Subspecific genetic differences in the saddle-back tamarin (Saguinus fuscicollis) postcranial skeleton

Saddle-back tamarins (Saguinus fuscicollis) have been differentiated into subspecies based on coat color and facial morphology. Morphology of first-generation genetic hybrids can provide an understanding of population differences and evolution that may otherwise be difficult to obtain. This study compares postcranial morphology in two hybrids of saddle-back tamarins (S. f. illigeri x S. f. lagonotus and S. f. illigeri x S. f. leucogenys) to the purebred subspecies. We examine whether postcranial morphology differs between the purebred subspecies and their hybrids, and whether hybrids exhibit heterosis indicative of genetic differences between the parental subspecies. Fifty postcranial dimensions, or traits, were measured on 287 S. fuscicollis skeletons. Measurements were corrected for sex differences and environmental differences (wild-derived or laboratory-born). Females were larger than males for most postcranial dimensions, especially in the pelvis. Significant environmental differences were found throughout the postcranial skeleton, with wild-derived animals generally larger than animals born in the laboratory. Significant heterosis was found for six postcranial traits in the S. f. illigeri x S. f. leucogenys cross, and heterosis was found for 15 postcranial traits in the S. f. illigeri x S. f. lagonotus cross. These results suggest that subspecies differences in skeletal morphology are generally due to genetic rather than environmental differences. The subspecies appear to represent geographic isolates that differ in gene frequencies and directional dominance for skeletal traits.     

Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis):evidence from hybrids

The subspecies of saddle-back tamarins (Saguinus fuscicollis) are known to be chromatically and morphologically diverse but little is known of the genetic basis for the observed morphological variation. The morphology of first generation subspecific hybrids can be compared to that of the parental subspecies to provide information on the extent and nature of genetic differences in morphology between subspecies. We compare two groups of saddle-back tamarin hybrids (S. f. illigeri × S. f. lagonotus and S. f. illigeri × S. f. leucogenys) to pure-bred members of their parental subspecies. These crosses were examined for heterosis, caused by allele frequency differences between the subspecies in combination with directional dominance. Thirty-nine craniofacial measurements were derived from three-dimensional coordinates of landmarks on 355 adult tamarin skulls. These measurements were corrected for sex differences and differences due to environment (wild-derived vs. laboratory-born) prior to analysis of hybridity. Sex differences were minimal for these traits. Environment had a more significant effect on craniofacial morphology. Laboratory environments produce larger faces but smaller orbits, anterior cranial vaults, and cranial bases. Significant heterosis was found for many individual traits and for the first principal component representing size and size-related shape measurements in the S. f. illigeri × S. f. lagonotus cross. The smaller samples involved in the S. f. illigeri× S. f. leucogenys cross led to a much lower number of statistically significant results, although most traits did display heterosis. Heterosis for craniofacial size was nearly statistically significant. These results suggest that there are large differences in allele frequencies among these subspecies of saddle-back tamarin for genes affecting craniofacial morphology. Based on these data we suggest that these subspecies are likely to be independent, largely isolated, evolutionary units. © 1993 Wiley-Liss, Inc.     

Temperature-metabolism relations in the cotton-top tamarin (Saguinus oedipus) model for ulcerative colitis

Examination of temperature-metabolism relations found no significant differences between thermoregulation of temperature housed laboratory cotton-top tamarins (Saguinus oedipus) and wild tamarins in Colombia, S.A. The results indicate that tamarins do not acclimate to a temperate environment and are metabolically stressed at T_a less than 32°C. This is consistent with an hypothesis of chronic metabolic stress as a factor in the etiology of cotton-top tamarin colitis, which is restricted to captive populations and not found in wild tamarins.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

Locomotor behavior and feeding ecology of the panamanian tamarin (Saguinus oedipus geoffroyi,callitrichidae, primates)

