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PubMed1998

Positional behavior and vertebral morphology in atelines and cebines.

Atelines are of particular interest to primate evolutionary studies because they converge with hominoids in postcranial anatomy, including the vertebral column. Currently, our understanding of ateline vertebral morphology is limited to mainly qualitative descriptions and functional interpretations based on general categories of positional behavior. Even less is known about the vertebrae of other platyrrhines. This study more closely examines vertebral form and function in atelines and cebines by combining direct field observations of axial postures and movements, assessments of spinal loading regimes, and a detailed vertebral morphometric analysis. Field observations (Corcovado, Costa Rica) on Ateles geoffroyi, Alouatta palliata, Cebus capucinus, and Saimiri oerstedii were quantified in conjunction with a morphometric analysis of ateline and cebine lumbar vertebrae. Hylobates was also included for comparison. Compared to Cebus and Saimiri, atelines engage more frequently in postures and locomotor behaviors that induce pronounced bending loads on the spine. All atelines share lumbar adaptations for resisting bending, including ventrodorsally elongated vertebral bodies and perpendicularly oriented transverse processes. Among atelines, lumbar region lengths and vertebral bodies are shortest in Ateles and Brachyteles, longest in Alouatta (resembling Cebus), and intermediate in Lagothrix. Compared to Cebus and all atelines, Saimiri has a relatively longer lumbar region, longer and less ventrodorsally expanded vertebral bodies, and more ventrally oriented transverse processes. These features accentuate bending loads, but increase the sagittal flexibility required for leaping. Vertebral convergence between hylobatids and atelines is more readily interpretable as a product of shared spinal loading patterns than shared positional behaviors.

Animals↗
PubMed1998

Functional and adaptive significance of primate pads and claws: evidence from New World anthropoids.

This study tests predicted morphoclines in fingertip morphology among four small-bodied (<1 kg) New World monkeys (Saimiri sciureus, Leontopithecus rosalia, Callithrix jacchus, and Saguinus oedipus) in order to test previous functional and adaptive explanations for the evolution of flattened nails, expanded apical pads, and grasping extremities within the Order Primates. Small-bodied platyrrhines which frequently forage among small-diameter substrates are expected to possess 1) relatively expanded apical pads, 2) well-developed epidermal ridges, 3) distally broad terminal phalanges, and 4) reduced flexor and extensor tubercles compared to those species which use large-diameter arboreal supports more frequently for their locomotor and postural behaviors. Results show that as the frequency of small-branch foraging increases among taxa within this sample, relative distal phalanx breadth also increases but distal phalanx length, height, and flexor tubercle size decrease. Moreover, epidermal ridge development becomes more pronounced as the frequency of small-branch foraging increases. Terminal phalanx breadth and epidermal ridge complexity are both positively correlated with apical pad size. The large, flexible apical pad increases stability of the hand and foot on small-diameter arboreal supports because the pad can contact the substrate in several planes which, in turn, enables the pad to resist disruptive forces from different directions by friction and interlocking (Hildebrand, 1995). The observed morphoclines demonstrate that a gradient in form from claw- to nail-like tegulae exists among these taxa. Thus, the distinction between claw- and nail-bearing platyrrhines is essentially arbitrary. These observations corroborate Cartmill's (1972) functional and adaptive model for the loss of claws in primates: namely, expanded apical pads are required for habitual locomotor and postural behaviors on small-diameter supports whereas claws are more useful for positional behaviors on large-diameter substrates. Finally, results from this study support previous suggestions that the keeled tegulae of callitrichines represent a derived postural adaptation rather than a primitive retention from an ancestral eutherian condition.

Adaptation, Physiological↗
PubMed1998

Platyrrhine systematics: a simultaneous analysis of molecular and morphological data.

