Interlimb coordination,gait, and neural control of quadrupedalism in chimpanzees

Interlimb coordination is directly relevant to the understanding of the neural control of locomotion, but few studies addressing this topic for nonhuman primates are available, and no data exist for any hominoid other than humans. As a follow-up to Jungers and Anapol's ([1985] Am. J. Phys. Anthropol. 67:89–97) analysis on a lemur and talapoin monkey, we describe here the patterns of interlimb coordination in two chimpanzees as revealed by electromyography. Like the lemur and talapoin monkey, ipsilateral limb coupling in chimpanzees is characterized by variability about preferred modes within individual gaits. During symmetrical gaits, limb coupling patterns in the chimpanzee are also influenced by kinematic differences in hindlimb placement (“overstriding”). These observations reflect the neurological constraints placed on locomotion but also emphasize the overall flexibility of locomotor neural mechanisms. Interlimb coordination patterns are also species-specific, exhibiting significant differences among primate taxa and between primates and cats. Interspecific differences may be suggestive of phylogenetic divergence in the basic mechanisms for neural control of locomotion, but do not preclude morphological explanations for observed differences in interlimb coordination across species. Am J Phys Anthropol 102:177–186, 1997 © 1997 Wiley-Liss, Inc.     

Relative efficiency of preferred and nonpreferred patterns of lateralized foraging in the gentle lemur (Hapalemur griseus)

Lateralized patterns of hand use in species-typical bamboo shoot foraging were evaluated for efficiency in five female and six male gentle lemurs (Hapalemur griseus sp.). Efficiency was defined as amount of time required to complete a foraging response sequence. The foraging pattern consisted of four component movements: PULL-IN, COUNTERFORCE, TURN, and FEED-IN. These component movements had been shown in a previous study to incorporate lateral hand biases that formed subsets of patterns that were characteristic for each gentle lemur. The duration of each foraging sequence was measured from the beginning of the first component to the initiation of the terminal component. Frequency of use scores were employed to divide the pattern sequences of each subject into preferred and nonpreferred categories. A within-subjects comparison of the mean durations of preferred patterns (M = 2.56 sec) with those of non- preferred patterns (M = 3.02 sec) found that preferred patterns were executed more rapidly, t(10) = 3.36, P = .007. A multiple regression showed that order of pattern preference accounted for 89% of the variance in mean duration of response time (R² = .89, P = .056). Thus, the use of preferred lateralized hand patterns resulted in more rapid bamboo shoot harvesting. Speed in foraging may be regarded as an adaptive strategy for a species that subsists on a high bulk, low nutrient density food such as bamboo. © 1995 Wiley-Liss, Inc.     

Cortical beta EEG oscillations related to changes in muscle tone activity during sleep in spider monkey (Ateles geoffroyi)

Background

The physiological mechanisms that allow for sleeping in a vertical position, which is primordial for arboreal primates, have not been studied yet.

Methods

A non‐invasive polysomnographic study of 6 spider monkeys (Ateles geoffroyi) was conducted. The relative beta power of the motor cortex and its linear relation with muscle tone in the facial mentalis muscle and the abductor caudae medialis muscle of the tail during wakefulness and sleep stages were calculated.

Results

A strong negative linear relationship (r = ?.8, P = .03) was found between the relative power of the beta2 band in the left motor cortex and abductor caudae medialis muscle tone during delta sleep.

Conclusions

The left motor cortex, through beta2 band activity, interacts with abductor caudae medialis muscle tonicity during delta sleep. This interaction takes part in the mechanisms that regulate the sleep postures.     

