Species and subspecies specificity in urine and scent marks of saddle-back tamarins (Saguinus fuscicollis)

Saguinus fuscicollisproduces scent marks which consist mainly of a mixture of urine and the secretions of circumgenital scent glands. The present study investigates the ability of saddle-back tamarins to discriminate between scent material from conspecifics and corresponding material from other species and to differentiate material from two subspecies of Saguinus fuscicollis.When choices between urine samples from conspecifics and from guinea pigs and choices between urine samples from conspecifics and from common marmosets were offered, the tamarins investigated samples from conspecifics more frequently. Similar responses were obtained when choices between scent marks from saddle-back tamarins and from common marmosets and between scent marks from saddle-back and red-chested moustached tamarins were offered. The tamarins also discriminated between scent marks and between extracts of scent marks from Saguinus f. fuscicollisand Saguinus f. illigeri.In these choice tests, subjects of both subspecies tended preferentially to investigate material from Saguinus f. fuscicollis.The results of these studies show that urine and scent marks contain chemical cues on which recognition of conspecifics can be based. Moreover, the scent marks of closely related subspecies also offer cues which could enable the tamarins to discriminate between them.     

Evidence of hybrid vigor in subspecific hybrids of the saddle-back tamarin (Saguinus fuscicollis)

The effect of hybridization on infant survival was investigated in subspecific crosses of the saddle-back tamarin (Saguinus fuscicollis) at the Oak Ridge Associated Universities (ORAU) Marmoset Research Center (Oak Ridge, TN). Cox Proportional Hazards Regression was used to compare infant survival between (1) pure subspecies, (2) F1, F2, and backcrossed hybrids, and (3) hybrids and their parental subspecies. Also, effects of management changes, sex, and litter size on infant survival were investigated. There were no significant differences in infant survival between the pure subspecies. Also, degree of hybridization (F1, F2, or backcross) did not have a significant effect on infant survival. Progeny of hybrid crosses between S. f. lagonotus and S. f. illigeri was found to have significantly (P < 0.05) higher infant survival than both of their parental subspecies. Individuals born after diet and management changes in the colony had significantly (P < 0.05) higher survival than those born before. There were no significant sex differences in infant survival. Individuals born into triplet litters had significantly (P < 0.05) lower survival than those born into twin litters. These results show heterosis (hybrid vigor) for infant survival in one subspecific S. fuscicollis cross (S. f. lagonotus × S. f. illigeri). The results suggest genetic divergence between the subspecies populations and possible reproductive isolation in the wild. © 1994 Wiley-Liss, Inc.     

A New Subspecies of <Emphasis Type="Italic">Saguinus fuscicollis</Emphasis> (Primates,Callitrichidae)

Saddleback tamarins (Saguinus fuscicollis, S. melanoleucus, and S. tripartitus) occur in the upper Amazon, west of the rios Madeira and Mamoré–Guaporé to the Andes. They currently comprise 13 species and subspecies in Bolivia, Brazil, Colombia, Ecuador, and Peru. Here we report on a previously undescribed subspecies of Saguinus fuscicollis from the interfluvium of the lower rios Madeira and Purus in the central Amazon of Brazil. It is a distinct form with a very pronounced mottling on the back giving the appearance of a saddle, a characteristic shared by the 3 species, and the reason for their collective common name. The lack of a white superciliary chevron and its highly mottled ochraceous-dark brown to black saddle that extends from the scapular region to the base of the tail distinguish the new taxon from Saguinus fuscicollis weddelli. The latter characteristic also distinguishes it from another saddleback tamarin (Saguinus fuscicollis ssp.) that has been reported immediately to the south of its range in the same interfluvium. We compare pelage coloration, external characters and craniometric measurements with its geographically closest relatives, Saguinus fuscicollis weddelli and S. f. avilapiresi, and indicate its probable geographic distribution in a small area between the rios Madeira and Purus, just south of the Rio Amazonas.     

