Isospora callimico n sp, (Coccidia: Eimeriidae) from Goeldi's marmoset (Callimico goeldii).
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Benefits of polyspecific associations for the Goeldi's monkey (Callimico goeldii).
Polyspecific associations are an important component of Callimico goeldii behavior and ecology. On average, Callimico goeldii was found in proximity to or in vocal contact with Saguinus troops (S. fuscicollis and S. labiatus) during 53% of all time intervals sampled. Polyspecific associations varied considerably between seasons, however, with association rates peaking during the wet-season month of February (89%) and declining in the dry season, with the lowest rate (13%) in July. The primary benefits of associations appear to be an increased use of the lower and middle canopy, and an increase in feeding behaviors during the wet season. Thus, Callimico goeldii appear to benefit most from associations during the wet season when fruits are its principal food source. Fruits are eaten more in the forest canopy than in the understory; thus, an increase in height use likely permits an increase in the fruit resources on which Callimico goeldii can forage and feed. In addition, Saguinus groups, with their smaller home ranges, are likely to be more knowledgeable than Callimico goeldii about the location and abundance of ripe fruits in their home ranges. Thus, Callimico goeldii may parasitize Saguinus for their fruit knowledge by following them through their ranges. In the dry season, limited dietary overlap between Callimico goeldii and Saguinus groups is likely to make associations less beneficial for Callimico goeldii as they adopt different foraging and ranging strategies.
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A reexamination of the phylogenetic position of Callimico (primates) incorporating new mitochondrial DNA sequence data.
The New World monkeys are divided into two main groups, Callitrichidae and Cebidae. Callimico goeldii shares traits with both the Cebidae and the Callitrichidae. Recent morphological phyletic studies generally place Callimico as the most basal member of the Callitrichidae. In contrast, genetic studies (immunological, restriction fragment, and sequence data) have consistently placed Callimico somewhere within the Callitrichidae, not basal to this clade. A DNA sequence data set from the terminal 236 codons of the mitochondrial ND4 gene and the tRNA(His), tRNA(Ser), and tRNA(Leu) genes was generated to clarify the position of Callimico. The sequences of 887 base pairs were analyzed by maximum-parsimony, neighbor-joining, and maximum-likelihood methods. The results of these various methods are generally congruent and place Callimico within the Callitrichidae between the marmosets (Callithrix and Cebuella) and the tamarins (Saguinus and Leontopithecus). Combined analyses of all suitable nuclear and mitochondrial gene sequences confirm the position of Callimico between the marmosets and the tamarins. As available molecular evidence indicates that Callimico is more closely related to the marmosets than to the tamarins, a reconsideration of the morphological evidence in light of the consensus tree from DNA sequence analyses is warranted. The marmosets and tamarins share four morphological characters (loss of the third molar, loss of the hypocone, reduced body size, reproductive twinning). Dwarfism may have evolved repeatedly among the Callitrichidae. It is well-known that the loss of a character can occur many times independently. The reproduction of marmosets and tamarins is extremely specialized and it is difficult to imagine that this complex and unique twinning system evolved separately in marmosets and tamarins. However, it is possible that a secondary reversal to single offspring took place in Callimico.
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The Callimico goeldii (Primates, Platyrrhini) genome: karyology and middle repetitive (LINE-1) DNA sequences.
Callimico goeldii (Goeldi's marmoset) is a neotropical primate with 2n = 47,X1X2Y in the male, and 2n = 48,X1X1X2X2 in the female, due to a Y-autosome translocation. Karyological comparisons of Callimico, Callithrix jacchus and Cebus apella suggest that Callimico is a member of the Callitrichidae. Isozyme data and restriction mapping of LINE-1 repetitive elements in these species and in a variety of other neotropical primates confirm these findings and supply strong evidence for including Callimico in the Callitrichidae.
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Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil.
We present the results of a 4-month field investigation of positional behavior, vertical ranging, and species differences in limb proportions and body mass in a mixed-species troop of Saguinus fuscicollis, Saguinus labiatus, and Callimico goeldii in northwestern Brazil. Despite certain similarities in overall positional repertoire, patterns of positional behavior varied significantly between species. Travel in Callimico occurred principally in the lowest levels of the canopy, and was characterized by an exaggerated form of hindlimb-dominated bounding (bounding-hop), and leaping to and from vertical trunks (55.1% of leaps). In contrast, saddle-back tamarins traveled in the lower and middle levels of the canopy, and engaged in a range of leaping behaviors, including stationary leaps (37.3%), acrobatic leaps (31.3%), and trunk-to-trunk leaps (20%). Red-bellied tamarins exploited the highest levels of the arboreal canopy. Travel in this species was dominated by quadrupedal bounding and acrobatic leaps (67% of leaps) that began and ended on thin, flexible supports. Species differences in positional behavior correlated with species differences in limb proportions and locomotor anatomy, and provide a framework for understanding niche partitioning in mixed-species troops of Saguinus and Callimico.