Neural control of the pyloric region in the foregut of the shrimp Penaeus (Decapoda: Penaeidae)

Pyloric pattern-generating neurons that control the pyloric region of the foregut were identified in the stomatogastric ganglion of the most primitive decapod genus Penaeus. Five types of motor neurons and one interneuron are involved in generation of pyloric motor pattern. One cell type of motor neurons innervates muscles of both the gastric mill and the pylorus like the gastric motor neurons in Cancer, but unlike those in Panulirus. These identified neurons are connected to each other either by electrical or inhibitory chemical synapses to construct the neural circuit. This pyloric circuit is similar to the homologous circuit of other crustacean species though some differences are seen in synaptic connections, supporting the hypothesis that the basic design of the neural circuit has been conserved during evolution of the Malacostraca, and that differences have occurred in the synaptic connectivity as the foregut structure has become complex. The motor neurons use either acetylcholine or glutamate as a neurotransmitter like in reptantians. The foregut structure, the number of the pyloric cells, muscle innervation, neurotransmitters, and circuitry are compared among malacostracan crustaceans to provide insight into how the neural circuits change and evolve to produce the motor patterns mediating behaviour. Accepted: 18 April 1997     

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.     

Hand Preference in Free-Ranging White-Throated Capuchins (Cebus capucinus) in Costa Rica

I studied the hand preference patterns of individuals in three troops of white-throated capuchins (C. capucinus) in Palo Verde, Costa Rica, during 11 months from February 1995 to January 1996. I used focal and ad libitum sampling techniques and tested several frameworks that seek to explain and to predict primate hand use patterns via a variety of spontaneous tasks that differ in manipulative difficulty and required postural regulation: reach, tap, grab, carry, and object-use. The monkeys showed symmetrical hand use patterns for the easy tasks, reach and tap; strongly asymmetrical patterns for the highly manipulative task, object-use, at the individual level; and weak population-level biases for tasks requiring a degree of postural regulation, carry. The results for data on grab are inconclusive. These results do not support the available primate hand use frameworks and differ from most of the captive literature on hand preference in Cebus. The findings indicate that postural regulation may influence hand use patterns in nonhuman primates at the population level.     

Feeding habits of chimpanzees (Pan troglodytes), red-tail monkeys (Cercopithecus ascanius schmidti) and blue monkeys (Cercopithecus mitis stuhlmanii) on figs in Budongo Forest Reserve, Uganda

Feeding habits of chimpanzees, red‐tail and blue monkeys on figs (Ficus) were studied in compartment N3 of Budongo Forest Reserve, western Uganda, from September 1997 to March 1998. The aim was to examine the spatial and temporal foraging habits of chimpanzees, red‐tail monkeys and blue monkeys on figs in the forest reserve. Both scan and focal sampling methods were used to assess the foraging habits of the primates. It was found that the primates fed on emerging leaves of Ficus mucuso Ficalho, F. varifolia Warb. and F. exasperata Vahl. They also preferred ripe fruits to emerging, young and unripe fruits. The primates spent 78% of the morning eating fruits and leaves and inhabited fig trees with fruits for about 4 h. Fig trees with ripe fruits attracted larger numbers of primate groups. It is concluded that information on the feeding habits of chimpanzees and monkeys is required in order to have a clear understanding of the social behaviour and pattern of movement of the primates and to assist in predicting the likely impacts of poor forest management, forest degradation and loss of food resources on their populations.     

A Laterally Interconnected Neural Architecture in MST Accounts for Psychophysical Discrimination of Complex Motion Patterns

The complex patterns of visual motion formed across the retina during self-motion, often referred to as optic flow, provide a rich source of information describing our dynamic relationship within the environment. Psychophysical studies indicate the existence of specialized detectors for component motion patterns (radial, circular, planar) that are consistent with the visual motion properties of cells in the medial superior temporal area (MST) of nonhuman primates. Here we use computational modeling and psychophysics to investigate the structural and functional role of these specialized detectors in performing a graded motion pattern (GMP) discrimination task. In the psychophysical task perceptual discrimination varied significantly with the type of motion pattern presented, suggesting perceptual correlates to the preferred motion bias reported in MST. Simulated perceptual discrimination in a population of independent MST-like neural responses showed inconsistent psychophysical performance that varied as a function of the visual motion properties within the population code. Robust psychophysical performance was achieved by fully interconnecting neural populations such that they inhibited nonpreferred units. Taken together, these results suggest that robust processing of the complex motion patterns associated with self-motion and optic flow may be mediated by an inhibitory structure of neural interactions in MST.     