Platyrrhine phylogeny has been investigated repeatedly with morphological characters and DNA nuclear gene sequences, with partially inconsistent results. Given the finding in the past decade that the mitochondrial genome is a potentially valuable source of phylogenetic information, we gathered DNA sequence data of a fragment of the 16S and the entire 12S mitochondrial genes. The objectives were to generate a cladistic phylogeny based on these data and to combine them in a simultaneous analysis with morphological characters and preexisting nuclear DNA sequences. Mitochondrial data analyzed on its own yielded a cladogram that was different from those generated with other data sets. The simultaneous analysis of mitochondrial, nuclear, and morphological data yielded a tree most congruent with that generated with nuclear data and to a lesser degree with the morphological one. It depicted a basal dichotomy that led to two major clades: one of them comprised [Atelinae (Callicebus + Pitheciini)] and the other major clade comprised [Aotus ((Cebus, Saimiri) (Callitrichinae))]. The weakest point of the phylogeny was the position of Aotus as basal within their clade as opposed to more closely linked with either the callitrichines or Cebus-Saimiri. Relationships within callitrichines and atelines were unstable as well. The simultaneous phylogenetic analysis of all data sets revealed congruent signal in all of them that was partially obscured in the separate analyses.

Amino Acid Sequence↗
PubMed1998

Degrees of sexual dimorphism in Cebus and other New World monkeys.

Sexual dimorphism in primate species expresses the effects of phylogeny, life history, behavior, and ontogeny. The causes and implications of sexual dimorphism have been studied in several different primates using a variety of morphological databases such as body weight, canine length, and coat color and ornamentation. In addition to these different patterns of dimorphism, the degree to which a species is dimorphic results from a variety of possible causes. In this study we test the general hypothesis that a species highly dimorphic for one size-based index of dimorphism will be equally dimorphic (relative to other species) for other size-based indices. Specifically, the degree and pattern of sexual dimorphism in Cebus and several other New World monkey species is measured using craniometric data as a substitute for the troublesome range of variation in body weight estimates. In general, the rank ordering of species for dimorphism ratios differs considerably across neural vs. non-neural functional domains of the cranium. The relative degree of sexual dimorphism in different functional regions of the cranium is affected by the independent action of natural selection on those regions. Regions of the cranium upon which natural selection is presumed to have acted within a species show greater degrees of dimorphism than do the same regions in closely related taxa. Within Cebus, C. apella is consistently more dimorphic than other Cebus species for facial measurements, but not for neural or body weight measurements. The pattern in C. apella indicates no single best measurement of the degree of dimorphism in a species; rather, the relative degree of dimorphism applies only to the region being measured and may be enhanced by other selective pressures on morphology.

Animals↗
PubMed1999

Homoplasy and adaptation in the atelid postcranium.

Homoplasy is a ubiquitous phenomenon in phylogenetic investigations, but it is rarely investigated on its own. As a case study in the pattern and basis of homoplasy in primates, the atelid postcranium is discussed here. Characters available from Ford's ([1986] in Erwin J, Swindler DR, eds: Comparative Primate Biology I: Systematics, Evolution, and Anatomy (New York: Alan R. Liss), p 73-135; [1994] in Fleagle JG, Kay RF, eds: Anthropoid Origins (New York: Plenum Press), p 595-674) analyses of New World monkeys are mapped onto alternative phylogenetic trees for the family Atelidae to contrast patterns of character evolution and to develop explanatory hypotheses for differences in the trees. In an unrooted phylogenetic network, pitheciines do not group together because those pitheciines that routinely adopt hind limb suspensory postures (Chiropotes, Cacajao) share traits with atelines. Ford's (1986) work on phylogeny has shown that these traits are homoplastic and also identified potential synapomorphies of a clade comprised of modern pitheciins and atelines. However, following that work, congruence between studies of craniodental and molecular data suggested a still broader definition of atelids (including Callicebus and Cebupithecia), and in this case only one trait may define atelids, and several traits arise in parallel. The homoplastic characters in this phylogeny suggest that the phylogenetic signal in this set of postcranial data is overwhelmed by parallel adaptations to the use of climbing behaviors in all of Ford's atelids and suspensory postures in a more restricted set of taxa. These parallelisms probably indicate a bias of selective pressures in the South American environment, especially given the frequent, independent evolution of suspensory mammals there. This highlights the fact that homoplasy can be a dominant source of similarity in data partitions strongly influenced by a particular behavioral regime, in this case positional behavior.

Adaptation, Physiological↗
PubMed1999

The origin of platyrrhines: An evaluation of the Antarctic scenario and the floating island model.

