Hormonal and behavioral variation in pied tamarins housed in different management conditions.

Pied tamarins are an endangered Amazonian primate that has limited breeding success in zoos. Unfortunately, little is known about their reproductive biology and adrenocortical activity. Objectives were: (1) determine if fecal hormones could be utilized to monitor gonadal and adrenocortical activity; (2) characterize male and female gonadal and adrenocortical hormones; and (3) determine if there were differences between adrenocortical activity and behavior in a nonbreeding, on-exhibit (NB-ON) pair compared to a breeding, off-exhibit (B-OFF) pair. Fecal samples were collected from four (two males; two females) individuals. Hormones were analyzed for fecal progesterone (FPM), androgen (FAM), and glucocorticoid (FGM) metabolites by enzyme immunoassay. Behavioral observations were conducted for 6 months. Data were collected on instantaneous behavior, location, and all occurrences of intraspecific behaviors. Fecal progesterone metabolites were validated by pregnancy (mean ± SE, pregnant: 28.47 ± 1.60 µg/g; nonpregnant: 8.63 ± 0.89 µg/g). Fecal androgen metabolites were higher (T = 31,971, P < 0.05) in the B-OFF male (863.66 ± 46.30 µg/g) than the NB-ON male (838.63 ± 60.70 µg/g). Fecal glucocorticoid metabolites were validated by response to veterinary procedure with elevated values (7.31 ± 1.48 µg/g) seven times the baseline (0.37 ± 0.04 µg/g) at 24-hr postphysical. Females had higher baseline FGM than the males (P < 0.05). Baseline FGM were higher (P < 0.05) in the NB-ON female (0.93 ± 0.03 µg/g) compared to the B-OFF female (0.38 ± 0.02 µg/g). Similarly, the NB-ON male's FGM baseline (0.71 ± 0.03 µg/g) were higher (P < 0.05) than the B-OFF male (0.21 ± 0.01 µg/g). Behavioral data revealed stereotypical behaviors in the NB-ON pair but no stereotypical behaviors in the B-OFF pair. Fecal hormone monitoring and behavioral analysis may provide insight on the limited breeding success of pied tamarins in zoos.

Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins.

Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus). In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins' 3-week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied 10-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels, whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.

Cerebral amyloid-beta protein accumulation with aging in cotton-top tamarins: a model of early Alzheimer's disease?

Alzheimer's disease (AD) is the most common progressive form of dementia in the elderly. Two major neuropathological hallmarks of AD include cerebral deposition of amyloid-beta protein (Abeta) into plaques and blood vessels, and the presence of neurofibrillary tangles in brain. In addition, activated microglia and reactive astrocytes are often associated with plaques and tangles. Numerous other proteins are associated with plaques in human AD brain, including Apo E and ubiquitin. The amyloid precursor protein and its shorter fragment, Abeta, are homologous between humans and non-human primates. Cerebral Abeta deposition has been reported previously for rhesus monkeys, vervets, squirrel monkeys, marmosets, lemurs, cynomologous monkeys, chimpanzees, and orangutans. Here we report, for the first time, age-related neuropathological changes in cotton-top tamarins (CTT, Saguinus oedipus), an endangered non-human primate native to the rainforests of Colombia and Costa Rica. Typical lifespan is 13-14 years of age in the wild and 15-20+ years in captivity. We performed detailed immunohistochemical analyses of Abeta deposition and associated pathogenesis in archived brain sections from 36 tamarins ranging in age from 6-21 years. Abeta plaque deposition was observed in 16 of the 20 oldest tamarins (>12 years). Plaques contained mainly Abeta42, and in the oldest animals, were associated with reactive astrocytes, activated microglia, Apo E, and ubiquitin-positive dystrophic neurites, similar to human plaques. Vascular Abeta was detected in 14 of the 20 aged tamarins; Abeta42 preceded Abeta40 deposition. Phospho-tau labeled dystrophic neurites and tangles, typically present in human AD, were absent in the tamarins. In conclusion, tamarins may represent a model of early AD pathology.

