Led by the nose: Olfaction in primate feeding ecology

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. 1 This view shifted with the growing understanding of its role in social behavior 2 and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory‐dependent mammals such as dogs and rodents. 3 , 4 Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large‐scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates’ feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.     

Loss of estrus in human evolution: Too many answers,too few questions

Models addressing the importance of “loss of estrus” in human evolution assume that, as part of a general trend among higher primates, endogenous hormonal fluctuations have less influence on human female sexuality than cognitive and socioenvironmental factors. The diversity of reproductive patterns among primate species is not satisfactorily explained as the outcome of evolutionary trends along dimensions such as brain enlargement, behavioral flexibility, or relative independence of behavior from physiology. Rather, the role of hormones and other factors must be viewed in the context of species' life history and ecological constraints. Human studies on the relationship between the menstrual cycle and sexual behavior have been limited to Western women in industrialized societies, which may not reveal evolved behavioral-physiological patterns. Furthermore, available studies have yielded inconsistent results. No single pattern emerges that can be said to characterize the human female, and no conclusion can be reached regarding the relationship between cyclic hormonal fluctuations and sexual behavior and, thus, whether human ovulation is concealed. Future studies are needed that are methodologically improved and systematically document the interaction among ecological, subsistence, social, and physiological variables.     

Deciphering primate phylogeny from macromolecular specificities

A problem in deciphering primate phylogeny, morphological convergence between different evolutionary lines, can be overcome by species comparisons of proteins, macromolecules with specificities closely linked to the genetic code in DNA. Various chemical, electrophoretic, and immunological data on serum and tissue proteins in primates are reviewed with respect to their phylogenetic significance. Much of this data deals with protein specificities in the Hominoidea and depicts a particularly close genetic relationship between man and the African apes. Hominoidea, Cercopithecoidea, Ceboidea, and Lorisoidea are characterized by their proteins as monophyletic or natural taxa, even though the conventional subdivisions within several of these superfamilies are not in complete accord with the protein analyses. The protein evidence supports the conventional grouping of Cercopithecoidea with Hominoidea in the infraorder Catarrhini and the grouping of Catarrhini and Platyrrhini (Ceboidea) in the suborder Anthropoidea. Lemuroidea and Lorisoidea appear to be closer to one another than to either Tupaioidea or Anthropoidea and closer to the Anthropoidea than to the Tupaioidea. Comparisons of primate DNA's by Hoyer and coworkers are demonstrating genetic affinities among primates which agree with those deduced from the comparison of protein specificities. Species differences and similarities in the relative amounts of different protein macromolecules reflect the grade relationships of primates, but, unlike the comparisons of amino-acid sequences or antigenic specificities, are not reliable indicators of phyletic affinities. Data on the ratios of M(uscle) to H(eart) type lactate dehydrogenase in a series of primate brains provides a biochemical example of the concept that there are “lower” (primitive) and “higher” (advanced) grades of evolutionary development among the extant primates.     

Ontogeny,auditory structures,and primate evolution

The anatomy of the auditory region, particularly the carotid circulatory patterns and ectotympanic-petrosal relationships, has played a prominent role in primate systematics and phylogenetic reconstructions. Ontogenetic stages of petrosal-ectotympanic relationship are presented for certain strepsirhines. It is suggested that the “ectotympanic tube” or “ossified annulus membrane” found in early Tertiary primates is not necessarily an homologous structure to the true ectotympanic tube seen in haplorhines, and thus cannot be considered a shared, derived feature linking known Paleogene primates from Europe or North America to tarsioid and/or anthropoid ancestry. No fossil primate yet discovered makes a convincing ancestor for the earliest known anthropoids from the Oligocene of Africa. This is probably due to the fact that it still lies undiscovered in the Paleogene of Africa.     

Cranial asymmetry in Ceboid primates: The emissary foramina

Until the last decade or so, relatively little was known of cranial asymmetries in nonhuman primates. Data are slowly, but surely, accumulating for such features as transverse sinus flow, sylvian point angle differences, external brain morphology, etc. Cranial asymmetries are being analyzed and related to such diverse problems as “handedness” and phylogenetic systematics. It has been known for over 200 years that cranial asymmetry exists in some of the cerebral blood flow patterns in man, particularly the internal jugular pathway. Although earlier anatomists assumed this was only characteristic of “higher primates” (meaning man and the great apes), little quantitative data have been available to either support or deny this belief. There is a particular dearth of information for New World primates. The aim of this study is to contribute to the growing literature on cerebral asymmetries by partially filling in this gap in our knowledge of New World primate biology.     

