Encyclopedia of Animal Cognition and Behavior

Living Edition
| Editors: Jennifer Vonk, Todd Shackelford

Primate Sensory Systems

  • Laura M. BoltEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-47829-6_1864-1
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Synonyms

Definition

Primates are mammals with complex and large brains compared to body size and traits including an enhanced sense of touch, increased reliance on vision, and reduced reliance on sense of smell compared to other mammals. Their sensory systems allow them to perceive and interpret the world around them, and include vision (sight), olfaction (smell), gustation (taste), audition (hearing), and tactile systems (touch). Each of these sensory modalities contain adaptations that help primates to survive in a range of habitats including arboreal environments. Through the information provided by their sensory systems, primates can find food, avoid predators, and effectively perceive and interact with other individuals of their species.

Introduction

The primates are an order of eutherian (placental with advanced development before birth) mammals comprised of strepsirhines (suborder Strepsirrhini: lemurs, lorises, galagos, and pottos) and haplorhines (suborder Haplorhini: tarsiers, Old and New World monkeys, apes, and humans). They diverged from other mammals approximately 80–90 million years ago, and today have approximately 504 living species (Estrada et al. 2017). Compared to other mammals, primates are characterized by having larger brains compared to body size, brains with greater complexity, clavicles which allow a broader range of motion, generalized dentition enabling a broader diet, five fingers and toes including opposable thumbs and big toes in many species, power and precision grips, fingerprints, toeprints, and palm prints, nails instead of claws, and forward-facing eyes with binocular vision. These characteristics are thought to be adaptations for arboreal (tree-living) environments, with the earliest primates and many extant primates living primarily in trees (Smith 1924). Many of the traits typifying the primate order reflect differences in sensory adaptations between primates and other mammals. For example, primates have an enhanced sense of touch due to their fingerprints and nails, while their five digits including opposable thumbs and big toes enable them to grip and manipulate objects in the environment with greater strength and precision (Liman 2006). Primates also rely less on olfaction and more on vision than other mammals. Their front-facing eyes with overlapping fields of vision allow them to see and interpret their surroundings reliably in three dimensions (Liman 2006). These visual and tactile adaptations give primates survival advantages, allowing them to interact with their environments in new ways, while their larger and more complex brains help primates process the additional sensory information received more efficiently. Compared to other mammals, primate brains have particularly enlarged occipital and parietal regions, which are linked to their greater reliance on vision and touch (Liman 2006).

Primates are also uniquely social among mammals, with the majority of primate species living in mixed-sex groups that stay together on a year-round basis (Dunbar 2010). In solitary species, primate sensory systems are adapted to help individuals better navigate diverse habitats and access food resources while avoiding predators. In group-living species, the complexity of primate sensory systems may additionally help facilitate ongoing social contact between conspecifics. Primate vision, olfaction, audition, and sense of touch are especially important for social relationships, with information about other group members obtained through the senses. Visual, olfactory, gustatory, auditory, and tactile senses work together in primates to help them perceive their environments more effectively and to communicate with other members of their species. The complexity of primate sensory systems may be understood as a series of adaptations that enhance primate ability to interact with their environments and with conspecifics.

Vision

Primate Stereoscopic Vision

Primates are characterized by their stereoscopic (binocular) vision, with overlapping fields of vision from each forward-facing eye creating a wide visual field of three-dimensional depth perception (Liman 2006). Stereoscopic vision is a sensory trait that has evolved multiple times, in evolutionary lineages as divergent as cephalopods (Class Cephalopoda) and vertebrates (Nityananda and Read 2017). While binocular vision is not unique to primates, having the combination of forward-facing eyes plus stereoscopic vision (stereopsis) is thought to be rare in vertebrates, and is only found in some birds (e.g., birds of prey, Order Accipitriformes), mammalian carnivores (Order Carnivora), and primates (Nityananda and Read 2017). The combination of forward-facing eyes plus stereopsis allows for a larger stereoscopic visual field than found in animals with side-facing eyes (Nityananda and Read 2017). While a wider stereoscopic visual field helps birds of prey and carnivores be more successful in hunting prey, it also leads to enhanced fitness for primates. As arboreal mammals, primates rely on their binocular vision to travel, find food, and evade predators while remaining in the treetops. The arboreal hypothesis suggests that primate traits including improved stereoscopic vision and increased grasping power evolved as adaptations for life in the trees, allowing primates better ability to perceive distance and therefore to travel between branches without falling (Smith 1924). An alternate hypothesis relates to visual predation and suggests that primate traits including improved binocular vision and fine motor skills evolved to facilitate the hunting of insects, which were likely a key food source for early primates (Cartmill 1992). As small-bodied prey that may move quickly in any direction in three-dimensional space, insects would have been difficult to catch without good depth perception (Cartmill 1992). A third hypothesis relates to angiosperm (flowering plant) evolution and suggests that traits like better vision and improved gripping ability of hands and feet are adaptations that allow primates to more successfully feed on fruit at the end of small branches (Sussman 1991). Regardless of the selective pressures that led to the development of a wider stereoscopic visual field and other derived traits in primates, excellent binocular depth perception is a ubiquitous component of visual systems in living primates. Stereoscopic vision helps individuals across species travel efficiently through both arboreal and terrestrial (ground-based) environments, find food, avoid predators, and interact with conspecifics.