The cotton-top tamarin (Saguinus oedipus) has five beta-microseminoprotein genes, two of which are pseudogenes.

beta-Microseminoprotein (MSP) is one of the most abundant proteins in human seminal plasma and is secreted from the prostate gland. Its evolution can be traced from primates down to nonvertebrate species such as amphioxus, despite substantial differences in the primary structure. Most mammals are known to have one single MSP gene, but we have previously shown that the cotton-top tamarin and the common marmoset-two New World monkeys-carry several MSP genes. In this study we continue our characterization of MSP genes in the cotton-top tamarin by presenting the full nucleotide sequence of the three previously identified genes, mspA, mspE, and mspJ. A promoter analysis using the luciferase reporter showed that mspE is as transcriptionally active as the single human MSP gene, whereas mspA and mspJ display no activity with this assay. Two novel MSP genes were also identified, mspB and mspH, both of which are pseudogenes. MspB has a frameshift mutation in the third exon resulting in a new C-terminus and premature stop of translation. MspH has the features of a processed pseudogene, originating from a transcript of mspE. It is integrated into the genome together with another processed pseudogene originating from a transcript of the nucleoporin gene NUP88. The MSP genes described in this study probably arose by phylogenetically rather late duplication or retrotransposition, suggesting that they are confined to a limited number of New World monkeys.

Cone pigment variations in four genera of new world monkeys.

Previous research revealed significant individual variations in opsin genes and cone photopigments in several species of platyrrhine (New World) monkeys and showed that these in turn can yield significant variations in color vision. To extend the understanding of the nature of color vision in New World monkeys, electroretinogram flicker photometry was used to obtain spectral sensitivity measurements from representatives of four platyrrhine genera (Cebus, Leontopithecus, Saguinus, Pithecia). Animals from each genus were found to be polymorphic for middle to long-wavelength (M/L) sensitive cones. The presence of a short-wavelength sensitive photopigment was established as well so these animals conform to the earlier pattern in predicting that all male monkeys are dichromats while, depending on their opsin gene array, individual females can be either dichromatic or trichromatic. Across subjects a total of five different M/L cone pigments were inferred with a subset of three of these present in each species.

Carcinoembryonic antigen family of adhesion molecules in the cotton top tamarin (Saguinus oedipus).

Humans and the cotton top tamarin, a model for colitis and colorectal cancer, share carcinoembryonic antigen (CEA) moieties. We quantified CEA in colonic washings and extracts in both, and CEA bands were confirmed by Western blot. We compared CEA-family expression in tissues and serum in the tamarin with that of the common marmoset, which develops colitis but not cancer. CEA levels are higher in tamarin washings compared with humans, and higher than in marmosets extracts (P<0.005). CEA molecular species appear to be specific, and human CEA-family member epitopes are also found in these primates. The higher CEA levels in the tamarin may reflect the overall higher cancer prevalence.

Cloning and expression of the glucocorticoid receptor from the squirrel monkey (Saimiri boliviensis boliviensis), a glucocorticoid-resistant primate.