Gonadal control of male scent in the tarmarin Saguinus fuscicollis (Callitrichidae, Primates)

Spontaneous responses to the scent marks of male Saguinus fuscicolliswere tested in experiments where the subjects received a choicebetween scent of intact males and castrated males. Male tamarinsdiscriminated between the odors of intact and castrated males,both on the basis of fresh individual scent marks and on thebasis of marks from several donors pooled in methanol. Theirdiscriminatory response to pooled odors was more pronouncedthan that to individual odors. Females discriminated betweenintact and castrated male scents only on the basis of pooledsamples. This result shows that castration causes changes inthe odor of males. The difference in the response of the tamarinsto individual scent marks as compared to pooled samples is discussedin terms of quantitative changes caused by extraction and ofindividual recognition.     

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.     

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.     

Estimation of immunoreactive testicular androgen metabolites in the urine of saddle-back tamarins

Hydrolysis, extraction, and radioimmunoassay techniques for the estimation of excreted testosterone metabolites in the urine of saddle-back tamarins have been validated and are described. The steroids measured with the testosterone antiserum used are mostly present as glucuronides and sulfates. Immunoreactivity in high-performance liquid chromatography (HPLC) fractions of urinary extracts and in a standard mixture of cortisol, testosterone, and dihydrotestosterone (DHT) were compared. The fractions with the same retention data as testosterone accounted for the major part of the immunoreactivity. Several other immunoreactive compounds of unknown identity were present in low concentrations. These results suggest that testosterone conjugates are the major steroid metabolites measured with this method in Saguinus fuscicollis. Urinary testosterone levels of castrated males were much lower than those of intact males. Testosterone treatment of castrated males resulted in a temporary superphysiological increase in the levels of urinary testosterone and in an individually variable increase in the levels of the minor immunoreactive compounds. These results suggest that estimation of testosterone metabolite levels in urine is a valid method for the assessment of testicular activity in Saguinus fuscicollis.     

Biochemical diversity and genetic distance in two species of the genusSaguinus

A comparative study of 20 blood genetic systems was performed on three populations of genusSaguinus: S. fuscicollis weddelli, S. midas niger, andS. midas midas. Some markers are useful for the characterization of the two species.ADA ⁵, ADA⁶, CA2³, CA2⁴, andES2 ² occur only inS. fuscicollis whileADA ⁴is fixed inS. midas. S. midas midas showed heterozygosity value comparable to those previously obtained for the genusAlouatta. Estimates of genetic distance betweenS. fuscicollis andS. midas species of about 14% are in accordance with those referred to in the literature for interspecific differences. Genetic distances between subspecies ofSaguinus midas were nearly 3%, which is within the range for subspecies.     

Social influences on first reproductive success and related behaviors in the saddle-back tamarin (Saguinus fuscicollis,callitrichidae)

Some aspects of sociosexual behavior and the age at which maturing females experienced their first evident pregnancy and at which maturing males caused their first evident pregnancy were recorded in Saguinus fuscicolliscohabiting from 6 months of age with either an adult or a maturing sex partner. The following pair combinations and trios were studied: young male -young female, young male-adult female, adult male-young female, and adult male-young male-young female. The most frequent type of social interaction between young animals was rough and tumble play, while huddling was the most frequent interaction between young animals and their adult partners. Grooming and sexual interactions were very infrequent and there were no differences in the frequencies of these interactions among subject groups. Maturing females cohabiting with an adult male conceived significantly earlier than maturing females cohabiting with a male of their own age. Maturing males cohabiting with adult females sired offspring at a significantly earlier age than males cohabiting with a female of their own age. Some possible behavioral and physiological processes involved in the causation of early reproductive success in young tamarins cohabiting with adults are discussed. Saguinus fuscicollis fuscicollis andSaguinus fuscicollis illigeri.     

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.     