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.     

Taste Preference Thresholds for Food-Associated Sugars in Baboons (Papio hamadryas anubis)

We aimed to determine taste preference thresholds for 5 food-associated sugars in Papio hamadryas anubis. In a 2-bottle preference test of brief duration (2 min) 4 subadult baboons significantly preferred concentrations as low as 10 mM sucrose, 20 mM fructose, lactose, and maltose, and 25 mM glucose over tap water. Presentation of suprathreshold sugar solutions led to marked concentration-dependent polydipsia. The results show that baboons are among the most sugar-sensitive nonhuman primates tested so far and, thus, support the assumption that Papio hamadryas anubis may use sweetness as a criterion for food selection.     

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. On leave from: Genetics Section, Instituto Nacional do Cancer (Rio de Janeiro)/Department of Genetics, Universidade Federal do Rio de Janeiro, Brazil     

Phylogeographic evidence for two species of muriqui (genus Brachyteles)

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two‐species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus’ distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120–80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.     

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 1.5×10^–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. On leave from: Genetics Section, Instituto Nacional do Cancer, Rio de Janeiro/Department of Genetics, Universidade Federal do Rio de Janeiro, Brazil     

Behavioral responses of two Malaysian primates (Hylobates lar andPresbytis melalophos) to selective logging: Vocal behavior,territoriality, and nonemigration

The durations of logging operations may be regarded as critical periods in which primates will be required to make rapid adjustments in behavioral patterns. Primates are extremely difficult to observe during logging operations, but their behavioral response may be interpreted from analysis of calling patterns. In Hylobates lar,increased calling frequencies of groups may be indicative of intruder pressure, as may reduced calling frequencies of animals which are avoiding confrontation with conspecifics or avoiding detection by loggers. In Presbytis melalophosthe function of calling is to mediate intergroup avoidance, such that differential calling frequencies would not be expected. Where reduction in calling occurs it is probably directed toward concealment from loggers. Groups do not emigrate from active logging areas and movement outside of established territories occurs only to a very limited extent.     

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens. Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.     

Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys(Alouatta Palliata) in Northeastern Costa Rica

I conducted a 15- month ecological study of habitat preferences and activity and foraging patterns of two troops of mantled howling monkeys, Alouatta palliata,in a lowland rain forest at La Selva Biological Reserve in northeastern Costa Rica. The two troops specialized on different habitats in spite of the fact that both of them had all habitats available and were not constrained by neighboring troops since the population density of howlers is low (7- 15 howlers/km ² ).Troop 1 spent the majority of time in primary forest (80%) followed by secondary forest (10%), while troop 2 spent the majority of time in undisturbed riparian habitat (60%) followed by primary forest (30%). Habitat sampling indicates that neither the total number of stems, species, or families nor the diversity (Shannon index) or evenness is a good indicator for howler habitat selection. Instead the density of trees from the 12 species most commonly consumed by each troop is the most important factor. Activity and foraging patterns were not dependent upon the season as has been described for howling monkeys in forests with a more pronounced dry season at Barro Colorado Island, Panama, and La Pacifica in northwestern Costa Rica. This is likely a result of the more constant food supply at La Selva, combined with less intraspecific competition due to the low howler density. The intraspecific variability of foraging patterns and troop- specific habitat specialization observed in Alouatta palliatashould be considered in the conservation biology of primates. Primate relocation programs should include not only an ecological assessment of the release site but also a comparison of the release site with the habitat that the groups currently occupy.     