New World primates such as the squirrel monkey have elevated cortisol levels and glucocorticoid resistance. We have shown that the apparent binding affinity of the glucocorticoid receptor in squirrel monkey lymphocytes is 5-fold lower than that in human lymphocytes (apparent Kd, 20.9 +/- 1.8 and 4.3 +/- 0.2 nmol/L, respectively; n = 3), consistent with previous studies in mononuclear leukocytes isolated from the two species. As a first step in understanding the mechanism of decreased binding affinity in New World primates, we used reverse transcription-PCR to clone the glucocorticoid receptor from squirrel monkey liver and have compared the sequence to receptor sequences obtained from owl monkey liver, cotton-top tamarin B95-8 cells, and human lymphocytes. The squirrel monkey glucocorticoid receptor is approximately 97% identical in nucleotide and amino acid sequence to the human receptor. The ligand-binding domain (amino acids 528-777) of the squirrel monkey glucocorticoid receptor contains four amino acid differences (Ser551 to Thr, Ser616 to Ala, Ala618 to Ser, and Ile761 to Leu), all of which are present in owl monkey and cotton-top tamarin receptors. The DNA-binding domain (amino acids 421-486) is completely conserved among human, squirrel monkey, owl monkey, and cotton-top tamarin receptors. Twenty-two differences from the human sequence were found in the N-terminal region (amino acids 1-421) of the squirrel monkey receptor. None of the substitutions in the ligand-binding domain matched mutations known to influence binding affinity in other species. To determine whether the substitutions per se were responsible for decreased affinity, squirrel monkey and human glucocorticoid receptors were expressed in the TNT Coupled Reticulocyte Lysate System. Expressions of human and squirrel monkey glucocorticoid receptors and a squirrel monkey receptor in which Phe774 was mutated to Leu (F774L) were similar. When expressed in the TNT System, squirrel monkey and human glucocorticoid receptors had similar, high affinity binding for dexamethasone (apparent Kd, 5.9 +/- 1.2 and 4.3 +/- 0.5 nmol/L, respectively; n = 3), whereas the squirrel monkey F774L receptor had lower affinity binding (apparent Kd, 20.4 +/- 2.0 nmol/L; n = 3). Thus, substitutions within the ligand-binding domain of the squirrel monkey glucocorticoid receptor cannot account for the decreased binding affinity of these receptors in squirrel monkey cells. Rather, the binding affinity is probably influenced by the expression of cytosolic factors that affect glucocorticoid receptor function.

Structure and composition of the outer connective tissue sheaths of peripheral nerve.

A regular pattern of parallel reflections with a periodicity of approximately 39 microns has been detected on peripheral nerve fascicles. The reflections have been found to originate from a layer of wavy epineurial collagen fibrils arranged in register around the entire circumference of the fascicle. The waves were observed to be disposed in parallel with the plane of the fascicular sheath and along its axis. The pattern was observed in cut or relaxed fascicles in situ as well as in isolated and split layers of the epineurium. The pattern was not observed on nerve fascicles under tension. An additional structural feature consisting of longitudinally disposed elastic fibres was also detected among the epineurial collagen fibrils. The perineurial collagen associated with sheets of cells was found to be disposed in flattened waves as in the inner layer of the epineurium. The period of the waves, however, was much shorter, in the range of 6-9 microns. From the nature of the wavy structure it can be surmised that on stretching or contraction the sheath length may change, thus accommodating displacement and movement of nerve fibres.

Energy metabolism and thermoregulation in the golden lion tamarin (Leontopithecus rosalia).

Energy metabolism and body temperature were examined in Leontopithecus rosalia, the golden lion tamarin. Total standard metabolic rate (SMR), defined as the metabolic rate of resting, fasted animals within thermoneutrality and during the inactive (nighttime) phase, averaged 381.5 +/- 65.2 ml O2.h-1 (mass-specific metabolic rate 0.520 +/- 0.089 ml O2.g-1.h-1). This value ranges from 73 to 89% of the expected SMR for animals of this body size depending on the predictive equation used. Active-phase resting metabolic rate within thermoneutrality was significantly greater than SMR, averaging 509.0 +/- 44.6 ml O2.h-1 (0.709 +/- 0.062 ml O2.g-1.h-1). Thermal conductance during the inactive phase was 20.3 +/- 2.7 ml O2.h-1.degrees C-1 (0.029 +/- 0.003 ml O2.g-1.h-1.degrees C-1) or 70% of that during the active phase (28.5 +/- 3.2 ml O2.h-1.degrees C-1, 0.042 +/- 0.004 ml O2.g-1.h-1.degrees C-1). These values are about 85% of the mammalian predicted value. Body temperature fluctuated substantially between day (39.6 degrees C) and night (37.4 degrees C). However, none of these differences between circadian phases are unusual for primates (or, indeed, mammals) of similar body size. Although the metabolic rate of Leontopithecus is lower than the predicted one, it is higher than those rates reported for small nocturnal primates with similar food habits. Leontopithecus' modest rates of energy turnover may reflect a combination of phylogenetic constraints, feeding ecology and/or an energy-saving tactic that comprises part of a strategy to maximize reproductive effort. Although callitrichids are often cited as having rapid growth and high reproductive effort, the moderately low SMR of Leontopithecus is consistent with its intrinsic rate of natural increase, which is 90-94% of that expected for a mammal of its body size.

