Sublingual structures in primates. Part 1: Prosimiae, Platyrrhini and Cercopithecinae

1. The sublingual structures of primates have been studied light-microscopically. There are 3 different sublingual structures in the species studied. The plica sublingualis occurs in all primates. The sublingual organ is a topographically modified plica sublingualis which occurs exclusively in Callicebus. A sublingua is present only in the prosimians. 2. The plica sublingualis contains the excretory ducts of the submandibular and sublingual salivary glands. The sublingua is ventrally adherent to the body of the tongue and is, with a few exceptions in Tupaia, characterized by a skeleton of cartilage tissue. A sublingua never exhibits excretory ducts or salivary glands. 3. In some Platyrrhini (Ateles, Aotus, Lagothrix, Alouatta, Callicebus), there are taste buds in the epithelium of the plica sublingualis. They are especially concentrated near the orifices of the salivary glands. 4. The fresh saliva of the submandibular and sublingual gland can be tested by the taste buds on the plica sublingualis, because there is a topographical coincidence. 5. There is a complete absence of taste buds at the plica sublingualis of the prosimians and the Cercopithecinae. 6. There are no taste buds in the epithelium of the sublingua. In the Lorisiformes and in the Lemuriformes the sublingua is a cleaning device of the anterior dentition, most probably in connection with a tactile sensibility. In the Tupaiformes and in the Tarsiiformes the sublingua is less developed. 7. There is no anatomical connection between the skeleton of cartilage tissue in the sublingua and the lytta, or the skeleton of the hyoideum. 8. In some Cercopithecinae (Macaca, Papio) a glandula apicis linguae is present.     

On the sublingual structures of Tarsius (Prosimiae, Tarsiiformes) and some platyrrhine monkeys (Platyrrhina, Simiae, Primates) with casual remarks on the histology of the tongue. In memoriam William Charles Osman Hill.

The sublingual structures of Tarsius, Cebuella and Callithrix are studied microscopically. Tarsius has a well developed but not specialized sublingua. In the platyrrhine monkeys the sublingua is lacking completely, but the frenal lamella (plica sublingualis) is very specialized. From this it is concluded that the sublingual organ of Callicebus is a topographically modified frenal lamella, not a sublingua.     

Sublingual structures of primates. II. Hominoidea, review, summary and literature

1. In Homo and the great apes (Pongidae) there occurs, besides the plica sublingualis a plica fimbriata at the ventral surface of the tongue. This duplicature of the mucosa does not occur in the Hylobytidae and in the other primates. 2. Some taste buds could be found in the epithelium of the plica sublingualis of the Pongidae. 3. There are many taste buds in the epithelium of the plica fimbriata of the Pongidae. On this sublingual structure there were counted 1776 taste buds in Pongo, 592 in Gorilla and 280 in Pan. A few taste buds could also be found on the plica fimbriata of a human newborn. 4. A glandula apicis linguae occurs in Homo, Pan, Gorilla and Pongo. 5. The fresh saliva of the glandula apicis linguae and the saliva on the floor of the mouth can be tested by the taste buds in the epithelium of the plica fimbriata, of papillae lenticulares and of areae gustatoriae at the ventral surface of the tongue. 6. It might be the function of the sublingual taste buds to taste the fresh saliva as a gradient for the central nervous comparison with the taste of the saliva on the dorsal surface of the tongue. 7. Because of the complete absence of a sublingua in the Platyrrhini and in the Cercopithecinae it is unlikely that the plica fimbriata of Homo and the great apes can be interpreted as a homalogon of the sublingua in the prosimians. 8. Because of the absence of a sublingua in other ordines of the Mammalia (Insectivora, Carnivora, Rodentia, Chiroptera, Ungulata) it is unlikely as well that the sublingua in the prosimians can be interpreted as a homologon of the tongues of the lower vertebrates. The sublingual structures occuring in the Marsupialia have to be investigated. 9. Because of these reasons the new development of the sublingua in the prosimians and the plica fimbriata in the Hominoidea, in complete independence from one another, seems to be a better explanation of the 2 structures and less contradictionary to anatomical and phylogenetic arguments. The different function of both structures in the recent primates gives a hint for the possible reason for their development during the process of evolution.     

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.     

