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.     

Evolution of the nose and nasal skeleton in primates

One traditional diagnostic feature of the Order Primates is a decreased emphasis on olfaction. 1 , 2 Some authors attribute this feature only to tarsiers and anthropoids, either through convergence or as a common feature of haplorhines. 2 - 4 Other authors de‐emphasize olfaction relative to vision, 5 - 7 which does not necessarily denote olfactory reduction per se. There are lengthy roots to this discussion. The importance of the sense of smell to at least some primates, humans in particular, has long been viewed as secondary to the importance of visual, auditory, and tactile senses. Smell, or olfaction, is viewed as the primitive special sense, the stimuli perceived in an unconscious manner, submerged relative to higher neural functions, 1 and a sense that has been increasingly reduced during the course of primate evolution. 1 - 8 Anatomical structures related to olfaction differ profoundly in proportions and complexity between higher taxonomic groups of primates (Haplorhini, Strepsirrhini). These anatomical differences are beyond dispute (Box 1). However, the relationship between the anatomical differences and primate sensory abilities, and hence the validity of using them to group primates into “microsmatic” or “macrosmatic” categories, 9 , 10 is less clear when we examine the physiological and genetic data on primate olfaction.     

Olfaction and Taste: Invasive Odours and Disappearing Objects

The metaphorisation of sight and hearing, the objective senses, dominate the founding ideas, or philosophemes, of Western philosophy. The senses of taste and smell are of little relevance in the formation of conceptual knowledge or in classificatory systems; they are, by virtue of their dissolving objects, incapable of giving objective knowledge in Western metaphysics. Derrida and Ulmer developed a metaphorology that exploits the chemical basis of the subjective senses of taste and smell. The anthropology of the senses takes this questioning of metaphysics into issues of how olfaction and taste function in sociality. In the routine practices of everyday life, is olfaction able to create the sense of community that it does in rituals? Or, has the repression of smell in humanity's evolution towards ‘civilisation’ muted the connective ability of multiple odour particles? In a culture and metaphysics that presumes the separability of the self from the other and the self from the object, is there a place for senses that make a nonsense of separation and objectivity through their state of meaningful dissolution? Through philosophy's metaphorisation, has taste been stripped of its sensuousness and made a sense for aesthetics and not flavours and textures? In a metaphorics premised in judgement and discernment, can taste be a sense that founds sociality? In blurring the boundaries between self and other that are necessary to form and maintain the distinction, the dissolvability of smell and taste makes another metaphorics and other socialities possible. Of all the senses, that of smell—which is attracted without objectifying—bears clearest witness to the urge to lose oneself in and become the ‘other’. As perception and the perceived—both are united—smell is more expressive than the other senses (Horkheimer and Adorno 1979:184).     

鸟类社会行为中的嗅觉通讯研究进展

长期以来, 学者普遍认为大多数鸟类的嗅觉能力较弱或丧失。早期实验未能得到统一而清晰的结果, 进一步扩大了这一认知误区。随着研究手段和技术的发展, 解剖学、电生理学、分子生物学和行为生态学等学科提供了鸟类嗅觉存在的证据。目前, 相关研究在鸟类14目33科中发现了嗅觉通讯的证据。与视觉和听觉一样, 这一感觉通路可能在鸟类的觅食、导航、防御、隐蔽、警戒和交流等社会行为中发挥着重要作用。本文着重于嗅觉通讯在鸟类社会行为中的功能, 通过回顾近十年的相关研究, 综述鸟类嗅觉在物种和个体识别、繁殖行为、亲缘识别、配偶选择与竞争等方面发挥的作用。我们也指出: 研究手段的创新将揭示更多鸟类物种在社会行为中对于嗅觉通讯的运用。此外, 当前研究多聚焦于少数物种和单一层面(如生理、生态和环境等), 使用分子生物学、解剖与生理学、行为学和神经生物学手段的整合研究较为缺乏; 而后者更有可能全面地揭示鸟类嗅觉通讯的复杂机理及其在社会行为中发挥的多种功能。     

A Preliminary Investigation of Parent–Progeny Olfactory Recognition and Parental Investment

The role of olfaction in kin recognition and parental investment is documented in many mammalian/vertebrate species. Research on humans, however, has only focused on whether parents are able to recognize their children by smell, not whether humans use these cues for investment decisions. Here we show that fathers exhibit more affection and attachment and fewer ignoring behaviors toward children whose smell they can identify than toward those whose smell they cannot recognize. Thus, olfaction might serve as a means for males to determine their genetic relatedness to purported offspring. We also demonstrate that mothers’ olfactory recognition and hedonistic ratings are linked with the use of physical punishment. Mothers report using more punishment with children whose odor they cannot recognize and less with children whose odor they rated as more pleasant. These results provide the first preliminary evidence in humans that olfactory cues may guide parents in the allocation of care.     