Cholesterol metabolism in New World primates: comparative studies in two tamarin species (Saguinus oedipus and Saguinus fuscicollis) and the squirrel monkey (Saimiri sciureus).

1. Cholesterol metabolism has been characterized in three species of New World primates, the cotton-top tamarin, the saddle-back tamarin, and the squirrel monkey. 2. When fed a diet containing cholesterol, the three species exhibited differing responses of plasma cholesterol levels. 3. Dietary cholesterol absorption was determined and plasma cholesterol die-away kinetics were analyzed in terms of a two-pool model. 4. The results of the analyses of cholesterol turnover are consistent with the observed species-specific differences in plasma cholesterol values and cholesterol absorption. 5. Cholesterol metabolism differs between the two tamarin species, as well as between the tamarins and the squirrel monkey. 6. Implications of species-specific differences between tamarin species are discussed in terms of the use of tamarin species as animal models for comparative studies of cholesterol metabolism and the etiology of cancer and cardiovascular disease.

Studies on the ascorbic acid metabolism of callitrichid monkeys by 14C isotope excretion technique.

Recently it has been found that the two monkey species Callithrix jacchus and Saguinus fuscicollis, both belonging to the same New World monkey family Callitrichidae and held in the same colony under identical conditions, had extremely different serum ascorbate levels. To examine the ascorbic acid metabolism the 14C-excretion of orally given 1-14C-ascorbic acid was studied under conditions of marginal and abundant vitamin C supply and under intentional stress. There were large differences in the mode of 14C excretion between low and high ascorbate supply. The differences were smaller between stress/no stress conditions intraindividually than between the two species, but they were in the same manner. In comparable trials S. fuscicollis reacted such that a higher status of stress can be supposed in this species.

Ascorbic acid in a New World monkey family: species difference and influence of stressors on ascorbic acid metabolism.

Like other simian primates, the New World monkey Callithrix jacchus, marmoset, and Saguinus fuscicollis, tamarin, require ascorbic acid as an essential nutrient. For adult marmosets, a daily intake of 15 mg/kg metabolic body weight was found to be necessary to obtain a serum level above the kidney threshold. A survey of the serum ascorbic acid level of marmosets and tamarins in a breeding colony resulted in a vast divergence between the two species, indicating a higher ascorbic acid requirement for tamarins. Unaccustomed trial conditions or additional stressors resulted in a higher catabolism of ascorbic acid to CO2 in both species, measured with 14C labeled material, compared to a higher rate of renal excretion when the animals were accustomed to the metabolic cage. These isotope excretion studies suggest a different metabolic behavior of ascorbic acid in the two species. This is supposedly caused by a higher sensitivity of the tamarins when subjected to the same conditions as marmosets.

Maintenance of cotton-top tamarins fed an experimental pelleted diet versus a highly diverse sweetened diet.

The future study of colon disease in captive callitrichid colonies may require manipulation of diets. The limited knowledge of the nutritional requirements for these species and the varied diets and supplementations fed to these animals in various colonies suggest the importance of testing the palatability and acceptability of diets for these primates. Individually housed cotton-top tamarins (Saguinus oedipus) were given either the regular Oak Ridge Associated Universities (ORAU) diet (monkey chow slurry, canned diet and supplements), a similar slurry using an experimental natural ingredient diet plus supplements, or the experimental diet without supplements. Neither dry food consumption, body weight, fecal output, nor the histological evaluation of the colons were affected by these diets. Daily intake of protein and calories were higher than previously reported estimates for the species. These results demonstrate that a natural ingredient non-sweetened pelleted diet is palatable for cotton-top tamarins for a period of 3.5 months, however, further testing over longer time periods is necessary. The nonnutritional (e.g. psychological) advantages of providing a highly diverse diet to primates housed in a relatively monotonous environment should be considered before adopting such a diet for an entire colony.