This paper evaluates whether 1) protoplatyrrhines could have migrated to South America via Antarctica, and 2) the floating island model is a plausible transoceanic mode of dispersal for land vertebrates like protoplatyrrhines. Results show that Eocene Antarctica and Australia supported large and dense forests, and that the Antarctic fauna was comprised of many species of vertebrates, including placental and marsupial land mammals. However, no primate remains have ever been reported from these continents. Antarctica and South America were connected until the Middle Eocene (i.e., after the oldest Asian anthropoids), but two major water barriers existed between Antarctica and Asia since the Early Eocene. The Eocene and Oligocene water gap separating Africa and Antarctica was excessively large. Thus, all scenarios involving an Antarctic route have been rejected. The African scenario is difficult to falsify because only one water barrier existed, both paleowinds and paleocurrents were favorable, and Paleogene African anthropoids show phylogenetic affinities to platyrrhines. I tested whether a journey on a hypothetical floating island over the Paleogene Atlantic Ocean exceeds the survival limit of a genetically viable group of animals such as protoplatyrrhines. Studies of water deprivation suggest that they could have been able, with a body weight averaging 1 kg, to survive without water for at least 13 days. I have used the present Atlantic Ocean as a model for the velocity of Paleogene paleowinds and paleocurrents. Considering winds as the key accelerating force of floating islands, the Paleogene Atlantic water barrier could have been crossed, in the most conservative scenario, in 8 days at 50 Mya, 11 days at 40 Mya, and 15 days at 30 Mya. In order to survive a transoceanic journey, however, protoplatyrrhines had to be preadapted to strong seasonal variations in water availability in their original (African) environment. Once on the sea, their brains would have physiologically interpreted the rarity of water as the beginning of the dry season, and the group would have switched its diet to alternative foods, i.e., everything available on the floating island.

Animals↗
PubMed2000

New fossil materials of the earliest new world monkey, Branisella boliviana, and the problem of platyrrhine origins.

Branisella boliviana, from the Late Oligocene of Salla, Bolivia, is the oldest fossil platyrrhine monkey discovered. To date, several fossil specimens of Branisella have been obtained, but most of them are fragmentary dentitions, so the animals craniodental morphology is still obscure. During the 1996 field season a pair of upper and lower jaw fragments and another nearly complete mandible were recovered. These new fossil materials reveal the following morphological features in Branisella: 1) P(2) is much smaller than P(3,4), whereas P(2) is relatively small but probably sexually dimorphic; 2) the zygomatic arch protrudes smoothly posterolaterally from the maxillary bone, as in extant Callicebus; 3) the mandibular arcade is nearly V-shaped and the symphysial angle, which is formed by the horizontal plane and the anterior face of mandibular symphysis, is about 40 degrees, i.e., it neither leans as far anteriorly as in callitrichines nor does it stand as vertically as Cebus; 4) upper and lower molars wore down rapidly in life, suggesting a herbivorous diet and the possibility of terrestriality; and 5) dental eruptive sequence is the same as in extant Aotus. As a whole, the dentition of Branisella is very similar to that of Proteopithecus from the Late Eocene of Fayum, Egypt, except in the lower canine morphology, suggesting a close phyletic relationship between them. The origin and early diversification of platyrrhine monkeys might have occurred on the African continent before crossing the Atlantic Ocean.

Animals↗
PubMed1997

Radiation and speciation of spider monkeys, genus Ateles, from the cytogenetic viewpoint.

The chromosomes of 22 animals of four subspecies of the genes Ateles (A. paniscus paniscus, A. p. chamek, A. belzebuth hybridus, and A. b. marginatus) were compared using G/C banding and NOR (nucleolar organizer region) staining methods. The cytogenetic data of Ateles in the literature were also used to clarify the phylogenetic relationships of the species and subspecies and to infer the routes of radiation and speciation of these taxa. Chromosomes 6 and 7 that showed more informative geographic variation and the apomorphic form 4/12, exclusively in A. p. paniscus, are the keys for understanding the evolution, radiation, and specification of the Ateles taxa. The ancestral populations of the genus originated in the southwestern Amazon Basin (the occurrence area of A. paniscus chamek) and spread in the Amazon Basin and westward, crossing the Andes and colonizing Central America and northwesternmost regions of South America. The evolutionary history of the northern South American taxa is interpreted using the model of biogeographical evolution postulated by Haffer [Science 185:131-137, 1969]. Ateles paniscus paniscus is the genetically most differentiated form and probably derives from A. belzebuth hybridus. Based on the karyotype differences, the populations of Ateles can be divided into four different groups. These findings indicate the necessity of a more coherent taxonomic arrangement for the taxa of Ateles.