Developmental morphology of the solum nasi in the mouse lemur (Microcebus murinus)

The solum nasi of Microcebus murinus is characterized by the presence of a zona annularis, continuity between the anterior transverse lamina and the paraseptal cartilage, a continuous paraseptal cartilage, a palatine cartilage and a posterior transverse lamina. It lacks a fibula reuniens and possibly a cartilage of the nasopalatine duct as well as a palatine papillary cartilage. The morphology in M. murinus closely resembles that seen in Tupaia and Galago. This affinity results from the retention of primitive traits. However, Galago is reported to lack a zona annularis, thus displaying a specialization not shared with M. murinus. Therefore, the zona annularis provides a useful trait for distinguishing between the ontogenies of M. murinus and Galago.     

Patterns of sexual dimorphism in body weight among prosimian primates.

Many primatologists believe that there is no sexual dimorphism in body size in prosimian primates. Because this belief is based upon data that came from only a few species and were largely flawed in some aspect of sample quality, I re-examined the extent of sexual dimorphism in body weight, using weights of 791 adult prosimians from 34 taxa recorded over the last 17 years at the Duke University Primate Center. There was no significant sex difference in body weight in 17 species, but males were significantly larger in Nycticebus pygmaeus, Tarsius syrichta, Galago moholi, Galagoides demidovii, Otolemur crassicaudatus and Otolemur garnettii. Moreover, females were significantly larger in Microcebus murinus. Thus, the general lack of sexual dimorphism could be confirmed, notably for lemurs, but prosimians as a group show more variability in sexual size dimorphism than was previously thought. After including previously published data obtained in the wild from 8 additional species, I found significant heterogeneity in the degree of sexual dimorphism at the family level, but only the Indridae and Galagidae were significantly different from each other. Among the prosimian infraorders, the Lorisiformes were significantly more dimorphic than the Lemuriformes. Differences in dimorphism between higher taxonomic groups are discussed in the context of prosimian evolution, concluding that phylogenetic inertia cannot provide a causal explanation for the evolution of sexual dimorphism. The relative monomorphism of most prosimians may be related to allometric constraints and, especially in the Lemuriformes, to selective forces affecting male and female behavioral strategies.     

The anatomical relations of the ductus vomeronasalis and the occurrence of taste buds in the papilla palatina of Nycticebus coucang (primates, prosimiae) with remarks on strepsirrhinism.

Nycticebus coucang is typically strepsirrhine. This condition is basically the same in all prosimians except Tarsius. The rhinarium shows a labial part; the marked furrow in its median plane clefts the margin of the upper lip. The latter is attached to the gum between the median incisors by means of paired folds (not corresponding to a frenulum labii superioris). The labial cleft is continued in the sulcus papillae palatinae. The ductus vomeronasalis opens into the ductus nasoplatinus which, in turn, enters the aboral part of the sulcus palatinus. Thus strepsirrhinism provides, occasionally, an open communication of the olfactory systems (nose, vomeronasal organ) with the environment in front of the rhinarium. Strepsirrhine primates possess an internarium very similar to the one of platyrrhine monkeys. The shape of the nostrils is not characteristics for strepsirrhinism. A split-lip condition is likely ancestral to the complete lip condition, since it is found in several stems of mammals, especially in archaic forms. Strepsirrhinism, such as in lemuroid prosimians, is probably just one case of the primitive split-lip condition. Therefore, a median furrow in the external hairy skin of the upper lip, found in some platyrrhine monkeys, could be a rudiment of a cleft, indicating that a kind of a split lip condition was ancestral to the undivided lips of platyrrhine monkeys. Taste buds occur in the epithelium of the lateral surface of the papilla palatina of Nycticebus. Other lorisid prosimians have not been studied in this respect. The taste buds test water soluble substances entering the sulcus either way. These substances may come from the environment entering the sulcus through the labial cleft.     