Links between the discovery of primates and anatomical comparisons with humans,the chain of being,our place in nature,and racism

I focus on the crucial links between the discovery of nonhuman primates by Westerners, discussions on our place in nature, the chain of being, racism, and the history of primate comparative anatomy and of so‐called “anatomical human racial studies.” Strikingly, for more than a millennium humans knew more about the internal anatomy of a single monkey species than about that of their own bodies. This is because Galen used monkeys to infer human anatomy, in line with the human‐animal continuity implied by the Greek notion of scala naturae. With the rise of Christianity, nonhuman primates were increasingly seen in a negative way. A more positive view emerged in the 14th century when nonhuman primates were directly studied/seen by Europeans, culminating in Tyson's 1699 work showing that chimps share more gross anatomical similarities with humans than with monkeys. However, the discomfort caused by this human‐chimp similarity then led to a new idea of animal‐human discontinuity, now related not to anatomy but to “civilization”: between Europeans vs. non‐Europeans + other primates. Moreover, Linnaeus' Systema Naturae and the emergence of “anatomical racial studies” influenced by Camper's craniology then led to even more extreme ideas, such as the notion that Europeans were both mentally and morphologically “ideal.” Unfortunately the biased and often incorrect “results” of such studies, combined with ideas based on Darwin's “struggle for survival”, became crucial in propaganda that lead to the rise of eugenics in the end of the 19th/first half of 20th centuries and that culminated in Nazism. Since the 1950s there has been an emphasis on the continuity/unity between all human groups and other primates, in great part influenced by what happened during World War 2. Reviews such as this one are, therefore, particularly necessary to illuminate and guard against attitudes against “the Other” and racist ideologies that are re‐emerging in modern political discourse across the globe.     

Extending Ethnoprimatology: Human–Alloprimate Relationships in Managed Settings

The majority of studies in ethnoprimatology focus on areas of sympatry where humans and nonhuman primates (hereafter, primates) naturally coexist. We argue that much can be gained by extending the field’s scope to incorporate settings where humans manage most aspects of primates’ lives, such as zoos, laboratories, sanctuaries, and rehabilitation centers (hereafter, managed settings). We suggest that the mixed-methods approach of ethnoprimatology, which facilitates examination of both humans’ and primates’ responses to one another, can reveal not only how humans’ ideas about primates shape management strategies, but also how those management strategies affect primates’ lives. Furthermore, we note that a greater focus on managed settings will strengthen links between ethnoprimatology and primate rights/welfare approaches, and will introduce new questions into discussions of ethics in primatology. For example, managed settings raise questions about when it might be justifiable to restrict primates’ freedom for a “greater good,” and the desirability of making primates’ lives more “natural” even if this would decrease their well-being. Finally, we propose that because ethnoprimatology is premised on challenging false dichotomies between categories of field site—specifically, between “natural” and “unnatural” free-ranging populations—it makes sense for ethnoprimatologists to examine settings in which humans exert considerable control over primates’ lives, given that the distinction between “wild” and “captive” is similarly unclear.     

Towards an understanding of multimodal traits of female reproduction in chimpanzees

Primates - Although primates have long been regarded as microsmatic, recent studies indicate that olfaction is an important sensory mode of primate communication, e.g., in the context of...     

关于非人灵长类的公正行为的研究

人类关注公正, 非人灵长类也表现出公正行为。本文先以现有研究资料为基础, 以理毛为例分析后认为, 非人灵长类关注投入—收益的对称性, 说明它们可能具备不公正规避这一心理特质; 关于非人灵长类公正行为的实验也表明, 它们不仅比较自身的投入—收益对称性, 而且能在社会比较过程中与其它个体相比。有实验得出期望假设和挫折效应能更好地解释被试的行为, 本文认为, 这些实验结论不一致的主要原因, 是研究者未充分考虑"投入"对被试行为的影响。文章在最后进行了总结并提出了三点研究展望。     

The Ecology and Evolution of Fruit Odor: Implications for Primate Seed Dispersal

Primates are now known to possess a keen sense of smell that serves them in various contexts, including feeding. Many primate species are frugivorous and provide essential seed dispersal services to a variety of plants. Studies of pollination ecology, and recently seed dispersal ecology, indicate that animal mutualist behavior exerts selection pressures that drive changes in flower and fruit traits. As a result, the use of olfaction in in primate feeding ecology may have affected the evolution of fruit odor in species that rely on primate seed dispersal. However, this hypothesis is seldom tested. Here, we summarize the available information on how primates may have affected the evolution of fruit odor. We ask what the chemistry of primate fruit odor may look like, what information fruit odor may convey, whether there are geographical differences in fruit odor, and what other factors may affect the odor of fruits consumed by primates. We identify many gaps in the available data and offer research questions, hypotheses, and predictions for future studies. Finally, to facilitate standardization in the field, we discuss methodological issues in the process of odor sampling and analysis.     

