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Thermoregulation in the slender loris (Loris tardigradus).

Thermoregulatory characteristics of slender lorises largely resemble those of other slow-moving Lorisidae: Body temperature is slightly below the normal mammalian level and basal metabolic heat production is only about half of the mass-specific standard. During cold exposure only a rather small body core is kept at a high temperature level whereas large parts of the body are allowed to cool. Contrary to the findings in other Lorisidae slender lorises are more tolerant against high environmental temperatures, largely due to the ability of considerably increasing evaporative cooling.

Animals↗

Morphological changes in the cochlear nuclear complex in primate phylogeny and development.

The primate cochlear nuclear complex exhibits several characteristic morphological differences in the various primate families from Lorisidae through Hominidae. The most striking differences occur in the organization of the dorsal cochlear nucleus in which the laminar pattern becomes progressively obscured. Granule cells form an external granular layer as well as being intermixed within the molecular and pyramidal layers in slow lorises and squirrel and rhesus monkeys. Whereas a prominent external granular layer remains in chimpanzees, granule cells are scant in other portions of the nucleus. Human adults lack an external granular layer. A small number of granule cells occur but with inconstant distribution. Primates lack the linear array of pyramidal cells oriented perpendicularly to the epithelial surface as seen in cats. The granule cell layer exhibits similar regression in development of the human cochlear complex. The external granular layer is prominent in the fetus but rapidly decreases in size after birth. It achieves its adult form prior to 18 months. The data suggest that neuronal attrition, or programmed cell death, may be the major mechanism accounting for the alterations that occur in the human granule cell layer. Other differences in cytoarchitecture, within the great apes and humans, include decreases in the small and giant cell populations of the cochlear complex. These changes, in consort with the organizational changes and reduction of granule cells as noted above, suggest a trend towards reduced intranuclear integration at the level of the cochlear nucleus coupled with encephalization of the auditory system.

Adult↗

Three-dimensional analysis of the arterial pattern of the upper limbs in Lorisiformes (Prosimiae, Primates).

A study of the arterial patterns of the upper limbs in Lorisiformes (Prosimiae), especially those of the rete mirabile and their correlating arteries, was carried out by three-dimensional arteriographic analysis. The rete displayed at least two types of plexiform distribution: (1) a vascular bundle in Lorisidae, which consists of a division of the main artery into a principal trunk surrounded upwards by about 50 small arteries, and (2) a simple network pattern in Galagidae, which, at most, is composed of simple vascular networks of the nature of a few widely scattered anastomoses. The arterial patterns of the upper limb in Lorisiformes are basically the same, but the position of divergence and the number and size of the vessels in the rete differ. The arterial patterns of the upper limbs in Lorisiformes closely resemble the development of the vessels in the 21- to 23-mm stages of human embryonic growth. In this study, we observed some similarity in the patterns between the rete mirabile and the superficial brachial artery in man.

Angiography↗

Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecific comparisons.

The composition of skin, muscle, and bone and their distribution throughout the body are compared for "advanced" or "specialized" species (Alouatta, Macaca, Canis, Felis, Lepus); smaller, more closely related species (Tupaia and the Lorisidae); and several species within the same ecosystem (Barro Colorado Island, Panama). Among the most significant variables, the skin of sloths, howlers and macaques constitutes more than 12% of body weight, whereas greyhound skin is 5% of weight; sloth and howler muscle are 25% of weight, macaque muscle about 40% of weight, greyhound and agouti muscle over 50% of weight. In tree shrews and galagos muscle is heavier (35%) than in pottos and slow lorises (below 28%), but bone and skin are lighter. All species differ in the segmental distribution of weight. Cats have light tails, light feet and heavy thighs, whereas howlers have heavy tails, heavy feet, and light thighs. The galagos have heavy hindlimbs and tails, the pottos and lorises have reduced tails and approximately equal fore- and hindlimbs. Convergences in segment pattern (sloths with pottos and lorises, marmosets with tree shrews, owl monkeys with galagos, cebus with macaques) as well as divergences are documented. All weight-of tissue and weight-of-segment variables are correlated directly with locomotor adaptation.

Adaptation, Physiological↗

Homologies of the anterior teeth in Indriiadae and a functional basis for dental reduction in primates.