The Callitrichidae are a family of New World primates that exhibit a complex of behavioral and morphological characters reputedly similar to those of tree squirrels of the genus Sciurus.In particular, the locomotor behavior of tamarins and marmosets has been described as “squirrel-like. ” In this paper I describe a field investigation of the locomotor behavior and ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi)and the redtailed squirrel (Sciurus granatensis).From January through August 1978, a total of 1200 hr was spent observing freeranging populations of tamarins and tree squirrels in an area of secondary forest on the Pacific Coast of Panama. Observations were made using an instantaneous time sampling technique. Individual activity records were collected on focal animals and recorded at 2.5-min intervals throughout the day. The following information was collected: (a) nature and structure of the substrate exploited, (b) activities on these supports and/or types of resources procured, and (c) body posture involved in the use of these supports. Data presented indicate major differences in substrate preference and positional behavior in tamarins and tree squirrels. Unlike squirrels, tamarins avoid vertical and sharply inclined supports during travel. Movements through the canopy is accomplished by a series of long leaps which begin and end on thin terminal supports. However, the Panamanian tamarin spent numerous hours clinging to large vertical trunks while feeding on plant exudate. Gums comprise 23.O% of the noninsect portion of the tamarin diet. The relationships between small body size, claw-like nails, substrate preference, and positional behavior are discussed. Claw-like nails enable this primate to exploit a food resource that would otherwise be inaccessible. The interrelationship between environment, behaviour, and morphology provides a frameworks from which to understand callitrichid adaptations. These adaptations are not convergent with those of the sciurid rodents. An earlier draft of this paper was presented at the 48th Annual Meeting of the American Association of Physical Anthropologists, San Francisco, April 1979.     

Trichobezoars in two saddleback tamarins (Saguinus fuscicollis)

Two captive-born Saddleback tamarins (Saguinus fuscicollis) died unexpectedly in the primate colony at the Peruvian Primatological Project. At necropsy, a firm, mobile, oblong, obscure mass was discovered in the stomach of each. They were removed and determined to be trichobezoars.     

Endocrine monitoring of the ovarian cycle and pregnancy in the saddle-back tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine

Direct measurements of urinary immunoreactive estrone conjugates (E1C) and pregnanediol glucuronide (PdG), were applied to monitoring the ovarian cycle (n = 9) and pregnancy (3 full term pregnancies, 2 mid-term abortions) in Saguinus fuscicollis. During the ovarian cycle, urinary E1C concentrations revealed a high degree of day-to-day variability and appeared to be uninformative in reflecting cyclic ovarian function. In contrast, PdG was a reliable indicator of ovarian cyclicity with excretion patterns corresponding well with plasma progesterone profiles. Luteal phase PdG concentrations were on average 4–7–fold higher than corresponding follicular phase values. On the basis of changes in circulating progesterone, a mean cycle length of 25.7 ±1.0 days with an average follicular phase of 7.1 ± 0.6 days and a mean luteal phase of 18.6 ± 0.7 days, was found (n = 14 cycles). Following conception, both urinary steroid conjugate concentrations increased and elevated levels were maintained beyond the normal luteal phase length, allowing pregnancy to be determined at around day 25–30. During mid- to late pregnancy, PdG levels declined while E1C concentrations continued to be elevated until approximately 6 weeks before parturition when a decrease occurred. Both hormones showed a clear and rapid fall to follicular phase values following termination of pregnancy at either parturition or mid-term abortion. Post partum ovulations (n = 5) occurred on average 17–18 days following birth with four ovulations leading to conceptions. The results demonstrate the potential of urinary steroid conjugate analysis as a practical and reliable method for non-invasive monitoring of reproductive status in the female saddle-back tamarin. © 1995 Wiley-Liss, Inc.     

Spontaneous pathology of the common marmoset (Callithrix jacchus) and tamarins (Saguinus oedipus, Saguinus mystax)

Background  Marmosets and tamarins are increasingly used in research, but their pathology remains poorly defined compared with Old World primates.