Development of the pharyngeal arch skeleton in Catostomus commersonii (Teleostei: Cypriniformes)

Skeletal elements of the gill arches of adult cypriniform fishes vary widely in number, size, and shape and are important characters in morphologically based phylogenetic studies. Understanding the developmental basis for this variation is thus phylogenetically significant but also important in relation to the many developmental genetic and molecularly based studies of the early developing and hence experimentally tractable gill arches in the zebrafish, a cyprinid cypriniform. We describe the sequence of the chondrification and ossification of the pharyngeal arches and associated dermal bones from Catostomus commersonii (Catostomidae, Cypriniformes) and make selected comparisons to other similarly described pharyngeal arches. We noted shared spatial trends in arch development including the formation of ventral cartilages before dorsal and anterior cartilages before posterior. Qualitatively variable gill arch elements in Cypriniformes including pharyngobranchial 1, pharyngobranchial 4, and the sublingual are the last such elements to chondrify in C. commersonii. We show that the sublingual bone in C. commersonii has two cartilaginous precursors that fuse and ossify to form the single bone in adults. This indicates homology of the sublingual in catostomids to the two sublingual bones in the adults of cobitids and balitorids. Intriguing patterns of fusion and segmentation of the cartilages in the pharyngeal arches were discovered. These include the individuation of the basihyal and anterior copula through segmentation of a single cartilage rod, fusion of cartilaginous basibranchials 4 and 5, and fusion of hypobranchial 4 with ceratobranchial 4. Such “fluidity” in cartilage patterning may be widespread in fishes and requires further comparative developmental studies. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Vegetation Thresholds for the Occurrence and Dispersal of <Emphasis Type="Italic">Microcebus griseorufus</Emphasis> in Southwestern Madagascar

Primate populations are declining the world over due to anthropogenic threats, including habitat loss and degradation. This raises the important question of how much habitat degradation a species can cope with. Habitat degradation is pronounced in Madagascar, where most of the human population depends on the direct exploitation of natural resources. We aimed to identify the response of Microcebus griseorufus (the gray-brown mouse lemur) to forest degradation and to define the structural traits of the vegetation that might be crucial for the species’ occurrence in anthropogenic landscapes. We documented the occurrence of Microcebus griseorufus in relation to vegetation structures along a gradient of forest degradation, at the edge of and west of Tsimanampetsotsa National Park in April and May 2007 and from October to December 2015. We confirmed the occurrence of Microcebus griseorufus using trapping and visual surveys, and measured vegetation structure. Logistic regression models showed that Microcebus griseorufus has a threshold response to tree density and the diameter of thick trees. The thresholds of occurrence were at 10–15% of the tree density recorded in intact forest and a mean diameter of trees with a diameter at breast height of >10 cm of 14.3 cm. The definition of such thresholds might help to maintain suitable habitat for this species and other primates living in anthropogenic landscapes, providing connectivity between isolated protected areas and allowing dispersal between populations.     

The ontogenesis of the manubrium sterni in Tupaia belangeri

The morphogenesis of the manubrium sterni was studied in a series of dated embryos of Tupaia belangeri. In addition to the sternal bands, the "paired suprasternal Anlage" takes part in the shaping of the manubrium sterni as reported by Klima (1968) for other mammals. It forms skeletal elements that mediate between the clavicle and the manubrium: the sternocalvicular ligament and the paired prominence on the dorsal surface of the manubrium, which underlies the clavicles. The paired prominence corresponds to the praeclavium present in some therians. Very probably, the discus articularis of the sternoclavicular articulation of some primates can be attributed to the suprasternal Anlage. There was, however, no indication that the ossa suprasternalia of primates develop from the suprasternal Anlagen: In Tupaia these Anlagen do not form the cranial part of the manubrium. Klima's "unpaired Anlage" develops differently in Tupaia than in other therians. It consists of connective tissue and is not integrated into the manubrium. It presents an insertion surface for the M. pectoralis major, which shifts its origin onto the manubrium, after the sternal bands have fused. The homology of the "unpaired Anlage" and the "pars chondralis interclaviculae" is doubtful.     