In a recent paper Schwartz ('74) proposes revised homologies of the deciduous and permanent teeth in living lemuriform primates of the family Indriidae. However, new evidence provided by the deciduous dentition of Avahi suggests that the traditional interpretations are correct, specifically: (1) the lateral teeth in the dental scraper of Indriidae are homologous with the incisors of Lemuriadae and Lorisidae, not the canines; (2) the dental formula for the lower deciduous teeth of indriids is 2.1.3; (3) the dental formula for the lower permanent teeth of indriids is 2.0.2.3; and (4) decrease in number of incisors during primate evolution was usually in the sequence I3, then I2, then I1. It appears that dental reduction during primate evolution occurred at the ends of integrated incisor and cheek tooth units to minimize disruption of their functional integrity.

Animals↗

Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade.

New crania of the Oligocene anthropoidean Aegyptopithecus provide a test of the hypothesized tarsier-anthropoidean clade. Three cranial characters shared by Tarsius and some modern anthropoideans (apical interorbital septum, postorbital septum, "perbullar" carotid pathway) were examined. 1) An apical interorbital septum is absent in Aegyptopithecus. A septum does occur in Galago senegalensis (Lorisidae) and Microcebus murinus (Cheirogaleidae), so the presence of a septum is not strong evidence favoring a tarsiiform-anthropoidean clade. 2) In Aegyptopithecus and other anthropoideans, the postorbital septum is formed mainly by a periorbital flange of the zygomatic that extends medially from the lateral orbital margin onto or near the braincase. The postorbital plate of Tarsius is formed by frontal and alisphenoid flanges that extend laterally from the braincase to the zygomatic's frontal process, which is not broader than the postorbital bars of other prosimians. Periorbital flanges evolved in Tarsius for support or protection of the enormous eyes, as suggested by the occurrence of maxillary and frontal flanges that cup portions of the eye but do not separate it from temporal muscles. 3) The internal carotid artery of Aegyptopithecus enters the bulla posteriorly and crosses the anteroventral part of the promontorium. The tympanic cavity was probably separated from the anteromedial cavity by a septum stretching from the carotid channel to the ventrolateral bullar wall. In Tarsius, the carotid pathway is prepromontorial, and a septum stretches from the carotid channel to the posteromedial bullar wall. Quantitative analyses indicate that anterior carotid position has evolved because of erect head posture. The cranium of Oligocene anthropoideans thus provides no support for the hypothesized tarsier-anthropoidean clade.

Animals↗

Muscles of facial expression in Otolemur, with a comparison to lemuroidea.

Gross and histologic aspects of facial expression muscles are presented here for Otolemur spp. (suborder Prosimii, family Lorisidae) and are compared with those of lemuroids. Muscles of facial expression are involved in social signaling among primates, and are a primary means by which close-proximity nonverbal communication is achieved. These muscles have been well described in catarrhines and many of the lemuroids; however, their arrangement is not well known in the lorisids. In the present study we examined muscles of facial expression in Otolemur by dissecting preserved faces. The arrangement and appearance of the muscles were noted, and samples were gathered from each muscle for histologic processing. The results showed 17 muscles of facial expression in Otolemur, as compared to seven reported in previous studies. Histologically, muscles of the ear region were arranged in tight, dense fascicles, while muscles of the orbital region were arranged more loosely. Grossly, the facial expression muscles in Otolemur were very similar in morphology and attachments to those in the lemuroids, with some differences in the ear region. Otolemur garnettii had several muscles that appeared to be more robust than in the larger O. crassicaudatus. This may be due to dietary and/or social differences between the species. In previous studies it was concluded that, relative to lemuroids, Otolemur has a primitive arrangement of facial expression muscles. The current results do not support that conclusion, and in fact support a far greater similarity between Otolemur and lemuroids in general. These results underscore the need for a reexamination of facial musculature in prosimians in general, and may have taxonomic value as regards the position of Otolemur with lemuroids and other galagos.

Animals↗

Topography, cytoarchitecture, and sulcal patterns in primary somatic sensory cortex (SmI) prosimian primate, Perodicticus potto.