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Locomotion in captive Leontopithecus and Callimico: a multimedia study.
Video studies, gait analysis, footprint tracks, and observational scan sampling show that, in comparably furnished enclosures, Leontopithecus rosalia and Callimico goeldii are superficially similar in their use of predefined locomotor patterns but differ profoundly in many underlying details which reflect differences in postcranial morphology. Each uses pronograde arboreal quadrupedal walking, quadrupedal bounding, and vertical climbing with comparable frequency, and both shift to bounding while moving quadrupedally at high speeds. In walking, both species use a diagonal sequence gait. However, in Callimico the distance per bout traveled while walking or running is shorter than in L. rosalia and there is an emphasis on leaping (from a stationary position) and bounding-leaps (saltational extensions of pronograde quadrupedalism), in contrast with the basically quadrupedal style of L. rosalia. This dichotomy is consistent with anatomical specializations, such as forelimb elongation in Leontopithecus and hindlimb elongation in Callimico. In vivo hand- and footprint studies demonstrate grasping halluces in both species while walking. Limb stances in L. rosalia during "transaxial bounding" involve an overstriding hindlimb, a predominance of oblique rather than in-line travel, and unique hand and foot positions. Anatomically, this locomotor style may be associated with reduced dexterity of the elongate hands and a relatively short hallux. The captive locomotor profiles for both species probably reflect biased samples of the locomotor repertoire of their wild counterparts. Nevertheless, these data reflect species-specific integrations of locomotor behavior and morphology, and corroborate expectations of locomotor diversity among callitrichine primates, even those of similar body size. It is suggested, however, that conventional quantitative studies of locomotor profiles may prove inadequate for resolving subtle aspects of locomotor morphology and behavior.
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Satellite DNA sequences in the neotropical marmoset Callimico goeldii (Primates, Platyrrhini).
Two families of tandemly repeated satellite DNAs were isolated from the neotropical primate Callimico goeldii (Goeldi's marmoset). One satellite, CgoA, is over 70% A + T and has a monomer length of 338 bp. The other satellite, CgoB, is 50% A + T and has a monomer length of 916 bp. Both CgoA and CgoB hybridize strongly with Callimico DNA, but not with the DNA of other new and old world primates. Based upon a neutral substitution rate of 1.5 X 10(-9)/site per year for primates, sequence data from 15 CgoA monomers indicate that the tandem array is at least 30 million years old. Since no other neotropical primate has amplified CgoA sequences, the data suggest that the ancestor of Callimico separated from the other neotropical primates at least 30 million years ago. This value is about fourfold larger than the value of 7-9 million years derived from immunological data by Sarich and Cronin (1980). Possible reasons for this discrepancy are discussed.
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Molecular cytotaxonomy of New World monkeys (Platyrrhini) - comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae.
Chromosome rearrangements are considered as "rare genomic changes" and can provide useful markers and even landmarks for reconstructing phylogenies complementary to DNA sequence data and bio-morphological comparisons. Here, we applied multi-directional chromosome painting to reconstruct the chromosome phylogeny and evolutionary relationships among the New World monkey (Platyrrhini) species Callithrix argentata, Cebuella pygmaea, Saguinus oedipus, Callithrix jacchus and Callimico goeldii. The results clarified several aspects of New Wold monkey phylogeny. In particular the phylogenetic position of C. goeldii was elucidated, which has been controversially discussed and variously classified in the family Callitrichidae, in the family Cebidae or in its own family Callimiconidae. Comparative genome maps were established by multi-color fluorescence in situ hybridization (FISH) with human, S. oedipus and Lagothrix lagothricha chromosome- specific DNA probes. From these data we reconstructed the putative ancestral karyotype of all Callitrichidae. Various derived chromosomal syntenies are shared by all five species and cytogenetically define Callitrichidae - including Callimico goeldii -- as a distinctive group within the Platyrrhini. C. pygmaea and C. argentata share identical chromosomal syntenies from which S. oedipus and C. jacchus differ by single independent translocations. A common derived chromosomal change links Callimico with the marmosets to the exclusion of the tamarins, however, it has further diverged from an ancestral marmoset karyotype by at least four apomorphic rearrangements. Saimiri sciureus, representing the Cebinae, exclusively shares a derived syntenic association with all Callithrichidae, defining the genus Saimiri as a sister group.