Origin and evolution of primate social organisation: a reconstruction

The evolution and origin of primate social organisation has attracted the attention of many researchers, and a solitary pattern, believed to be present in most nocturnal prosimians, has been generally considered as the most primitive system. Nocturnal prosimians are in fact mostly seen alone during their nightly activities and therefore termed 'solitary foragers', but that does not mean that they are not social. Moreover, designating their social organisation as 'solitary', implies that their way of life is uniform in all species. It has, however, emerged over the last decades that all of them exhibit not only some kind of social network but also that those networks differ among species. There is a need to classify these social networks in the same manner as with group-living (gregarious) animals if we wish to link up the different forms of primate social organisation with ecological, morphological or phylogenetic variables. In this review, we establish a basic classification based on spatial relations and sociality in order to describe and cope properly with the social organisation patterns of the different species of nocturnal prosimians and other mammals that do not forage in cohesive groups. In attempting to trace the ancestral pattern of primate social organisation, the Malagasy mouse and dwarf lemurs and the Afro-Asian bushbabies and lorises are of special interest because they are thought to approach the ancestral conditions most closely. These species have generally been believed to exhibit a dispersed harem system as their pattern of social organisation ('dispersed' means that individuals forage solitarily but exhibit a social network). Therefore, the ancestral pattern of primate social organisation was inferred to be a dispersed harem. In fact, new field data on cheirogaleids combined with a review of patterns of social organisation in strepsirhines (lemurs, bushbabies and lorises) revealed that they exhibit either dispersed multi-male systems or dispersed monogamy rather than a dispersed harem system. Therefore, the concept of a dispersed harem system as the ancestral condition of primate social organisation can no longer be supported. In combination with data on social organisation patterns in 'primitive' placentals and marsupials, and in monotremes, it is in fact most probable that promiscuity is the ancestral pattern for mammalian social organisation. Subsequently, a dispersed multi-male system derived from promiscuity should be regarded as the ancestral condition for primates. We further suggest that the gregarious patterns of social organisation in Aotus and Avahi, and the dispersed form in Tarsius evolved from the gregarious patterns of diurnal primates rather than from the dispersed nocturnal type. It is consequently proposed that, in addition to Aotus and Tarsius, Avahi is also secondarily nocturnal.     

Food prehension and manipulation in Microcebus murinus (Prosimii, Cheirogaleidae)

Among primates, apes and monkeys are known to use their hands and to exhibit independent control of their fingers. In comparison, Prosimii are thought to have less digital individualization and to use their mouth more commonly for prehension. Unfortunately, prehension and manipulation studies in Prosimii have been conducted in conditions constraining the subject to grasp with the hand. Moreover, the effect of food size remains unexplored, even though it could affect the use of the hands versus the mouth. Thus, whether prosimians use the hand or the mouth to grasp and manipulate food items of different sizes in unconstrained conditions remains unclear. To address this question, we characterized the eating and manipulation patterns of Microcebus murinus in unconstrained conditions, using three food sizes. The results showed that M. murinus showed (i) an eating pattern similar to that of rodents, with smaller food items being grasped with the mouth, (ii) a greater tendency to use the hands for prehension of larger foods, and (iii) plasticity during food manipulation similar to that which has been observed in rodents. These results are discussed in the framework of grasping in mammals and are used to discuss the origins of prehension in primates.     

Unique proximal tibial morphology in strepsirrhine primates

Although the morphology of the tibial plateau in primates has received very little attention in the literature, it does exhibit features of phylogenetic and functional interest. This paper describes the morphology of the tibial plateau (particularly the intercondylar region) in extant and fossil primates, and in three mammalian outgroups: the pen-tailed tree shrew (Ptilocercus), tree shrew (Tupaia), and flying lemur or dermopteran (Cynocephalus). Extant and fossil strepsirrhine primates exhibit an eminence with a single spine, which contrasts with the intercondylar morphology of haplorhine primates. Most extant platyrrhines, all catarrhine primates (including humans), and some fossil haplorhines possess an eminence with two spines (medial and lateral) connected by a ridge of bone that intersects the intercondylar groove. Tarsius and callitrichines possess an eminence with a reduced medial spine that superficially resembles that of strepsirrhine primates. Dermopterans also exhibit a morphology similar to that of strepsirrhines. In Scandentia, the intercondylar morphology of Tupaia is similar to that of rodents, whereas Ptilocercus resembles tarsiers and callitrichines. We hypothesize that proximal tibiae with either a single spine or reduced medial spine morphology facilitate a greater degree of knee rotation about the eminence relative to the double-spine condition, and are likely associated with more frequent adoption of vertical body positions. In contrast, a double-spine eminence limits knee rotation and is probably associated with greater use of horizontal supports. Although the polarity is complicated by the unknown phylogenetic status of likely sister taxa, it seems most probable that the single-spine morphology is a derived feature of strepsirrhines.     

