-adapted P. falciparum strain IPC/RAY. Cerebral malaria could develop during primo infection of monkeys, whether the animals had been splenectomized or not. It did not occur in all animals and the appearance of neurological symptoms could not be predicted, as it was not related to the degree of parasitemia or duration of parasite infections.     

Cytochemistry of experimental protein malnutrition in primates: effect on the spinal cord of the squirrel monkey, Saimiri sciureus

Synopsis The localization of certain phosphatases, esterases and dehydrogenases in the spinal cord of healthy and severely protein malnourished squirrel monkeys were investigated histochemically. The latter were given drastically reduced levels of proteins in their diets for 15 weeks, and for the purpose of comparison several animals were sacrificed after 9, 11, 13 and 15 weeks on the feeding schedule. Cytochemical investigations were carried out on sections prepared from fresh-frozen spinal cord removed from the animal in the shortest possible time after an appropriate dose of nembutal anaesthesia. The distribution of thiamine pyrophosphatase, inosine diphosphatase, acid phosphatase and ATPase was found to be significantly altered under the impact of dietary abuse. The changes appear to be related to altered protein metabolism, energy transport and general slowing down of the metabolic reactions. The results obtained on phosphatases are reinforced by the distribution of enzymes of the Krebs cycle, pentose shunt and anaerobic metabolic pathways. Whereas the activity of the Krebs cycle enzymes is greatly reduced, the pentose shunt reacts to protein deprivation by increasing the level of activity of its enzymes. Similarly the activities of enzymes of the anaerobic pathway are also enhanced. The significance of these observations and the role of glial cells along with the neuron as a functional unit are discussed.     

Experimental protein malnutrition in squirrel monkeys: cytochemical interaction of nucleolus and cytoplasm in the anterior horn cells of the spinal cord of Saimiri sciureus.

Nuecleolo-cytoplasmic relationships have been studied using histochemical techniques in the spinal cord of healthy neonates compared with those born to mothers malnourished through most of the gestation period, and healthy and severely protein-malnourished young adult squirrel monkeys. Formaldehyde-fixed as well as fresh frozen tissues were used for histological study and for histochemical techniques to demonstrate lipids, carbohydrates, nucleic acids and enzymes of various metabolic cycles. Changes in the neuronal cytoplasm of the low protein animals appear to be related to impaired protein metabolism and energy transport. The nucleolus reacts to cytoplasmic changes by enlarging its size and by active synthesis of secretion of nucleolar material, which is then passed into the cytoplasm through an evagination of the nuclear envelope. The greater the degree of chromatolysis in the cytoplasm, the more active the nucleolus appears to be in terms of its enlarged size and transfer of secretion products into the cytoplasm. It is believed that the perinuclear accumulation of secretion products in the neuronal cytoplasm of the protein-deficient animals has its origin in the nucleolus. Such an accumulation in the severely malnourished animals appears to be a compensatory mechanism for the increased cytoplasmic catabolism and loss of ribonucleoprotein material in order to facilitate additional protein synthesis for cell survival.     

Breeding and rearing squirrel monkeys (Saimiri sciureus) in captivity.

A breeding colony of squirrel monkeys (Saimiri sciureus) was established to provide animals for behavioral research concerned with early development. The origin of the initial breeders was Peru, Colombia, and Bolivia. During the past 10 years, the colony has grown to 125 adult females, 20 adult males, and 120 immature animals of various ages. The annual conception rate for the last 5 years averaged 68%. This resulted in 84% viable births of which 82% survived past 6 months of age. The majority of the births (65%) occurred during June-August, and 87% during May-September. The most efficient and successful breeding strategy was to form mixed-sexed groups of 10--15 females and 2--3 males before the mating season began and to maintain the integrity of these groups with minimal interference. Progeny were reared apart from their natural mother without difficulty, and their growth and development were found to be similar to those of mother-reared monkeys.     

Seasonal changes in plasma testosterone and ejaculatory capacity in squirrel monkeys (Saimiri sciureus)

Seasonal changes in body weight, plasma testosterone and ejaculatory capacity were observed in five intact and two testosterone-implanted castrated squirrel monkeys for a total of 13 months. Electroejaculation was employed for obtaining data concerning ejaculation. In the intact animals, there were significant increases in body weight, ejaculate volume and plasma testosterone during the breeding season. With the exception of one animal, there was also a decrease in ejaculation latency during the season. Seasonal differences in the sperm count and sperm motility were not observed. Testosterone-implanted castrates showed changes in both ejaculate volume and ejaculation latency similar to those seen in intact monkeys during the breeding season. The body weight and plasma testosterone of the castrates remained quite constant throughout the year. Supported by NIH grants HD 00778, MH 21178 and MH 23645.     

Susceptibility of squirrel monkey (Saimiri sciureus) to infection by mammalian schistosomes.

In a study of host-schistosome relationships, the squirrel monkey (Saimiri sciureus) was exposed to 500 cercariae of Schistosoma bovis (Kenya), S. intercalation (Cameroon), S. mattheei (South Africa), 2 strains of S. mansoni (Puerto Rico and South Africa), 2 strains of S. rodhaini (Uganda and Kenya), and Schistosomatium douthitti (North America). It is apparent that the squirrel monkey can be employed as an experimental host for a broad range of mammalian schistosomes. Based upon cercariae-adult worm ratios, it is a good host for S. intercalatum, S. mattheei, the Puerto Rico and South Africa strains of S. mansoni, and Schistosomatium, but only a fair host for S. bovis and the Uganda and Kenya strains of S. rodhaini. Individuality of host-parasite relationships is borne out by the great ranges recorded for egg deposits in different organs as well as by total body egg counts and eggs/worm pair.     