Histochemistry of mucosubstances in Brunner's-gland cells and duodenal goblet cells of two New World monkey species (Saimiri sciureus and Saguinus fuscicollis).

Duodenal goblet cells and Brunner's-gland cells obtained from two species of New World monkeys (Saimiri sciureus and Saguinus fuscicollis) were studied using conventional histochemical methods and by applying a panel of 17 labelled lectins. The secretions of both goblet and Brunner's-gland cells were found to contain neutral mucosubstances, while those of goblet cells also exhibit acid and sulphated carbohydrate components. Lectin binding studies allowed a more detailed analysis of the mucus glycoproteins. Marked differences between the two examined species were not detected. N-Acetyl-galactosamine, galactose, fucose and N-Acetyl-glucosamine were found to be the predominant sugar residues in Brunner's-glands glycoproteins, with mannose and glucose being only minor components.

Phenotypic diversity of the cellular 1,25-dihydroxyvitamin D3-receptor interaction among different genera of New World primates.

High serum of 1,25-dihydroxyvitamin D3 [1,25-(OH)2D3] concentrations and target organ resistance to the hormone are characteristic findings in some New World primates (platyrrhines). We examined the abilities of cultural dermal fibroblasts from individual platyrrhines of four different genera, Aotus, Alouatta, Pithecia, and Saguinus, to internalize and respond to 1,25-(OH)2D3 in an attempt to identify possible phenotypic heterogeneity in the 1,25-(OH)2D3-receptor interaction among them. Results were compared to those from two Old World primates (catarrhines), Pan troglodytes and Pongo pygmaeus. Compared to catarrhine cells, cells from Alouatta, Pithecia, and Saguinus demonstrated 1) a 10-fold decrease in [3H] 1,25-(OH)2D3 internalization capacity; 2) a 2- to 5-fold increase in the apparent internalization constant [3H]1,25-(OH)2D3; and 3) a 3- to 15-fold increase in the 1,25-(OH)2D3 concentration required to elicit half-maximal induction of [3H]25-hydroxyvitamin D3-24-hydroxylating activity (ED50; rank order Sanguinus much greater than Pithecia greater than Alouatta). Although the internalization capacity of cells from two different primates in the genus Aotus was 3- to 4-fold lower than that in catarrhine cells, the internalization constant for hormone and ED50 for 24-hydroxylating activity were similar. These data suggest that the functional 1,25-(OH)2D3-receptor phenotype of the owl monkey, Aotus trivirgatus, is more closely aligned to the catarrhine phenotype than are those of other platyrrhines in the families Cebidae and Callitricidae.

Palatability and digestibility of soya- and milk proteins in Callithricidae.

4 protein sources were tested for palatability, digestibility, influence on bodyweight and consistency of faeces in Callithrix jacchus and Saguinus fuscicollis. The protein sources were incorporated at crude protein levels of 12, 17 and 22% in a pelleted diet. A banana supplement was also fed which reduced the total protein content to 10.7, 14.7 and 18.3%. The test diets, fed for 3 weeks, were well accepted with the milk proteins being slightly preferred. Consumption of the 12% protein pellets was greater than their 22% equivalents. True protein digestibility was calculated to be 97% for lactalbumin, 96% for casein, 90% for soy protein concentrate and 83% for soyabean meal. Changes in bodyweight were negligible. Dry matter of faeces varied between 25% (lactalbumin diets) and 28% (casein diets), but did not change with increasing protein intake. Increasing levels of cellulose, from 2.4 to 7.2% total crude fibre lowered the apparent protein digestibility from 84.3 to 79.2% and the digestibility of dry matter from 82.2 to 76.5%.