Animals↗
PubMed1997

Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides.

The analysis of fecal ovarian steroids provides a powerful noninvasive method to obtain insights into ovulatory cycles, gestation length, and the timing of sexual interactions relative to the periovulatory period in wild primates. Techniques developed to collect and assay feces from free-ranging muriqui monkeys (Brachyteles arachnoides) for estradiol and progesterone yield the first explicit reproductive data on this species, and provide the first opportunity to evaluate the timing of observed copulations with muriqui ovarian cycles. Hormonal profiles from seven females indicate average cycle lengths of 21.0 +/- 5.4 days (n = 20). Females conceived after 3-6 ovulatory cycles. Gestation length averaged 216.4 +/- 1.5 days for the five females for which conception cycles were sampled. Discrete copulation periods spanned an average of 2.1 +/- 1.2 days (n = 29), with intervals between these concentrated periods of copulations averaging 15.6 +/- 6.7 days (n = 20). There were no significant differences among females in cycle lengths, copulation period lengths, or copulation interval lengths. Ejaculation was visible following 71.8 +/- 26.7% of copulations during the females preovulatory periods. All females copulated outside the periovulatory period. The proportion of copulation days outside the periovulatory period was slightly greater (p = 0.08) for primiparous females (64.8 +/- 28.3%) than for multiparous females (28.7 +/- 19.7%).

Animals↗
PubMed1997

Steroid excretion during the ovarian cycle in captive and wild muriquis, Brachyteles arachnoides.

Urine, feces, and copulation frequency were collected from two captive muriqui females, Brachyteles arachnoides, at the Centro de Primatologia do Rio de Janeiro following the resumption of postpartum ovarian cycles. Fecal steroid profiles from seven wild muriqui females at the Estação Biologica de Caratinga, Minas Gerais, Brazil, were compared to the captive females to determine the approximate patterns of steroid excretion relative to the urinary LH peak. Hormonal profiles from one of the captive female muriquis revealed a discrete urinary LH peak. For this female, fecal progesterone increased on the same day as the urinary LH peak, while fecal estradiol increased 6 days later and urinary steroids increased 5 days later. For both captive females, the onset of fecal progesterone increase was preceded by the onset of copulations, which occurred during at least a 5-day period. The complete fecal hormonal profiles of the one captive female for which continuos data were available were similar to those found in wild muriqui monkeys, with the onset of an increase in sustained progesterone levels occurring several days prior to the onset of sustained estradiol increase. These patterns suggest that fecal progesterone may be excreted rapidly in this species. The onset of sustained increase in fecal progesterone levels, together with the consistent delay in the onset of the sustained increase in estradiol, may provide the best indicators of the periovulatory period for muriqui females.

Animals↗
PubMed1997

Effects of duration of separation on responses to mates and strangers in the monogamous titi monkey (Callicebus moloch).

Adult male and female titi monkeys form an intense social bond characterized by high levels of affiliative interactions between pairmates and agonistic responses to strangers. In natural settings, separation between mates can vary from brief periods, as when mates drift apart during feeding, to permanent separation, occasioned by desertion or death. In this study we asked how different durations of separation altered the behavior of male and female titi monkeys (Callicebus moloch). We compared the effects of brief separation such as might occur incidentally during feeding (1-2 h) with prolonged separation such as might occur if one partner died or deserted (5 days). Effects were observed during a 30 min reunion of pairmates or during a 30 min encounter with a stranger of the opposite sex. Following brief separation, interactions between mates and between strangers clearly differed in measures of affiliation, but not in behaviors indicative of arousal. Following prolonged separation, measures of arousal increased with both mated pairs and strangers. Females tended to interact more readily with a stranger following prolonged separation than after brief separation, but interactions between mates were essentially unchanged and differed substantially from those between strangers. The data suggest that the pair bond persists in titi monkeys after prolonged social isolation, despite increased interest in interacting with potential new partners.