Model life tables for the smaller new world monkeys

Mortality statistics from five populations of small New World monkeys (includinsg Callithrix jaccus, Leontopithecus rosalia, Saguinus fuscicollis, and Saguinus oedipus) were combined to generate a standard model life table reflecting the mortality patterns of these primates. The model is applied to three individual populations to illustrate a strategy for smoothing and interpolating mortality statistics of varying completeness and quality. © 1993 Wiley-Liss, Inc.     

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.     

Responses of Captive Single- and Mixed-Species Groups of Saguinus to Novel Nonthreatening Objects

The provision of novel objects allows one to probe for behavioural differences among species. This is particularly relevant when studying species that form mixed-species groups, as divergent responses may provide clues to the advantages that individuals gain from associating. We compared the responsiveness to novel objects in captive single- and mixed-species groups of saddleback (Saguinus fuscicollis) and red-bellied (Saguinus labiatus) tamarins to determine the influence of a congener. We tested groups with novel objects placed near the top, the middle, and on the floor of their enclosures and measured latency to approach and touch them. We tested predictions related to differences in lifestyle patterns under natural conditions. As we predicted, S.labiatus, which usually occur at a higher mean height in the forest than their congeners, responded to objects placed near the top of the enclosure significantly quicker in both single- and mixed-species groups. S. fuscicollis responded to objects placed on the floor quicker, and in mixed-species groups S. fuscicollis approached them before S. labiatus did. There were specific differences in median touch–approach time (T-A): Saguinus fuscicollis had a shorter T-A time than that of S. labiatus, which can be related to their manipulative foraging style. Reaction times decreased in mixed-species trials for both species, suggesting that the reaction of one species may effect the congener. Both species may benefit through association, though the dominance of Saguinus labiatus over S. fuscicollis may limit the advantages to S. fuscicollis. Over all our study supports the idea that cross-specific social facilitation is an important consequence of mixed-species groups of Saguinus.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

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.     

The impact of cropping on wild populations of Saguinus mystax and Saguinus fuscicollis in Peru

A transect census technique was used to estimate the population densities of Saguinus mystax and Saguinus fuscicollis at two sites in Peru. Cropping of these two species had occurred five years before the census at one site and two years before at the other. The populations of S. mystax at both sites had recovered completely from cropping, and the relationship between S. mystax and S. fuscicollis had not been altered at one site and had been reversed in favor of S. mystax at the other.     

Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis

From field data collected in the Amazon Basin of northeastern Peru, I present evidence that moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins maintain detailed knowledge of the distribution and location of many tree species in their home range. During the wet season months of October through December 1984, fruits and exudates from 20 tree species and over 150 individual trees accounted for 75% of plant feeding time. These trees exhibited a patchy distribution; mean nearest-neighbor distances between trees of the same species averaged 148 meters. Moustached and saddle-back tamarins visited an average of 13 trees per day, concentrating their feeding efforts on 4–11 individual trees from a small number of target species. In 70% of all cases the nearest tree of a given species was selected as the next feeding site. Movement between these sites was characterized by relatively straight-line travel. It is argued that S. mystax and S. fuscicollis offset the patchiness component of the fruit and exudate part of their diet through goal-directed foraging and an ability to compare accurately the distances and directions from their present location to a large number of potential feeding trees.     

Immunological Studies on the Tuber-bearing Solanums III. Variability within S. bulbocastanum and its hybrids with species in series Pinnatisecta