Diminished internalization and action of 1,25-dihydroxyvitamin D3 in dermal fibroblasts cultured from New World primates.

We investigated the occurrence of 1,25-dihydroxyvitamin D3 [1,25-(OH)2D3]-resistant osteomalacia in the New World primate colony of Saguinus imperator at the Los Angeles Zoo. The mean serum concentration of 1,25-(OH)2D3 was elevated 5-fold in the New World primates compared to that in their Old World counterparts. The specific internalization of 0.6 nM [3H]1,25-(OH)2D3 by cultured dermal fibroblasts from New World primates was reduced 75% compared to that by cells from Old World primates or man. The decrease in hormone uptake resulted from a decrease in the number of high affinity intracellular binding sites for 1,25-(OH)2D3 and apparently caused a 90-95% reduction in 1,25-(OH)2D3-induced 25-hydroxyvitamin-D3-24-hydroxylase activity. There was no alteration in the capacity or avidity of New World primate serum for 1,25-(OH)2D3 compared to that of serum from Old World primates. These data suggest that the occurrence of vitamin D-resistant osteomalacia in New World primates is the result of decreased high affinity, receptor-mediated uptake of 1,25-(OH)2D3 by the target cell.

Low affinity of the receptor for 1 alpha,25-dihydroxyvitamin D3 in the marmoset, a New World monkey.

Circulating levels of 1,25-dihydroxyvitamin D are 10-fold higher in the marmoset, a New World monkey, than in man; to assess hormone receptors, we evaluated interactions of 1,25-dihydroxyvitamin D3 with virus-transformed lymphocytes. Soluble extracts of transformed lymphocytes from humans showed hormone binding with affinity and capacity similar to that of receptors for 1,25-dihydroxyvitamin D from other human tissues. However, soluble extracts of transformed lymphocytes from the marmoset showed a strikingly lower affinity for 1,25-dihydroxyvitamin D (Kd 2.2 vs 0.27 nM in marmoset vs human) and a mildly lower binding capacity (6.9 vs 16 fmol/mg protein). A defective receptor for 1,25-dihydroxyvitamin D3 could account for resistance of target tissues to this hormone in the marmoset.

Effects of fibre on digestibility and passage time in callithricidae.

The effects of fibre in a pelleted diet on food intake, digestibility of crude fibre, dry matter and energy, on passage time and consistency of faeces were studied in 2 species of Callithricidae, Callithrix jacchus and Saguinus fuscicollis. Coarse cellulose, microcellulose, wheat bran and shrimp meal (chitin = crude fibre) were tested in diets containing 2,4 and 6% total crude fibre, respectively. Digestibility and passage time were determined by inclusion of 0.5% Cr2O3 in the diet. Both celluloses had little influence on the digestibility of energy and dry matter. Digestibility of crude fibre was very low. Wheat bran led to evident depression of energy and dry matter digestibility. High digestibility of crude fibre occurred at the higher levels of inclusion in the diet. Shrimp meal was highly digested with little influence on digestibility of energy and dry matter, indicating considerable degradation of chitin. Wheat bran showed a marked effect, while microcellulose had no effect on passage time, consistency and volume of faeces.

Energy requirements of captive cotton-top tamarins (Saguinus oedipus oedipus).

Food intake of captive cotton-top tamarins was measured at various stages of the life cycle and energy intake was calculated from the results. The intake of adults for maintenance was found to vary around 500 kJ X kg-3/4 X day-1 and to decrease with age. During the last 8 weeks of pregnancy, females increased in weight by about 2 g X day-1 but energy intake did not show a marked rise above the maintenance range. During lactation, their energy intake appeared to double. Measurements of intake at various stages of growth were compared with a model of the energy requirements for growth which predicted intake quite closely. Compared with non-primate mammals of similar size, the growth rate of this species is slow, and because of this, the energy intake during growth and lactation is also comparatively low.