Animals↗
PubMed1998

Immobilization and health assessment of free-ranging black spider monkeys (Ateles paniscus chamek).

Eight free-ranging black spider monkeys (Ateles paniscus chamek) were immobilized with Telazol in Bolivia for the purpose of radio-collaring. During this procedure, the animals received complete medical examinations, and samples were collected for health analyses. Biochemical test results varied with the degree of condition of the animals, and a variety of physical abnormalities were found. Evidence of previous infections with Leptospira sp., encephalitis virus, and yellow fever virus was found. All findings contribute to establishing baseline health values for the species. The handling of primates for research projects provides a valuable opportunity to collect health-related data and samples that can contribute to wildlife management and conservation efforts. The capture and handling of free-ranging primates is always accompanied by risk of injury or mortality. It is ethically important to maximize the amount of information gathered during these procedures. Furthermore, sharing the undesirable impacts with the scientific community enables informed decisions to be made during future project development.

Anesthetics↗
PubMed1998

The menstrual cycle of the spider monkey (Ateles geoffroyi).

The ovarian cycles of four adult female spider monkeys (Ateles geoffroyi) were followed daily throughout 30 days by means of vaginal swabs and blood samplings. Cytological analyses of the vaginal swabs and radioimmunoassay determination of the daily levels of estradiol-17 beta (E2) and progesterone (P4) wer done in order to classify the kind of ovarian cycle of this species. Our results show that Ateles geoffroyi females display menstrual cycles of about 24 days on average. By comparison with the well-known menstrual cycles of women, apes, and Old World monkeys, the four distinctive cytological phases (bleeding, follicular, periovulatory, and luteal) could be recognized; mid-cycle E2 peaks followed by mid-luteal increases of the same hormone were present in all four females. P4 levels were higher after the E2 peak, although both hormones were present throughout the cycles. Also, age-dependent features, hormone profiles, and changes in menstrual phases lengths were detected.

Analysis of Variance↗
PubMed1998

Seed dispersal by neotropical seed predators.

From a plant's perspective, the difference between a seed predator and a seed disperser should be straightforward: attract animals that will disperse seeds and defend seeds from potential predators. Unlike pulp-eating frugivores, seed predators regularly encounter diverse plant protective mechanisms. The purpose of this paper is to examine feeding constraints, morphological adaptations, and the mechanical process of seed predation. While there is evidence that some seed predators cause severe losses to seed crops, there is also evidence that seed predators enhance seed dispersal and germination. We also examine four methods by which neotropical seed predators may contribute to dispersal. 1) Seed predators examined here ingested fruit when seeds were full-sized, but not yet mature (i.e., seeds of mature fruit may be avoided by seed predators and available for dispersal by other frugivores). 2) Sympatric seed predators may ingest seeds from different plants thus reducing overall predator load on any individual plant. 3) Seed predators that manipulate seeds (e.g., remove pericarp and seed coat) may enhance germination if the prepared seeds are dropped, discarded, or buried and not ingested. 4) Small seeds may miss mastication and swallowed intact with a food bolus. The last mechanism is the most likely to contribute to seed dispersal by the widest array of vertebrate seed predators, but primate seed predators may facilitate seed dispersal using all four mechanisms. Therefore, the traditional dichotomy of seed predator vs. seed disperser oversimplifies the interactions between seed predators and plants.

Animals↗
PubMed1998

A new pitheciin primate from the middle Miocene of Argentina.