The topographic organization of the primary somatic sensory projection area (SmI) in relation to cytoarchitectural fields and sulcal patterns was examined in the prosimian primate Perodicticus potto. The area of cortex responding to low threshold (LT) cutaneous stimulation of the glabrous and hairy surfaces of the hand was determined by microelectrode mapping techniques, with standardized threshold stimuli for defining receptive fields. A single somatotopic projection of the two hand surfaces was found; the glabrous projection area is rostral to that of the hairy hand. Within both the glabrous and hairy areas, receptive fields on the distal digits are found anterior to those on the proximal hand. The glabrous hand projection area is coextensive with a dense granular area typical of koniocortex. The hairy hand area corresponds to a cytoarchitectural field which is less granular than the glabrous field. While koniocortex occupies the crown of the gyrus caudal to the coronally oriented sulcus, a large more rostral field, which contains both granule and large pyramidal cells, occupies the whole of the caudal bank of the sulcus. Force thresholds of many receptive fields (RFs) in Perodicticus were high both on the borders and within the LT area (perhaps because of the advanced age of these animals). However, the receptive field sizes for both the glabrous and hairy hand areas were of the same magnitude as those of Nycticebus (Carlson and FitzPatrick, '82). From the combined studies of three species of Lorisidae, Perodicticus, Galago (Carlson and Welt, '80), and Nycticebus (Carlson and FitzPatrick, '81), using similar mapping and stimulation techniques, both general and specific features of SmI hand area organization can be illustrated. A single projection of the glabrous and hairy hand is common to Perodicticus and Galago, but two glabrous projection areas are seen in Nycticebus. The projection area for the hand in Perodicticus is twice as large (relative to brain size) as in Galago and Perodicticus. The possible behavioral significance of increased differentiation of the hand area in Nycticebus and elaboration of the area in Perodicticus could be examined by study of hand use and tactile capacity in these same species.

Animals↗

Monophyletic origin of Alu elements in primates.

To get insight into the early evolution of the primate Alu elements, we characterized sequences of these repeats from the Malagasy prosimians, lemurs (Lemuridae) and sifakas (Indriidae), as well as from galagos (Lorisidae). These sequences were compared with the oldest Alu species known from the human genome: dimeric Alu J and S and free Alu monomers. Our analysis indicates that about 60 Myr ago, before the prosimian divergence, free left and right monomers formed an Alu heterodimer connected by a 19-nucleotide-long A-rich linker. The resulting elements successfully propagated in diverging primate lineages until about approximately 20 Myr ago, conserving similar sequence features and essentially the same Alu RNA secondary structure. We suggest that until that time the same "retropositional niche", molecular machinery making possible the proliferation by retroposition, constrained the evolution of Alu elements in extant primate species. These constraints became subsequently relaxed. In the Malagasy prosimians the dimeric Alu continued to amplify after acquiring a 34- to 36-nucleotide extension of their linker segment, whereas in the galago genome the "retropositional niche" was occupied by novel short elements.

Animals↗

The myoglobin of primates. VII. Perodicticus potto edwarsi (potto).

The primary structure of the myoglobin of the prosimian Lorisidae Perodictius potto edwarsi (potto) was studied. Tryptic, chymotryptic, peptic, subtilisin and thermolysin peptides were aligned against the sequence of human myoglobin. Sixteen differences were found which were confirmed by sequential analysis. On comparison of the West African potto with two other prosimian myoglobins known so far, there were 12 differences between the potto and the galago (East African) and 18 differences between the potto and the sportive lemur (Madagascar).

Amino Acid Sequence↗

Primate jumping genes elucidate strepsirrhine phylogeny.

Transposable elements provide a highly informative marker system for analyzing evolutionary histories. To solve controversially discussed topics in strepsirrhine phylogeny, we characterized 61 loci containing short interspersed elements (SINEs) and determined the SINE presence-absence pattern at orthologous loci in a representative strepsirrhine panel. This SINE monolocus study was complemented by a Southern blot analysis tracing multiple loci of two different strepsirrhine specific SINEs. The results thereof were combined with phylogenetic trees reconstructed on the basis of complete mitochondrial cytochrome b sequences from all recognized strepsirrhine genera. Here we present evidence for (i) a sister group relationship of Malagasy Chiromyiformes and Lemuriformes, (ii) Lorisidae being a monophyletic sister clade to the Galagidae, and (iii) common ancestry of African and Asian lorisids. Based on these findings, we conclude that strepsirrhines originated in Africa and that Madagascar and Asia were colonized by respective single immigration events. In agreement with paleocontinental data, the molecular analyses suggest a crossing of the Mozambique channel by rafting between the late Cretaceous and the middle Eocene, whereas Asia was most likely colonized between the early Eocene and the middle Oligocene on a continental route. Furthermore, one SINE integration links the two Lemuriformes families, Lemuridae and Indriidae, indicating a common origin of diurnality or cathemerality and a later reversal to nocturnality by the indriid genus Avahi.

Animals↗

Evolution of the sweetness receptor in primates. II. Gustatory responses of non-human primates to nine compounds known to be sweet in man.