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A field study of the socio-ecology of the Goeldi's monkey (Callimico goeldii) in northern Bolivia.
A 5-month field study on both the distribution and ecology of Callimico goeldii was carried out in the seasonally dry rain forest of north-western Bolivia. The species was found to be very sparsely distributed (approximately one group per 4 km2) in isolated groups of about 6 animals throughout the study area. Callimico was found to associate a great deal with two species of Saguinus that inhabit the same region in greater densities. It appears to be a habitat specialist, preferring low-lying and damp, but well-drained, bamboo forest and spending nearly all its time within 3 m of ground level, travelling mainly by vertical clinging and leaping. We believe that this ecological specialisation accounts for the species' discontinuous micro-distribution, and that this in turn is related to Callimico's distinctive pattern of social organisation.
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Infant carrying in family groups of goeldi's monkeys (Callimico goeldii).
Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.
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Radiographic evaluation of neonatal skeletal development in Callimico goeldii reveals closer similarity to Callithrix jacchus than to Saguinus oedipus.
The phylogenetic affinities of the neotropical Goeldi's monkey (Callimico goeldii) have long been a matter of debate. Whereas most morphological evidence appears to place Callimico in a sister group position relative to the Callitrichidae, genetic studies place C. goeldii within the Callitrichidae and suggest that it is more closely related to marmosets than to tamarins. The present study presents the first radiographic analysis comparing the secondary limb bone ossification of newborn C. goeldii with representatives of the marmosets (Callithrix jacchus) and tamarins (Saguinus oedipus). The state of secondary ossification of the epiphysis and short bones is classified into three different ontogenetic stages. Our results reveal that in terms of the number of ossification centers, C. goeldii is significantly closer to C. jacchus than to S. oedipus. This is the first morphological study to support the findings of molecular studies, and the results suggest that C. goeldii is more closely related to marmosets than to tamarins.
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Mothers, not fathers, determine the delayed onset of male carrying in Goeldi's monkey (Callimico goeldii).
In biparental species, females are thought to accept and even to seek male assistance in rearing of the young. In this study, we present data that suggests that Goeldi's monkey females (Callimico goeldii) actually reject male parental care for a certain period. In Callimico, which have biparental care, mothers carry the infant exclusively for the first three weeks despite the fact that fathers are interested in their infants directly after birth. Fathers initiated significantly more body contact with their mates when newborn infants were present and retrieved one-day-old infants that were experimentally presented to them. The onset of paternal carrying in our colony was 27.5 days compared to 11.5 days (medians) observed in the field. However, presentation of a live potential predator induced earlier onset of paternal carrying by about 10 days. Additional costs to maternal carrying such as foraging and predator avoidance are likely factors influencing the decision of the mother as to when to share the cost of infant carrying with the father. We conclude that Goeldi's monkey fathers start carrying their infants so late because they do not get them earlier from the mother. We suggest that one ultimate explanation for that delay might be increased infant mortality when infant transfer starts at an earlier stage.
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[Morphometry and histology of the eye of Callimico goeldii (Thomas 1904, callimiconidae primates) (author's transl)].
The histologic anatomy of the eye of Callimico goeldii is described and histometric data are communicated. The retina is treated with special attention. The eye of Callimico features all characteristics of a visual organ adapted to diurnal activity as is known from many higher primates and man. The well-differentiated Fovea centralis and the numerical relations of the three retinal neurons, which are clearly reduced from the periphery towards the center of the retina, indicate a particularly high degree of centralization ("Zentralisationsstufe" sensu Rohen). Similar numerical relations are found in the taxonomically related families Cebidae and Callithrichidae. A high degree of centralization is understood to facilitate a good visual resolution. The eyelid apparatus is differentiated like in other higher primates. The eye muscles contain extraordinarily many nervous-muscular entities that are interpreted to serve as nervous regulatory functions. The histologic results relate well with certain behavioral phenomena of this species.
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Hormonal monitoring of age at sexual maturation in female Goeldi's monkeys (Callimico goeldii) in their family groups.
The aim of this study was to determine whether or not sexual maturation is attained in the family group in captive-born Goeldi's monkey (Callimico goeldii) and if so, at what age and body weight. To monitor ovarian activity in 14 female Goeldi's monkeys, urinary content of pregnanediol-3alpha-glucuronide (PdG) was determined using radioimmunoassay. Urinary samples were collected between the ages of 6 and 70 weeks. Subjects became sexually mature while still housed in their family groups, at a median age of 57 weeks (48-< 70 weeks). Median body weight at the age of sexual maturity was 473 g (N=10; 420-543 g). This corresponded to 90% of the median non-pregnant body weight of breeding females in our colony (526 g, N=8). Therefore, Goeldi's monkey is similar to Leontopithecus but different from Cebuella, Callithrix, and Saguinus, in terms of daughters ovulating in the family group and at a relatively young age.