Human olfactory neurons respond to odor stimuli with an increase in cytoplasmic Ca2+.

The sense of smell allows terrestrial animals to collect information about the chemical nature of their environment through the detection of airborne molecules. In humans smell is believed to play an important role in protecting the organism from environmental hazards such as fire, gas leaks and spoiled food, in determining the flavor of foods, and perhaps in infant-parent bonding. In addition, the study of human olfaction is relevant to a number of medical problems that result in olfactory dysfunction, which can affect nutritional state, and to the study of the etiology of neurodegenerative diseases which manifest themselves in the olfactory epithelium. Although much is known about behavioral aspects of human olfaction, little is understood about the underlying cellular mechanisms in humans. Here we report that viable human olfactory neurons (HON) can be isolated from olfactory tissue biopsies, and we find that HON respond to odorants with an increase in intracellular calcium concentration ([Cai]).     

The perfume of reproduction in birds: Chemosignaling in avian social life

This article is part of a Special Issue “Chemosignals and Reproduction”.Chemical cues were probably the first cues ever used to communicate and are still ubiquitous among living organisms. Birds have long been considered an exception: it was believed that birds were anosmic and relied on their acute visual and acoustic capabilities. Birds are however excellent smellers and use odors in various contexts including food searching, orientation, and also breeding. Successful reproduction in most vertebrates involves the exchange of complex social signals between partners. The first evidence for a role of olfaction in reproductive contexts in birds only dates back to the seventies, when ducks were shown to require a functional sense of smell to express normal sexual behaviors. Nowadays, even if the interest for olfaction in birds has largely increased, the role that bodily odors play in reproduction still remains largely understudied. The few available studies suggest that olfaction is involved in many reproductive stages. Odors have been shown to influence the choice and synchronization of partners, the choice of nest-building material or the care for the eggs and offspring. How this chemical information is translated at the physiological level mostly remains to be described, although available evidence suggests that, as in mammals, key reproductive brain areas like the medial preoptic nucleus are activated by relevant olfactory signals. Olfaction in birds receives increasing attention and novel findings are continuously published, but many exciting discoveries are still ahead of us, and could make birds one of the animal classes with the largest panel of developed senses ever described.     

Pheromones in birds: myth or reality?

Birds are anosmic or at best microsmatic… This misbelief persisted until very recently and has strongly influenced the outcome of communication studies in birds, with olfaction remaining neglected as compared to acoustic and visual channels. However, there is now clear empirical evidence showing that olfaction is perfectly functional in birds and birds use olfactory information in a variety of ethological contexts. Although the existence of pheromones has never been formally demonstrated in this vertebrate class, different groups of birds, such as petrels, auklets and ducks have been shown to produce specific scents that could play a significant role in within-species social interactions. Behavioral experiments have indeed demonstrated that these odors influence the behavior of conspecifics. Additionally, in quail, deprivation of olfactory inputs decreases neuronal activation induced by sexual interactions with a female. It seems therefore well established that birds enjoy a functional sense of smell and a fast growing body of experimental evidence suggests that they use this channel of olfactory communication to control their social life. The unequivocal identification of an avian pheromone is, however, still ahead of us but there are now many exciting opportunities to unravel the behavioral and physiological particularities of chemical communication in birds.     

Better smelling through genetics: mammalian odor perception

The increasing availability of genomic and genetic tools to study olfaction-the sense of smell-has brought important new insights into how this chemosensory modality functions in different species. Newly sequenced mammalian genomes-from platypus to dog-have made it possible to infer how smell has evolved to suit the needs of a given species and how variation within a species may affect individual olfactory perception. This review will focus on recent advances in the genetics and genomics of mammalian smell, with a primary focus on rodents and humans.     

Physical contact while handling is not necessary to reduce fearfulness in the rabbit

Rabbits handled around nursing time during the first week after birth show reduced fear response toward humans. Our earlier attempt to reduce the duration of daily treatment necessary to achieve this effect showed that even a minimal human contact, characteristic of animal caretaking in intensive rabbitries, results in reduced fearfulness. Being descendants of a nocturnal mammal species, olfactory cues are of central importance in rabbits, especially just after parturition, when the other sensory organs are undeveloped. In the present experiment, we investigated whether exposing newborn rabbit pups to human smell at nursing time is sufficient to reduce fear of humans in rabbits. For this, we exposed rabbit pups to one of the following handling treatments in the first week of life: (1) full handling, within 0.5 h after nursing, which consisted of removing the pups from the nest and weighing them (about 5 min/litter), (2) exposing rabbit pups to the smell of humans for about 5 min/litter, without touching them, (3) untreated controls. At 28 days of age, the timidity of the pups was measured in a 5 min approach test. Pups that were either handled or exposed to human smell appeared to be equally less fearful as they approached the experimenter's hand with a lower latency and more frequently than untreated controls. This indicates that olfactory exposure during handling results in imprinting even without a human contact in rabbits.     