The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands

Orangutans are the only great apes found outside of Africa. At present, they occur only on the two large Sunda‐shelf islands of Sumatra and Borneo. Most researchers recognize two separate subspecies, Pongo pygmaeus abelii in Sumatra and P.p. pygmaeus in Borneo.^1,2 Relative to other primates, they have a variety of unusual features. These large‐bodied frugivores are among the most solitary of anthropoid primates.^3–5 They are also highly dimorphic, with the average body mass (78 kg) of males being more than twice that of females (36 kg).⁶ Despite its large body size the red ape has more specialized morphological adaptations for arboreality than do the African great apes. Researchers generally recognize sexually mature male orangutans with two physically distinct morphs, a phenomenon described as bimaturism. Males of the relatively smaller morph are known for forcing copulations with adult females.^5,7–9.     

Activity budget,home range and diet of the Colombian night monkey (Aotus lemurinus) in peri-urban forest fragments

Forest fragmentation and deforestation are major threats to primates at a global scale. The survival of primates in forest fragments largely depends on their behavioral and dietary flexibility, as well as their ability to use a modified matrix in anthropogenic landscapes, hence the importance of determining these ecological parameters in habitats with strong anthropic interventions. This paper aims to describe the activity budget and diet of two groups of the Colombian night monkey (Aotus lemurinus) and to estimate their home range in two peri-urban forest fragments in the city of Manizales, Colombia. We combined scan sampling and handheld GPS fixes in order to determine the behavioral, dietary and spatial patterns of the study groups. Night monkeys spent most of their time resting and traveling and were mainly frugivorous relying on at least 26 plant species in their diet. The most consumed plants included Persea americana, Cecropia angustifolia, Musa x paradisiaca, Cecropia telenitida, and Croton cf. mutisianus. Two of these plants are cultivated species and can provide important resources for populations in small forest fragments. Home range sizes were estimated at 1.7 to 1.8 hectares, using a grid count method. Our results suggest the potential adaptability that these primates have when exposed to anthropogenic habitat disturbances and habitat degradation. Nonetheless, future studies should evaluate the influence of demographic factors and resource availability on the behavioral, dietary and spatial patterns of A. lemurinus in peri-urban forests, in order to further understand their ability to cope with the pervasive processes of habitat fragmentation in the northern Andes.

     

Neurogenic and Myogenic Properties of Pan-Colonic Motor Patterns and Their Spatiotemporal Organization in Rats

Background and Aims

Better understanding of intrinsic control mechanisms of colonic motility will lead to better treatment options for colonic dysmotility. The aim was to investigate neurogenic and myogenic control mechanisms underlying pan-colonic motor patterns.

Methods

Analysis of in vitro video recordings of whole rat colon motility was used to explore motor patterns and their spatiotemporal organizations and to identify mechanisms of neurogenic and myogenic control using pharmacological tools.

Results

Study of the pan-colonic spatiotemporal organization of motor patterns revealed: fluid-induced or spontaneous rhythmic propulsive long distance contractions (LDCs, 0.4–1.5/min, involving the whole colon), rhythmic propulsive motor complexes (RPMCs) (0.8–2.5/min, dominant in distal colon), ripples (10–14/min, dominant in proximal colon), segmentation and retrograde contractions (0.1–0.8/min, prominent in distal and mid colon). Spontaneous rhythmic LDCs were the dominant pattern, blocked by tetrodotoxin, lidocaine or blockers of cholinergic, nitrergic or serotonergic pathways. Change from propulsion to segmentation and distal retrograde contractions was most prominent after blocking 5-HT₃ receptors. In the presence of all neural blockers, bethanechol consistently evoked rhythmic LDC-like propulsive contractions in the same frequency range as the LDCs, indicating the existence of myogenic mechanisms of initiation and propulsion.

Conclusions

Neurogenic and myogenic control systems orchestrate distinct and variable motor patterns at different regions of the pan-colon. Cholinergic, nitrergic and serotonergic pathways are essential for rhythmic LDCs to develop. Rhythmic motor patterns in presence of neural blockade indicate the involvement of myogenic control systems and suggest a role for the networks of interstitial cells of Cajal as pacemakers.