The gustatory responses of nine compounds, namely glycine, D-phenylalanine, D-tryptophan, cyanosuosan, magapame, sucrononate, campame, cyclamate and superaspartame, all known as sweet in man, were studied in 41 species or subspecies of non-human primates, selected among Prosimii (Lemuridae and Lorisidae), Platyrrhini (Callitrichidae and Cebidae) and Catarrhini (Cercopithecidae, Hylobatidae and Pongidae). The first six compounds are generally sweet to all primates, which implies that they interact with the primate sweetness receptors essentially through constant recognition sites. Campame is sweet only to Cebidae and Catarrhini, cyclamate only to Catarrhini, superaspartame principally to Callitrichidae and Catarrhini, which implies that all these compounds interact with the receptors partly through variable recognition sites. From the present work, from other previous results (where notably it was observed that alitame is sweet to all primates, ampame only to Prosimii and Catarrhini, and aspartame only to Catarrhini), and from the multipoint attachment (MPA) theory of sweetness reception (as elaborated by Nofre and Tinti from a detailed study of structure-activity relationships of various sweeteners in man), it is inferred that the primate sweetness receptors are very likely made up of eight recognition sites, of which the first, second, third, fourth, seventh and eighth are constant, and the fifth and sixth variable. From these results and from the MPA theory, it is also inferred that the recognition sites of the primate sweetness receptors could be: Asp-1 or Glu-1, Lys-2, Asp-3 or Glu-3, Thr-4, X-5, X-6, Thr-7, Ser-8, where the variable recognition sites X-5 and X-6 would be: Ala-5 and Ala-6 for Callitrichidae, Ser-5 and Ala-6 for Cebidae, Ala-5 and Thr-6 for Prosimii, and Thr-5 and Thr-6 for Catarrhini. By using Tupaiidae (tree shrews) as a reference outgroup and by means of other structural and functional molecular considerations, it appears that Callitrichidae have retained the most primitive receptor among the four types of primate receptors. The possible taxonomic and phylogenetic implications of these findings are discussed.

Animals↗

Taste preference in nonhuman primates to compounds sweet in man.

Primates have stimulated more interest than any other group as humans are ranked in this same mammalian order. Gustatory responses of human and nonhuman primates have already been compared for compounds such as monosaccharides, oligosaccharides, polyols, amino acids, dipeptides, proteins, dihydrochalcones, sulfamates, saccharin, acesulfame, diterpenes or urea derivatives, all known to be sweet in man. But no rational comparison in primates has been attempted. Using a structure-activity relationship study in primates, it is now possible to classify the primate sweetness receptors into four types according to the behavioral responses observed from various selected compounds sweet in humans. The four types are represented by (1) the Callitrichidae and (2) the Cebidae, both from the infraorder Platyrrhini (New World monkeys), (3) the Lemuridae and Lorisidae, from the suborder Prosimii (prosimians), and (4) the Cercopithecidae (Old World monkeys), Hylobatidae (lesser apes), Pongidae (great apes), and Hominidae (humans) from the infraorder Catarrhini (Old World simians). By a comparative study of the putative receptor recognition sites postulated for each type of receptor, it is inferred that the Callitrichidae (marmosets and tamarins) have retained the most primitive sweetness receptor among primates. As we believe that the evolution of the sweetness receptor is a key factor involved in the raising of nonhuman primates from a 'primitive grade' towards a more 'advanced' or 'simian grade,' the possible phylogenetic implications of these findings will be discussed.

Animals↗

Immunodiffusion systematics of the primates. III. The strepsirhini.

Immunodiffusion comparisons have been run using 26 antisera including seven made to strepsirhine species. Spur size data resulting from these comparisons have been analyzed by computer and depict Strepsirhini as a monophyletic group within Primates including Lemuriformes and Lorisiformes. Cheirogaleidae is retained with Lemuriformes. Indriidae rather than Cheirogaleidae is depicted as closer to Lemur. Evidence is presented indicating that Lorisiformes is composed of three groups rather than two as in traditional classifications. The three groups, which are considered here to diverage at a family level, are Galagidae, Lorisidae, and Perodicticidae.

Animals↗

Renal disease in prosimians.

At the San Diego Zoo, renal lesions occurred spontaneously in 22 of 113 prosimian primates, 17 of them in the family Lorisidae (14 in galagos), three in Lemuridae, and one each in Indriidae and Tupaiidae. Of the Galago cases, six were in G. senogalensis and eight in G. crassicadatus panganiensis. Lesions included focal and diffuse proliferative glomerulonephritis, membranoproliferative glomerulonephritis, interstitial nephritis, and pyelonephritis.