We report here a new fossil primate from the middle Miocene of Argentina. The material consists of isolated teeth, mandibular fragments, and a talus. The fossils were collected in the Collón Cura formation at Cañadón del Tordillo in Neuquén Province. An age of 15.71 +/- 0.07 Ma has been reported for the Pilcaniyeu Ignimbrite, which lies just below the paleosols in which the fossils were found. This material is thus the youngest occurrence of fossil primates in Argentina (hitherto documented in the Santacrucian and older land mammal ages) but still is older than the middle Miocene platyrrhine primates from La Venta, Colombia, in particular the pitheciins Nuciruptor and Cebupithecia. The material is recognized as a new genus and species of Pitheciinae, Propithecia neuquenensis. The mesiodistally compressed, high-crowned incisors are specialized and similar to species in the tribe Pithecini and to the nonpitheciin Soriacebus (early Miocene, Patagonia). We rule out a phylogenetic relationship to the latter because of differences in molar morphology. Propithecia does, however, fit well into the pattern of pitheciin evolution, being more derived than the middle Miocene pitheciin Nuciruptor but not as much as another middle Miocene taxon, Cebupithecia. As such, this makes Propithecia the oldest taxon that can be confidently placed within this modern New World monkey subfamily. By analogy with the molar structures and diets of extant platyrrhines, Propithecia has a molar structure consistent with a variety of low-fiber diets ranging from fruit and gum to seeds. Its incisors suggest seed-eating in much the same way as extant pitheciins, like Pithecia. The talus resembles that of Callicebus, suggesting arboreal quadrupedal locomotion.

Animals↗
PubMed1998

Primate diversity, habitat preferences, and population density estimates in Noel Kempff Mercado National Park, Santa Cruz Department, Bolivia.

This report documents primate communities at two sites within Noel Kempff Mercado National Park in northeastern Santa Cruz Department, Bolivia. Diurnal line transects and incidental observations were employed to survey two field sites, Lago Caiman and Las Gamas, providing information on primate diversity, habitat preferences, relative abundance, and population density. Primate diversity at both sites was not particularly high, with six observed species: Callithrix argentata melanura, Aotus azarae, Cebus apella, Alouatta caraya, A. seniculus, and Ateles paniscus chamek. Cebus showed no significant habitat preferences at Lago Caiman and was also more generalist in use of forest strata, whereas Ateles clearly preferred the upper levels of structurally tall forest. Callithrix argentata melanura was rarely encountered during surveys at Lago Caiman, where it preferred low vine forest. Both species of Alouatta showed restricted habitat use and were sympatric in Igapo forest in the Lago Caiman area. The most abundant primate at both field sites was Ateles, with density estimates reaching 32.1 individuals/km2 in the lowland forest at Lago Caiman, compared to 14.1 individuals/km2 for Cebus. Both Ateles and Cebus were absent from smaller patches of gallery forest at Las Gamas. These densities are compared with estimates from other Neotropical sites. The diversity of habitats and their different floristic composition may account for the numerical dominance of Ateles within the primate communities at both sites.

Alouatta↗
PubMed1999

Sequences from the 5' flanking region of the epsilon-globin gene support the relationship of Callicebus with the pitheciins.

The purpose of this study was to determine nucleotide sequences from the 5' flanking region of the epsilon-globin gene of selected platyrrhine primates and to analyze the data for phylogenetic information and estimated times of divergence. We report new sequence data for two species of New World monkeys, Callicebus torquatus and Pithecia irrorata. We analyzed these data in conjunction with homologous sequences from other primate species. The data support the hypothesis that the titi monkeys (Callicebus) and seed predators (Tribe Pitheciini) form a clade (Subfamily Pitheciinae), and also provide limited support for that subfamily being allied with the atelines. We also present estimated dates of divergence for the Callicebus and pitheciin lineages.

Animals↗
PubMed1999

Taste difference thresholds for sucrose in two species of nonhuman primates.

The purpose of this study was to determine taste difference thresholds for sucrose in frugivorous spider monkeys and omnivorous baboons. Using a two-bottle preference test of brief duration, we presented four Ateles geoffroyi and four Papio hamdryas anubis with six different reference concentrations (RCs) of 25, 50, 100, 200, 300, and 400 mM sucrose and tested their ability to discriminate these from lower concentrations of this carbohydrate. The just noticeable differences (JNDs), expressed as Weber ratios (delta/I), were found to range from 0.075-0.25 in the spider monkeys, with a tendency for lower values with higher RCs. In contrast, the baboons showed the reverse trend, with the lowest Weber ratio of 0.10 at the two lowest RCs and higher values of up to 0.25 with the highest RC tested. Thus, the JNDs were found to be generally similar in both species and at least as low as in humans. The results support the assumption that both spider monkeys and baboons may use sweetness as a criterion for food selection. The different patterns of differential sensitivity for sucrose across the range of concentrations tested suggest a correlation between the ability to discriminate between different concentrations of sucrose and the dietary habits of the two species.

Animals↗