Different odor tests contribute differently to the evaluation of olfactory loss

In a clinical context, the importance of the sense of smell has increasingly been recognized, for example, in terms of the evaluation of neurodegenerative disorders. In this study, 2 strategies of olfactory testing, a simple one and a more complex one, were compared with respect to their suitability to assess olfactory dysfunction. Odor threshold (T), discrimination (D), and identification (I) were assessed in a control sample of 916 males and 1160 females, aged 6-90 years, and in 81 men and 21 women, aged 38-80 years, suffering from idiopathic Parkinson's disease (IPD). Sums of the 3 subtest results T, D, and I yielded threshold discrimination identification (TDI) scores reflecting olfactory function. Sensitivity of any of the 3 subtests to confirm the diagnosis established by the composite TDI score was assessed separately for each test. Principal component analyses were applied to determine any common source of variance among the 3 specific subtests. Sensitivities of the subtests to provide the diagnosis established by the composite TDI score were 64% (T), 56% (D), and 47% (I), respectively. In IPD patients, each of the subtests provided the correct diagnosis (sensitivity >90%), as olfaction was impaired in 99% of the patient group. Two principal components emerged in both controls and IPD patients, with eigenvalues >0.5. The first component received high loadings from all factors. The second component received high loadings from odor threshold, whereas loadings from odor discrimination and identification were much smaller. In conclusion, combined testing of several components of olfaction, especially including assessment of thresholds, provides the most significant approach to the diagnosis of smell loss.     

Bacterial olfaction

Sensing their environment is a crucial ability of all life forms. In higher eukaryotes the sensing of airborne volatile compounds, or olfaction, is well developed. In plants, slime moulds and yeast there is also compelling evidence that these organisms can smell their environment and respond accordingly. Here we show that bacteria are also capable of olfaction. Bacillus licheniformis was able to sense airborne volatile metabolites produced by neighbouring bacterial cultures and cells could respond to this chemical information in a coordinated way. When Bacillus licheniformis was grown in a microtitre plate adjacent to a bacterial culture of the same or a different species, growing in complex medium, biofilm formation and pigment production were elicited by volatile molecules. A weaker response occurred in increasingly distant wells. The emitted volatile molecule was identified as ammonia. These data demonstrate that B. licheniformis has evolved the ability collect information about its environment from the surrounding air and physiologically respond to it in a manner similar to olfaction. This is the first time that a behavioural response triggered by odorant molecules received through the gas phase is described in bacteria.     

Evolutionary changes of the importance of olfaction in cetaceans based on the olfactory marker protein gene

Odontocetes and mysticetes are two extant suborders of cetaceans. It is reported that the former have no sense of olfaction, while the latter can smell in air. To explain the ecological reason why mysticetes still retain their sense of smell, two hypotheses have been proposed — the echolocation-priority hypothesis, which assumes that the acquisition of echolocation causes the reduction of the importance of olfaction, and the filter-feeder hypothesis, which assumes that olfactory ability is important for filter-feeders to locate their prey because clouds of plankton give off a peculiar odor. The olfactory marker protein (OMP) is almost exclusively expressed in vertebrate olfactory receptor neurons, and is considered to play important roles in olfactory systems. In this study, full-length open reading frames of OMP genes were identified in 6 cetacean species and we analyzed the nonsynonymous to synonymous substitution rate ratio based on the maximum likelihood method. The evolutionary changes of the selective pressures on OMP genes did fit better to the filter-feeder hypothesis than to the echolocation-priority hypothesis. In addition, no pseudogenization mutations are found in all five odontocetes OMP genes investigated in this study. It may suggest that OMP retains some function even in ‘anosmic’ odontocetes.     

Attitudes toward Olfaction: A Cross-regional Study

This study aimed to determine whether there are regional influences on attitudes toward olfaction. A total of 1082 participants aged 21-50 years from 4 different regions (Mexican, Korean, Czech, and German) were asked to rate general attitudes toward olfaction in everyday life. To examine affective attitudes to odors (i.e., pleasantness), participants were also asked to list 3 odors as being the most pleasant or unpleasant, respectively. Next, the mentioned odor names were attributed to 1 of 4 main categories: "Food & Drink," "Social relationship," "Nature," and "Civilization" and the distribution of these categories was compared across regions. Mexicans were significantly different to the other regions in their general attitudes toward olfaction. In addition, in all regions, in comparison with men, women indicated a higher interest in the sense of smell. Moreover, a significant positive correlation was present between individuals' self-rating of olfactory sensitivity and general attitudes toward olfaction. Finally, there were significant cross-regional differences in affective attitudes toward specific categories of odors. In conclusion, our findings support and extend the notion that regions affect attitudes toward the olfactory world.     