Methods  Necropsy records of 129 marmosets and 52 tamarins were reviewed; none was used experimentally.

Results  The most common marmoset lesions were dehydration, emaciation, nephritis, colitis, and inanition. The most common tamarin lesions were dehydration, ascites, emaciation, and congestive heart failure. Colitis and heart disease were the most common cause of death in marmosets and tamarins, respectively. Immature marmoset and tamarin deaths often occurred within the first month of life. Immature marmosets usually died from inanition, stillbirth, and colitis; immature tamarins from atelectasis, stillbirth, heart failure, and colitis. Lymphoma was the most common neoplasm for both marmosets and tamarins.

Conclusion  The findings were similar to prior reports with differences in frequency and severity. We report the first case of endometriosis in a marmoset.     

Taxonomic status of Saguinus tripartitus (Milne-Edwards, 1878)

A review of specimens and field notes of Carlos Olalla and his sons showed that they collected Saguinus tripartitus and Saguinus fuscicollis lagonotus at the same place on the right bank of the lower Rio Napo in Peru. Thus, these two forms are sympatric, although they probably occur in different habitats. Therefore, Saguinus tripartitus should be treated as a distinct species, not as a subspecies of Saguinus fuscicollis.     

A field study of Geoffroy's tamarin (Saguinus geoffroyi) in Panama

A 3-month field study was conducted in Panama to determine presence and relative abundance of Saguinus geoffroyi, the Geoffroy's tamarin, and status of its habitat (see Acknowledgments for taxonomic note). This primate has a wide geographical distribution in eastern Panama; however, local distribution is highly variable. Tropical forest habitat is rapidly being converted for agriculture and timber. Areas where human access was strictly limited showed tamarin densities significantly greater than in less protected areas. Disturbance has a distinct impact on population densities. There may also be a relationship between tamarin abundance and specific types of vegetation. Future actions regarding the conservation of S. geoffroyi and its habitat are recommended.     

Adrenal myelolipoma in the cottontop tamarin (Saguinus o. oedipus)

Two cases of myelolipoma in the cottontop tamarin (Saguinus o. oedipus) were found unequivocally within the adrenal gland, supporting an earlier suggestion that the adrenal gland was the possible origin of a juxtarenal myelolipoma in the same species. In the present study a 30-mm-diameter myelolipoma was present in the adrenal gland in case 1, whereas in case 2 the myelolipoma was only detected on histological examination. In case 1, changes in the adrenal gland were considered to be of minor clinical significance, whereas in case 2 the myelolipoma was an incidental finding.     

Complex patterns of morphological and mtDNA variation in Lacerta perspicillata (Reptilia; Lacertidae)

Lacerta perspicillata is a north-west African lacertid lizard that shows considerable intraspecific variation, with three subspecies described on the basis of colour pattern and body size. Recent observations of a population containing two morphological forms and more than one deep genetic lineage, as well as an apparent lack of concordance between forms and genetic lineages, suggest that the complexity is greater than previously thought. To analyse and quantify this variation, we studied the variability within this species at two levels: (1) external morphology (multivariate analysis of scalation, body dimensions, and colour pattern) and (2) mtDNA (sequencing and single-strand confirmation polymorphism analysis). Fifty-two individuals were studied at Taza, northern Morocco. Two morphological groupings (ostensibly representing two previously described subspecies) and two deep mtDNA lineages were detected at this site, with complete correspondence between the two. This, together with an apparent lack of hybrids, would normally support respective full species recognition. However, analysis of 98 individuals from other populations demonstrated that the situation is highly complex with the same genetic lineages having reversed morphotypes in other areas, making such a designation difficult. Across the other studied populations, we found no support for any of the currently recognized subspecies. The lack of congruence between mtDNA lineages and morphometric patterns (in some cases) and the morphological similarity among lizards from different lineages suggest ecophenotypic convergence or multiple introgressive hybridization. The study highlights the tremendous complexity that may exist within a taxon and the inadequacy of older alpha-taxonomy based designations in describing it.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 479–490.     