Carcinosarcoma of the maxilla in a squirrel monkey (Saimiri sciureus)

We present the first, to our knowledge, described case of carcinosarcoma of the maxilla in a squirrel monkey. Carcinosarcomas are rare tumors of the upper aerodigestive tract, and consist of carcinomatous and sarcomatous tissue. Histologic analysis revealed a neoplasm composed of an adenocarcinomatous component (epithelial element) and a mesenchymal component (sarcomatous element). Metastatic growth was documented in the lung tissue and the submandibular lymph node. The histolopathologic findings, the pattern of metastasis, and the clinical progression closely resembled those of carcinosarcoma involving salivary glands in humans.     

Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus)

Squirrel monkeys (Saimiri sciureus, Iquitos) were exposed to a sequence of three stresses: A live snake, ether anesthesia, and physical restraint. Plasma cortisol concentrations were determined both following each stress exposure and before and after the sequence of stresses. Dominant males demonstrated lower unstressed plasma cortisol levels than subordinates. Although the form of the relationship between adrenal activity and social dominance differs for the types of stress, dominant animals always show the greatest adrenal reactivity to stress.     

Seasonal changes of serum concentrations of estradiol and progesterone in Bolivian squirrel monkeys (Saimiri sciureus)

Serial measurements of estradiol (E2) and progesterone (P) were used to describe the ovarian cycle of the Bolivian squirrel monkey. Group-caged, sexually mature female squirrel monkeys, housed with males, were sampled daily between 0900 and 1100 hr. Sampling was carried out during the breeding and nonbreeding seasons, for periods of 19–20 days from September 1981 to May 1982. Seasonal differences in serum concentrations of E2 and P were found with low levels of E2 and P and an absence of preovulatory surges of E2 during the nonbreeding season. This pattern was also observed in some animals during the breeding season. An abrupt increase in serum P concentrations in December appeared to signal the onset of cycling. Cycling animals had well-defined peaks of E2 (450–9,500 pg/ml) followed by increasing levels of P, which were >200 ng/ml in some animals. After the breeding season, E2 and P levels returned to their initially low levels. Levels of both steroids in cycling animals were higher than those reported for other primates and for previous measurements made in squirrel monkeys. Cycle length based on time interval between consecutive E2 peaks varied from 6–12 days.     

The number of umbilical vessels in the squirrel monkey (Saimiri sciureus).

The number of vessels present in the umbilical cords of 40 nonsurviving squirrel monkey fetuses an neonates has been determined by gross and histologic examination. Four umbilical vessels were present in 72.5% of the cords and 27.5% contained three vessels. Coincident fetal malformations are noted.     

Nucleolar activity in the primate dorsal root ganglion cells associated with dietary protein malnutrition.

The nucleolar changes in the dorsal root ganglion cells of the squirrel monkey, Saimiri sciureus, have been investigated by the use of histological and histochemical methods in the healthy neonates (born to mothers maintained on 25% protein diet during gestation) and young adults, and compared with those observed in the protein-malnourished neonates (born to mothers maintained on a 8% protein diet during gestation). Also studied were young adults maintained on a high protein diet (25% protein) as well as on a low protein diet (2% protein content) for a period of 15 weeks. Whereas in the healthy animals (neonates and young adults) only a few cells show nucleolar budding and finally their extrusion into the cytoplasm, the protein-malnourished animals show a significantly enhanced nucleolar activity in the form of increased size (3-4 times the original) and active budding either from one focal point or at several places on the body of the nucleolus. In the neurons which show chromatolytic changes, these extrusions migrate to the nuclear membrane, wherefrom they pass on to the cytoplasm through an evagination of the nuclear envelope. Such a migration appears to occur by a focal dissolution of the nuclear membrane. It appears that, under conditions of severe malnutrition and advanced chromatolytic changes in the neuronal cytoplasm, the nucleolar material provides a compensatory mechanism for the increased cytoplasmic catabolism and loss of ribonucleoprotein material in order to facilitate additional protein synthesis for cell survival.     

Biology of reproduction in the squirrel monkey (Saimiri sciureus): II. The ovary

Gross and microscopic observations on the squirrel monkey ovary is described. The luteal tissues are present in two broadly distinct stages of activity. The degree of follicular development appears to be affected by the level of luteal activity. Circumstantial evidences have been presented to indicate that squirrel monkey females may be an induced ovulator.Supported by Grant HDO 1952–03 from the United States Public Health Service.     

Conditions of observation and social distance in groups of squirrel monkeys,Saimiri sciureus

Observation conditions were very influential in determining the social distance among members of groups of squirrel monkeys. With observer visible to the animals and recording by talking into a tape recorder the monkeys did not show a consistent pattern of social distance as reflected by actual space and frequency of bodily contacts, whereas when the observer was concealed, looking through a one-way vision screen and recording silently by marking on paper, the subjects tended to group in unisexual clusters, with that of the females showing higher cohesiveness.     

Experimental protein malnutrition in squirrel monkeys: reaction of the nissl substance in the motor neurons of the spinal cord

Summary Experimental protein malnutrition was induced in juvenile squirrel monkeys by feeding them synthetic diets which contained 2% protein for a period of 15 weeks. Along with their controls who were fed 25% protein food and laboratory monkey chow, groups of monkeys were sacrificed at nine, 11, 13, and 15 weeks of feeding schedule. The spinal cords were stained with chromalum-gallocyanin, PAS, Trichrome Masson's method and Alcian Blue. The neurons and the surrounding glial cells showed significant cytoohemical changes in different groups of the malnourished animals. The motor neurons of the spinal cord showed a varying but dramatic reaction to protein deficiency, which reflects a profound physiological distortion. These observations have been discussed in relation to probable functional derangement under the influence of protein deficiency.