Antibacterial essential oils in malodorous cancer patients: clinical observations in 30 patients.

Malodorous necrotic ulcers in cancer patients are of major concern as it leads to social isolation and poor quality of life. Current medications and topical therapies have proven inadequate in their ability to reduce foul smell to acceptable levels. We report the positive experience we have had in using antibacterial essential oils in patients with incurable head and neck cancer and associated malodorous necrotic ulcers. All patients received a standard course of therapy with oral or systemic antibiosis. In addition, we rinsed the ulcers with an antibacterial essential oil mix (mainly based on Eucalyptus oil) twice a day. All patients experienced complete resolution of the foul smell by only the third or fourth day of therapy. As a secondary effect we saw that besides smell reduction the oils had anti-inflammatory effects on neoplastic ulcers. In some patients ulcers started to heal and achieved complete re-epithiliazation. The patients experienced great personal relief upon resolution of their malodorous conditions. Quality of life improved significantly with the resulting reintroduction of social contact with friends and relatives.     

Imaging of brain activation by odorants in humans

Application of positron emission tomography and magnetic resonance imaging has provided several new insights into various olfactory functions. One is that sniffing and smelling engage separate subsystems in the human olfactory cortex. Another is that perception of odorous compounds (odorants) is mediated by a set of core regions, which are partly different for pure olfactory than for olfactory plus trigeminal odorants. Depending on the task associated with odor perception, the core regions are recruited together with other circuits, in a parallel and hierarchical manner. The sense of smell seems, therefore, to be organized similarly to other sensory modalities, and the specific psychophysical characteristics of olfaction should be attributed to an early involvement of the limbic system rather than to a conceptually different mode of processing.     

A Comparison of the Sensory Development of Wolves (Canis lupus lupus) and Dogs (Canis lupus familiaris)

Little is known about the development of the sensory systems of wolves. The timing of sensory development in wolves is usually extrapolated from studies on dogs, since they are members of the same species. However, early developmental differences between these two subspecies have already been identified. For example, wolves tend to approach and investigate objects in their environment 2 wk before dogs. These changes in developmental timing may play an important role in the behavioral differences between adult wolves and dogs. The purpose of this study is to compare the development of the sensory systems in wolves and dogs. Responses of seven wolf pups and 43 dog pups to familiar and novel olfactory, auditory, and visual stimuli were tested weekly from 2–7 wk of age. Eleven wolf pups were also observed for orientation towards auditory and visual stimuli during 2‐h sessions, 5 d a week, from 2–8 wk of age. These observations were supplemented by the daily records of caretakers. The results suggest that wolves and dogs both develop olfaction by 2 wk, audition by 4 wk, and vision by 6 wk on average, despite the 2‐wk shift in their ability to explore. This means that when wolves begin to explore at 2 wk, they are blind and deaf, and must rely primarily on their sense of smell. Thus, there is a significant alteration of how these subspecies experience their environment during the critical period of socialization. These findings lead to an alternative explanation for the difference in dogs' and wolves' abilities to form interspecies social attachments, such as those with humans.     

Scenting a Subject: Odour Poetics and the Politics of Space

Olfactory studies are truly multidisciplinary, from anthropology to zoology. What literary criticism can offer is analysis of the language of smell and the discourses of olfactory practice which give smell meanings. In this paper I explore the poetics of odour in selected contexts in the developed West of the twenty-first century. I argue that the language of smell is elusive, contradictory, disguised: nonetheless, it deploys metaphor, story, personal meaning and social meaning, all frames that ‘nest’ together. I demonstrate contradictions of olfactory practice with reference to urban space and technologies of scent, acting on bodies and places. I argue that a relationship between scent, identity and space can be understood in terms of an olfactory sublime, to which there is also resistance, sanctioned by new laws. In public space, the complexity of deodorisation appears in the conflict between fragrance-free and compulsory olfaction, as I argue with reference to Halifax, Nova Scotia and to the London Underground.     

Olfaction and brain size in the bowhead whale (Balaena mysticetus)

Although there are several isolated references to the olfactory anatomy of mysticetes, it is usually thought that olfaction is rudimentary in this group. We investigated the olfactory anatomy of bowhead whales and found that these whales have a cribriform plate and small, but histologically complex olfactory bulb. The olfactory bulb makes up approximately 0.13% of brain weight, unlike odontocetes where this structure is absent. We also determined that 51% of olfactory receptor genes were intact, unlike odontocetes, where this number is less than 25%. This suggests that bowheads have a sense of smell, and we speculate that they may use this to find aggregations of krill on which they feed.