The impact of plant secondary compounds on primate feeding behavior

The recent literature on plant secondary compounds and their influence on primate feeding behavior is reviewed. Many studies of nonhuman primates document the extreme selectivity that primates, particularly herbivorous species, demonstrate in their food choice. Until quite recently investigators interpreted this to mean that herbivorous primates were not food limited. This view has been challenged in the past 10 years by researchers concentrating on the primate–plant interaction. Chemical analyses have demonstrated that plant parts are of varying quality due to differences in nutrient and secondary compound content. The assumption that all leaves (or fruits, flowers, and insects) are potential foods of equal value to the primates eating them is refuted. The observed selectivity and preferences of primates for specific plant or insect species and parts are now viewed as strategies for dealing with the nutrient and secondary compound content variation in these foods.     

Raptors and primate evolution

Most scholars agree that avoiding predators is a central concern of lemurs, monkeys, and apes. However, given uncertainties about the frequency with which primates actually become prey, the selective importance of predation in primate evolution continues to be debated. 1 - 9 Some argue that primates are often killed by predators, 5 , 6 while others maintain that such events are relatively rare. 2 , 7 , 9 Some authors have contended that predation's influence on primate sociality has been trivial 10 , 11 ; others counter that predation need not occur often to be a powerful selective force. 12 - 14 Given the challenges of documenting events that can be ephemeral and irregular, we are unlikely ever to amass the volume of systematic, comparative data we have on such topics as feeding, social dynamics, or locomotor behavior. Nevertheless, a steady accumulation of field observations, insight gained from natural experiments, and novel taphonomic analyses have enhanced understanding of how primates interact with several predators, especially raptors, the subject of this review.     

Gene Golden Age paradox and its partial solution

The prevalence of purifying selection in the nature suggests that larger organisms bear a higher number of slightly deleterious mutations because of smaller populations and therefore weaker selection. In this work redistribution of purifying selection in favor of information genes, pathways and processes was found in primates compared with treeshrew and rodents on the ground of genome-wide analysis. The genes which are more favored in primates belong mainly to regulation of gene expression and development, in treeshrew and rodents, to metabolism, transport, energetics, reproduction and olfaction. The former occur predominantly in the nucleus, the latter, in the cytoplasm and membranes. Thus, although purifying selection is on average weaker in the primates, it is stronger concentrated on the “information technology” of life (regulation of gene expression and development). Increased accuracy of information processes probably allows escaping “error catastrophes” in spite of more complex organization, larger body size and higher longevity.     

Standardized descriptions of primate locomotor and postural modes

As quantitative studies on primate positional behavior accumulate the lack of a standard positional mode terminology is becoming an increasingly serious deficiency. Inconsistent use of traditional terms and inappropriate conflation of mode categories hamper interspecific and interobserver comparisons. Some workers use common terms without definition, allowing at least the possibility of misunderstanding. Other researchers coin neologisms tailored to their study species and not clearly enough defined to allow application to other species. Such neologisms may overlap, may completely encompass, or may conflate previously defined labels. The result is, at best, the proliferation of synonyms and, at worst, the creation of confusion where clarity had existed. Historical precedents have sometimes resulted in “catch-all” terms that conflate any number of kinematically different behaviors (e.g. “brachiation,” “climbing,” and “quadrumanous climbing”). We recognize three areas where distinction of positional modes has some current importance: (1) Modes that require humeral abduction should be distinguished from adducted behaviors; (2) locomotor modes that involve ascent or descent should be distinguished from horizontal locomotor modes; and (3) suspensory modes should be distinguished from supported modes. We recommend a nomenclature that is not dedicated to or derived from any one taxonomic subset of the primates. Here we define 32 primate positional modes, divided more finely into 52 postural sub-modes and 74 locomotor sub-modes.     

The functional morphology of the primate shoulder as revealed by comparative anatomical,osteometric and discriminant function techniques

A background to assessments of the ecological adaptations of fossil primates is the relationship of the detailed shape of bones in living forms to their known locomotor patterns, and this has been here attempted for the shoulder. Within the locomotion of the primates the function of the shoulder varies according to the extent to which the trunk is suspended by the arms. An analysis of the differences in the shoulder muscles has shown that much of their quantitative variation is mechanically in phase with these functional differences. A series of features of the shoulder bones, chosen because of their association with the mechanically meaningful features of the musculature, have been found to vary (a) in association with the known contrasts in locomotion and (b) in such a way as to render more efficient mechanically the associated muscular structure. Investigation of bony dimensions “residual” to such a study has shown that they are not highly correlated with primate locomotion but are, in contrast, associated with the commonly accepted taxonomic grouping of the order. The combination by discriminant functions of such sets of “locomotor” and “residual” dimensions reveals unsuspected information for living primates and might well allow more precise definition of the functional and taxonomic status of a fossil. The experimental testing of functional inferences from morphology is a necessary part of such studies, and preliminary reports of experimental stress analysis utilising the photoelastic technique confirm and reinforce their validity.     