It was shown in the previous paper of this series that the Mexicanspecies Solanum bulbocastanum, S. cardiophyllum subsp. cardiophyllumand subsp. ehrenbergii, S. michoacanum and S. pinnatisectummay be differentiated to some extent by the double diffusiontechnique, and more fully by immuno-electrophoretic analysis.Above all, the relative electrophoretic mobilities of certaincomponents, as expressed by the index have been found to be very constant for each species, with the apparent exception of S. bulbocastanum. A detailed investigation of S. bulbocastanum has now shown thatalthough the many clones of this species appeared similar whenexamined by double diffusion, differences were exposed by immuno-electrophoreticanalysis. In particular, the values fell into two discrete groups, 0.15 to 0.23 and 0.30 to 0.46. Theplants in these groups had been collected from Oaxaca and Guatemala,and from Central Mexico, respectively. Most of the former grouphad been identified as S. bulbocastanum subsp. partitum, andall the latter group as subsp. bulbocastanum and subsp. dolichophyllum.Not only was the wide variation in values of index resolved into two meaningful groups, but it was also found thatall lines within any one collection had almost identical values. The index value for S. cardiophyllum subsp.cardiophyllum is 1.0, and for subsp. ehrenbergii is 0.7. The F₁ hybrids between either ofthese subspecies and S. bulbocastanum had fairly uniform valuesclose to the calculated means of the parental values. The shapesof the leaves of these hybrids were also uniform and more orless intermediate between those of the parents in each case. The F₂ hybrids between S. bulbocastanum and S. pinnatisectum,and also the triple hybrids between these two species and eitherS. cardiophyllum or S. michoacanum, showed a wide range of valuesof index and of leaf shapes, with partial segregation towards the parental types. The serological andmorphological characters segregated independently. S. X sambucinum was found to have a wide variation in serologicaland morphological characters. This variation was consistentwith the theory that S. X sambucinum is a natural hybrid betweenS. pinnatisectum and S. cardiophyllum subsp. ehrenbergii. Within the groups of species investigated, the relative electrophoreticmobilities of certain antigens as displayed by immuno-electrophoreticanalysis were found to vary significantly in different species,in different subspecies of the same species, and in specieshybrids.     

Sexual dimorphism in scent substances and cuticular lipids of adult Papilio protenor butterflies

Adults of Papilio protenor demetrius emit a faint odour; the male odour is notably stronger than that of the females. The extracts of whole individuals of each sex comprised 53 compounds regarded as cuticular lipid components, of which the 17 major compounds were straight-chain alkanes and alkenes with 23-31 carbon atoms, higher fatty acids, long-chain aliphatic ketones, squalene, and cholesterol. However, highly volatile compounds were not detected in the whole individual extracts. Eight of the 17 major compounds showed a significant sex difference in relative abundance per individual. Principal component analysis, using the major compounds as variables, revealed a marked sexual dimorphism in the chemical composition of cuticular lipids. From the extracts of 10 dissected individuals of each sex, 21 highly volatile compounds were identified in amounts of less than 200 ng/individual. Among them, linalool and 2,3-butanediol showed a significantly larger amount in males than in females, indicating that the adult odour is also sexually dimorphic. Moreover, both sexes shared several odoriferous compounds, such as heptanal, nonanal, methyl salicylate, benzyl alcohol, and benzoic acid. The faint odour of P. protenor adults, perceivable by the human nose, appears to originate from these volatile compounds.     

Population recovery in the moustached tamarin (Saguinus mystax): Management strategies and mechanisms of recovery

In 1978, 66% of the individuals of Saguinus mystax and 9.5% of Saguinus fuscicollis were cropped from a population at the Yarapa river, Peru. The effects of cropping on the remaining tamarin population were evaluated by conducting censuses in 1981 and 1982 and by trapping and release of Saguinus mystax in 1981. Three hundred kilometers of trail were covered in the censuses, and all the groups within the 1.9-km² study area were located. Within three years after cropping, the population of S. mystax had increased by 124%, more than double the size left in 1978. Increased reproductive rate, early breeding, and reduced infant mortality contributed to the recovery. On the other hand, S. fuscicollis had decreased by 12% in the three years following the cropping but had increased in the fourth year to a level slightly below the precropping density. The cropping of more S. mystax than S. fuscicollis might have contributed to the decline of the latter. The cropping of a sizable percentage of S. mystax from a natural population does not seem to impair its recuperative powers. It may take longer than four years for a population exhibiting high density, such as that at the Yarapa site, to recover completely.