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Resting energy metabolism of Goeldi's monkey (Callimico goeldii) is similar to that of other callitrichids.
The resting metabolic rates (RMRs) of six adult Goeldi's monkeys (Callimico goeldii) were measured using standard methods of open circuit respirometry during both the active (daytime) and inactive (nighttime) circadian phases for this species. One subject was measured both while she was pregnant and after she delivered a full-term, stillborn infant. Inactive-phase RMR within thermal neutrality (above 27.5 degrees C) averaged 288.5 +/- 30.8 ml O2/hr; active-phase RMR within thermal neutrality averaged 416.3 +/- 60.9 ml O2/hr. These values are 74.6% and 107.6%, respectively, of the mammalian expected for animals of this body mass. During the inactive phase, metabolic rate increased an estimated 4.3% for every degree decline in temperature below 27.5 degrees C. The RMR in Goeldi's monkey is similar quantitatively and qualitatively to those of other captive callitrichids that have been studied, with active-phase RMR being at or slightly above the mammalian expected, and inactive-phase RMR being significantly reduced. We propose that this circadian pattern of RMR is a consequence of small body size, and is not a specific metabolic adaptation within the Callitrichidae. Thus we predict that metabolic studies measuring both circadian phases in other small primates will also find this pattern of reduced RMR during the inactive phase. The inactive-phase RMR within thermal neutrality of the pregnant female was not different from that measured after the stillbirth, despite an almost 15% difference in body mass. During pregnancy, however, the female was more metabolically responsive to temperature below thermal neutrality, and had a lower upper critical temperature (i.e., was less tolerant of heat).
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Distribution and density of Callimico goeldii in the Department of Pando, Bolivia.
A survey of the distribution and density of Callimico goeldii was conducted at five sites across northwestern Bolivia, in the Department of Pando. C. goeldii was found at two sites north of the Manuripi River, with high densities at one site located along the Acre River. Estimates of habitat availability at these sites suggest that C. goeldii reaches high densities in areas with low human density and well established and extensive bamboo forests. These results, when reviewed with those of prior studies, indicate that the patchy distribution of C. goeldii in Pando is a result of both riverine barriers and the availability of bamboo habitat.
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Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus.
Callimico goeldii, Saguinus fuscicollis, and S. labiatus are sympatric in northern Bolivia and differ from each other in patterns of spatial and structural use of their environment. C. goeldii has a home range five times larger than that of mixed-species troops of S. fuscicollis and S. labiatus. The larger overlapping home range of C. goeldii allows it to move among Saguinus troops, giving it access to a wide range of different microhabitats. All three species use the most common microhabitat in the area, primary forest with dense understory, more than any other microhabitat type. C. goeldii habitat use varies by season, with bamboo and Heliconia microhabitats used more during the dry season. Each species shows preferences for different height classes: C. goeldii is found almost exclusively in the understory, S. fuscicollis uses the understory and middle canopy, and S. labiatus is found mostly in the middle canopy. These height class preferences are reflected in each species' locomotor styles, with C. goeldii showing the highest rates of vertical clinging and leaping, and S. labiatus showing the highest rates of branch-to-branch leaping and quadrupedal movement. The results suggest that C. goeldii may be restricted to forests with dense understory and a mosaic of other microhabitats. Furthermore, C. goeldii does not appear to use its tegulae for large branch foraging, but rather for vertical clinging and leaping between small vertical supports.
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An investigation into sexual motivation and behavior in female Goeldi's monkey (Callimico goeldii): effect of ovarian state, mate familiarity and mate choice.
Four adult female Callimico were studied in terms of their sexual motivation relative to three unrelated adult males using an operant paradigm followed by a pair test or a two-male choice test. Reductions in urinary cortisol concentrations and the duration of immobility were used as indicators of subjects' adjustment to the experimental situation. When females were tested with unfamiliar males there was no effect of ovarian state on operant or species-typical measures of female sexual motivation. When females were retested with the same males after a 1-week familiarization, sexual motivation was higher during the peri-ovulatory phase than during the post-ovulatory phase in terms of operant but not in terms of species-typical proceptive behavior or in terms of receptive behavior. During the familiarization periods, female sociopositive behavior and sexual motivation demonstrated marked variation depending on the identity of the male. Males with which females demonstrated high sexual motivation during familiarization were the object of equal amounts of female operant behavior during pair tests and two-male choice tests; males with which females had demonstrated low sexual motivation were the objects of less female sexual motivation under conditions of female choice than in pair tests.
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