Mortality causes of the moustached tamarin (Saguinus mystax) in captivity.

From January 1987 to November 1990, 125 adult Saguinus mystax died at the CRCP. Enteritis/colitis (26%), hypoglycemia/cachexia (19%), and parasitic enteritis (13%) were the most common causes of death. Less common were purulent peritonitis (9%), lobular pneumonia (8%), and hemorrhagic gastroenterocolitis (6%). These results confirm the high frequency of gastroenteric lesions reported in Callitrichidae in captivity.     

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.     

Bilateral giant myelolipoma in the adrenal of a cotton-top tamarin (Saguinus oedipus)

Abstract: A rare case of bilateral adrenal myelolipomas in a female cotton-top tamarin is reported. Large bilateral masses in the adrenal glands were composed of mature adipose cells containing varying amounts of hematopoietic cells of the myeloid, erythroid, and megakaryocyte series. The gross and histologic features of this case closely resemble human “giant” adrenal myelolipomas.     

Hyperossification in miniaturized toadlets of the genus Brachycephalus (Amphibia: Anura: Brachycephalidae): Microscopic structure and macroscopic patterns of variation

Species of the genus Brachycephalus, have a snout‐vent length of less than 18 mm and are believed to have evolved through miniaturization. Brachycephalus ephippium, is particularly interesting; because its entire skull is hyperossified, and the presacral vertebrae and transverse processes are covered by a dorsal shield. We demonstrate in this paper that, at the macroscopic level, a completely hyperossified skull and dorsal shield occur only in B. ephippium, but not in B. ferruginus, B. izechsohni, B. pernix, B. pombali, B. brunneus, B. didactylus, and B. hermogenesi. An intermediate condition, in which the skull is hyperossified but a dorsal shield is absent, occurs in B. vertebralis, B. nodoterga, B. pitanga, and B. alipioi. The microscopic structure of hyperossification was examined in skulls of B. ephippium and B. pitanga, revealing a complex organization involving the presence of Sharpey fibers, which in humans are characteristic of periodontal connections. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Ecological study of the saddle backed tamarin (Saguinus fuscicollis) in Northern Bolivia

The author carried out an ecological survey of the saddle backed tamarin (Saguinus fuscicollis) in the Pando, northern Bolivia, from July to December 1979. It was found thatS. fuscicollis formed a family group consisting of two to seven individuals and spent almost all the daytime in moving to forage insects, although it fed mainly on fruits of the family Moraceae. Primary forest was preferred for sleeping sites, whereas the animals spent more hours in secondary forest than in primary forest in their home range. Marking sites were concentrated in the center of the home range but encounter behaviors tended to take place near the borderlines of the home range. It was also found that infants began feeding on fruit at about 5 weeks of age, whereas they shared insects obtained by their mothers until about 10 weeks of age.     

Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal component analysis

Constancy of variation/covariation structure among populations is frequently assumed in order to measure the differential selective forces which have caused population differentiation through evolutionary time. Following Steppan ([1997] Evolution 51:571-594), this assumption is examined among closely related tamarin species (genus Saguinus), using two distinct approaches applied to the task of evaluating similarity in patterns of morphological variation: common principal component analysis and matrix correlations. While the results of these analyses may appear contradictory, closer examination reveals them as complementary, highlighting the wisdom of combined methodologies. Overall, the results reveal a close relationship among the morphologically based variance structures of the tamarin species a relationship whose pattern is consistent with the pattern of phylogenetic relatedness as found via a molecular genetic study. More specifically, both methodological approaches provide some support for divergence of S. geoffroyi and S. oedipus (with regards to their patterns of morphological variation) from other tamarin species. This suggests that variance/covariance structure may have diverged through evolutionary time in the tamarin lineage, placing assumptions of constancy in doubt.