Animals↗

Non-invasive detection and monitoring of estrus, pregnancy and the postpartum period in pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites.

Estrone-conjugates (E1C) were measured in the feces of six female pygmy lorises (Nycticebus pygmaeus) during estrus (n = 12), pregnancy (n = 4) and the postpartum period (n = 3). Noninvasive feces collection permitted frequent sampling throughout estrus and pregnancy, without disturbance of animals. The estrous period was defined as an increase in fecal E1C levels above an average of 70 ng/g feces with peaks above 100 ng/g feces obtained in consecutive fecal samples collected over a 6- to 11-day period between the end of July and the first third of October. Comparison of the periovulatory profile of E1C and the stage of labial opening of the vagina revealed a high agreement (P < 0.001). In all pregnant females, an E1C rise was found approximately 47 days postestrus, the source of which may be the growing fetal placental unit. Estimated gestation lengths ranged between 187 and 198 days (n = 4).

Animals↗

Cranial allometry and geographic variation in slow lorises (Nycticebus)

A series of 20 craniodental measurements was obtained for two sister taxa: Nycticebus coucang (common slow loris) and N. pygmaeus (pygmy slow loris). Multivariate analysis of variance was performed with adult data to describe patterns of subspecific and specific variation in this genus. The geometric mean of adult cranial dimensions was compared to field data on latitudinal coordinates for available specimens to investigate if size variation in Nycticebus is clinal in nature. Ontogenetic series for larger-bodied N. coucang and smaller-bodied N. pygmaeus were compared to test the hypothesis that species and subspecific variation in skull form results from the differential extension of common patterns of relative growth. A MANOVA provides independent support of Groves's [pp. 44-53 in Proceedings of the Third International Congress on Primatology, Vol. 1 (Basel: S. Karger), in 1971)] classification of Nycticebus into two species, with four subspecies in the common slow loris and one form of the pygmy slow loris. Within N. coucang, cranial proportions for all four subspecies are ontogenetically scaled, and size differentiation is mainly clinal (Bergmann's Rule). N. c. bengalensis represents the most northerly disposed and the largest form. N. c. javanicus represents the next-largest form and is located in a southerly direction the next-farthest away from the equator. N. c. coucang and N. c. menagensis are both equatorial; however, the latter subspecies is the smallest. A genetic basis for some of the taxonomic variation between N. c. coucang and N. c. menagensis is supported by such nonclinal variation in body size. Variation in the presence/absence of I2 is not size-related but rather tracks geographic proximity and isolating factors which predate the most recent inundation of the Sunda Shelf. Although they inhabit a nonequatorial environment, pygmy slow lorises are the smallest of all Nycticebus. As N. pygmaeus is sympatric with N. c. bengalensis, the largest slow loris, it appears that the evolution of its smaller body size represents a case of character displacement. Unlike N. coucang, skull size becomes significantly smaller in more northern N. pygmaeus. This may also reflect character displacement between sympatric sister taxa underlain by a cline-dependent ecological factor which is marked in more northerly latitudes. On the other hand, the negative correlation between body size and latitude in N. pygmaeus could be due to the influence of nonprimate fauna, such as predators, which themselves evince a similar clinal pattern. Analyses of relative growth indicate that skull proportions in the two species of Nycticebus are ontogenetically scaled in two-thirds of the cases. All but one of the seven comparisons (interorbital breadth) which do not indicate ontogenetic scaling represent part of the masticatory complex. This likely reflects a reorganization of N. pygmaeus maxillomandibular proportions linked to smaller size and changes in diet.

Animals↗

Monitoring pregnancy in twinning pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites.

Estrone and estrone conjugates were measured in the feces of three female pygmy lorises (Nycticebus pygmaeus) throughout estrus, pregnancy, and the postpartum period. Two females gave birth to twins, while the third had a single stillborn. A comparison between the hormonal profiles of these three pregnancies with each other and with previously reported pregnancies resulting in singletons or twins [Jurke et al., American Journal of Primatology 41:103-115, 1997] revealed a characteristic pattern of hormonal excretion. This report adds data to and confirms previous claims that monitoring estrone in this species provides a tool to assess gestation length (via determination of estrus period) and to predict the date of parturition and the number of offspring. However, there was an exceptional case of a pregnancy which had the hormonal appearance of a twin pregnancy but resulted in a single stillborn infant. This case prompted us to search for new insights into the characteristics and the origin of the estrogens that are excreted into the feces. Aromatase activity was evaluated in five partial placentae.

Animals↗