Interactions between Social Structure,Demography, and Transmission Determine Disease Persistence in Primates

Catastrophic declines in African great ape populations due to disease outbreaks have been reported in recent years, yet we rarely hear of similar disease impacts for the more solitary Asian great apes, or for smaller primates. We used an age-structured model of different primate social systems to illustrate that interactions between social structure and demography create ‘dynamic constraints’ on the pathogens that can establish and persist in primate host species with different social systems. We showed that this varies by disease transmission mode. Sexually transmitted infections (STIs) require high rates of transmissibility to persist within a primate population. In particular, for a unimale social system, STIs require extremely high rates of transmissibility for persistence, and remain at extremely low prevalence in small primates, but this is less constrained in longer-lived, larger-bodied primates. In contrast, aerosol transmitted infections (ATIs) spread and persist at high prevalence in medium and large primates with moderate transmissibility;, establishment and persistence in small-bodied primates require higher relative rates of transmissibility. Intragroup contact structure – the social network - creates different constraints for different transmission modes, and our model underscores the importance of intragroup contacts on infection prior to intergroup movement in a structured population. When alpha males dominate sexual encounters, the resulting disease transmission dynamics differ from when social interactions are dominated by mother-infant grooming events, for example. This has important repercussions for pathogen spread across populations. Our framework reveals essential social and demographic characteristics of primates that predispose them to different disease risks that will be important for disease management and conservation planning for protected primate populations.     

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or “face touch.” Some mammals have highly organized vibrissae and are able to “whisk” them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non‐primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well‐organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well‐organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and “face touch.” Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Fruits, fingers, and fermentation: the sensory cues available to foraging primates

Survival and reproductive success hinge on the perception ofenvironmental stimuli. In this regard, foraging efficiency dependson discerning predictive signals in food. A widespread occurrenceof ethanol in fruits indicates a sustained historical exposureof frugivores to this compound. Accordingly, Dudley (2000, Quart.Rev. Biol. 75:3–15) proposed that ethanol could representa prominent sensory cue to primates because of direct and indirectlyassociated caloric and physiological rewards. However, littleis known regarding the extent to which ethanol correlates withsuch parameters. This information is essential to estimatingthe importance of detecting and detoxifying ethanol in fruits.Here I present a preliminary analysis of fruits from SoutheastAsia; low levels of ethanol were present in fruits of all developmentalstages (range: 0.005–0.48%). Moreover, ethanol correlatedpositively with concentrations of soluble sugars, suggestingthat it could be a valuable foraging cue. Recent findings onthe sensitivity of primate olfaction and gustation to ethanolare consistent with this notion. However, when primates smellfruits deliberately, it often occurs together with digital and/ordental evaluation of texture. Here I show that softening texturealso characterizes the fruit ripening process, and that coloris of ambiguous importance to primates possessing trichromaticvision. I discuss the relevance of these findings to the originsof primates and the ecology of key sensory systems and deducethat detecting and selecting fruits on the basis of cues otherthan color is a persistent theme in primate evolution. Ethanolhas likely played a significant and underestimated role in theregulation of primate foraging behavior.     

Defining fallback foods and assessing their importance in primate ecology and evolution

Physical anthropologists use the term “fallback foods” to denote resources of relatively poor nutritional quality that become particularly important dietary components during periods when preferred foods are scarce. Fallback foods are becoming increasingly invoked as key selective forces that determine masticatory and digestive anatomy, influence grouping and ranging behavior, and underlie fundamental evolutionary processes such as speciation, extinction, and adaptation. In this article, we provide an overview of the concept of fallback foods by discussing definitions of the term and categorizations of types of fallback foods, and by examining the importance of fallback foods for primate ecology and evolution. We begin by comparing two recently published conceptual frameworks for considering the evolutionary significance of fallback foods and propose a way in which these approaches might be integrated. We then consider a series of questions about the importance of fallback foods for primates, including the extent to which fallback foods should be considered a distinct class of food resources, separate from preferred or commonly eaten foods; the link between life history strategy and fallback foods; if fallback foods always limit primate carrying capacity; and whether particular plant growth forms might play especially important roles as fallback resources for primates. We conclude with a brief consideration of links between fallback foods and primate conservation. Am J Phys Anthropol 140:603–614, 2009. © 2009 Wiley-Liss, Inc.