The development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

Sperm Ultrastructure of Tarsius bancanus(Tarsiidae, Primates): Implications for Primate Phylogeny and the Use of Sperm in Systematics

The ultrastructure of the epididymal sperm of Tarsius bancanus is described. The sperm possess the typical eutherian pattern of a dorsoventrally flattened, ovate sperm head, comprising a nucleus capped by a symmetrical acrosome, and a distinct midpiece and principal piece containing a 9 + 9 + 2 arrangement of outer coarse fibres and microtubules. However, unique features are also present. The overall head length (9 μm) equals the greatest for any primate yet examined, and the subacrosomal space ("perforatorium" or "pseudoperforatorium") tilted at 30° to the sagittal axis of the sperm, is described for the first time for mammals. The acrosome extends only a short distance beyond the length of the nucleus of the mature sperm, and a significant reduction in the acrosome to nuclei ratio appears to occur during the final stages of sperm maturation. In contrast to earlier predictions based on the spermatid of Tarsius syrhicta , the mature spermatozoa of Tarsius shows greatest morphological similarity with the sperm of the Anthropoidea, which have a short symmetrical acrosome, than with the Strepsirhini, which have a relatively long acrosome that can be either symmetrical (Lemuriformes) or asymetrical (Lorisiformes). Four proposed phylogenies of the Primates are assessed using comparative sperm ultrastructure. Placing the Tarsiidae as a sister group to the Lorisidae appears the least likely. The sperm data are consistent with the Tarsiidae being a sister group to the Anthropoidea, to the Strepsirhini, or even to the extant primate groups as a whole. Use of sperm morphology to provide characters in phylogenetic systematics of the primates is discussed, and the principle of "total evidence" is preferred to the common practice of "hanging" sperm on phylogenetic hypotheses based on other evidence. © 1997 The Royal Swedish Academy of Sciences. Published by Elsevier Science Ltd.     

Polymorphic microsatellite markers for Philippine tarsiers (<Emphasis Type="Italic">Tarsius syrichta</Emphasis>)

This study reports the isolation and characterization of eight microsatellite markers for the study of Philippine tarsiers (Tarsius syrichta), small primates endemic to this Southeast Asian archipelago. The markers were used to screen 14 Tarsius syrichta for allelic diversity. This suite of highly polymorphic microsatellites provides the first chance to genetically study parentage and dispersal patterns in Philippine tarsiers.     

Morphology and histology of the larynx of the common toad Rhinella arenarum (Hensel, 1867) (Anura,Bufonidae)

The structure of the larynx of the toad Rhinella arenarum was exhaustively studied. The laryngeal skeleton consists of three bilaterally symmetrical cartilages: the cricoid and two arytenoids. Internally, each half‐larynx has an anterior and a posterior chamber. The first chamber is delimited by the epithelium covering the arytenoid cartilage and the anterior membrane. The latter consists of fibro‐elastic tissue and contains blood capillaries that, judging by their location and distribution, might serve to maintain vocal cord turgidity. At the level of the cricoid cartilage, two structures are reported here for the first time: the posterodorsal and the anteroventral processes. Both processes are associated with the insertion of the posterior membrane. A cartilaginous rod is located at the free margin of the posterior membrane. This rod appears to support the membrane when the air flows. The distal portion of the larynx communicates with the proximal region of the lung. The epithelium of the laryngeal mucosa contains ciliated cells, goblet cells, secretory cells with short microvilli and neuroendocrine cells immunopositive to PGP 9.5. The results obtained in this study provide new information about the internal organization of the larynx in anurans, which could serve as additional morphological characters for phylogenetic relationships.     

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.     

Front dentition of the omomyiformes (Primates)

Within the primates the front dentition plays a major role in the classification of the different taxa. The extant strepsirhines are clearly characterized by the possession of a tooth comb. Tarsius differs in this complex by a construction which remembers the beak of an owl (vertically implanted medial incisors, upper pair bigger than mandibular pair). The front teeth of the extinct Microchoeridae are described. The dental formula of the group is discussed and compared with the Omomyidae. The wear pattern presents evidence of a dental comb as early as the Late Eocene.