Primate Color Vision

Some primates also have color vision. Color vision depends on the ability of retinal photoreceptors (rods and cones) and the brain regions associated with seeing to perceive different wavelengths of light, then to compare them to one another. Retinal rods allow organisms to see their surroundings under low light conditions, such as at night, while cones increase visual perception during brighter conditions, such as during daylight (Bowmaker 1998). Vertebrate eyes have rods and cones with different types of opsin, the photopigment that enables eyes to perceive different types of light wavelength and to see in color. Color vision evolved in fish and reptiles during early vertebrate evolution, but some retinal cones were lost during the evolution of mammals, likely due to the earliest mammals being nocturnal (Bowmaker 1998). As early mammals adapted to using their visual systems primarily at night, their visual acuity in low light levels was enhanced by reducing their color vision to a dichromatic (two light wavelength ranges) system (Liman 2006). This dichromatic system allowed them some color vision but limited their perception to only two light wavelength ranges, short (sensing blue light) and long (sensing red and green light without being able to differentiate between them) (Bowmaker 1998). A dichromatic vision system is still present in most living mammals, but trichromatic (three ranges of light wavelength) color vision evolved again in the primate order. Along with marsupials (Infraclass Marsupialia), primates are the only mammals in which some species possess three types of retinal cone (Bowmaker 1998). Trichromacy enables some primates to perceive three different light wavelength ranges in comparison to one another; in addition to short (sensing blue light) and long (sensing red light) wavelengths, trichromats can also perceive medium (sensing green light) wavelengths (Carvalho et al. 2017). This gives trichromat primates the ability to tell the difference between red and green and therefore to see in full color.

Primates are characterized by this increased ability to see in color compared to other mammals, while still maintaining a wide variation in color perception ability across taxa. Their range of ability to perceive color is thought to be adaptive given the varying light conditions that primates live in, with some primates being nocturnal (active at night), some being diurnal (active during daylight), and some being cathemeral (active across the diel cycle) (Liman 2006). Some extant primates can perceive three different light wavelength ranges (red, green, and blue) and can see in full color (trichromats), others can perceive two different light wavelength ranges (red, plus blue or green) and see in partial color (dichromats), and some can perceive only one light wavelength range (red) and do not see in color (monochromats) (Carvalho et al. 2017). Old World monkeys, apes, and humans (catarrhines, Parvorder Catarrhini), and one genus of New World monkey (platyrrhine, Parvorder Platyrrhini), the howler monkey (Alouatta spp.), are trichromats and consistently able to see in full color (Liman 2006). In most other New World monkeys and some lemur species, females are able to see in full color if they have a specific genetic polymorphism on an X chromosome. However, males and other females in these species lack this gene and are dichromats who cannot differentiate between red and green colors (Liman 2006). Lemur species where females have this trichromat polymorphism include some sifaka and ruffed lemurs (Propithecus spp. and Varecia spp.) and the red-fronted lemur (Eulemur rufifrons), all of which are diurnal or cathemeral (Carvalho et al. 2017). However, most diurnal and cathemeral primate species are consistent dichromats, including nearly all New World monkeys and most lemurs. Monochromat primates can see light, dark, and shades of grey, but no color. Monochromat primates are all nocturnal and include strepsirhines such as lorises and galagos (Lorisidae and Galagidae families), lemurs including fork-marked lemurs (Phaner spp.), fat-tailed dwarf lemurs (Cheirogaleus medius), and hairy-eared dwarf lemurs (Allocebus trichotis), and one genus of New World monkey, the owl monkey (Aotus spp.) (Carvalho et al. 2017).

The differences in both activity patterns and dietary preferences among extant primates may explain the persistence of these differences in color perception. Nocturnal primates who are monochromats may be insectivorous (i.e., eat insects as a primary dietary resource) and better able to detect the movement of insects in a low-light environment due to their lack of color perception (Carvalho et al. 2017). In contrast, primate trichromats who are frugivorous or folivorous (i.e., eat fruit or leaves as a primary dietary resource) may be better able to locate red or yellow fruits or young leaves against a background of green vegetation during daylight (Carvalho et al. 2017). Finally, primate dichromats may have a range of dietary adaptations but be better able to find camouflaged or hidden prey than those with full color vision under certain light conditions (Carvalho et al. 2017).

Other Primate Eye Adaptations

Living primates also show variation in other features associated with visual perception in low- and high-light levels. Like most other vertebrates, nocturnal primates have tapetum lucidum, an eye tissue covering which reflects light backwards through the photoreceptor layer and toward retinal cells, causing reflective eye shine and providing greater visual sensitivity in low-light levels (Ollivier et al. 2004). With the exception of a few diurnal brown and ruffed lemur species (Eulemur and Varecia spp.), living lemurs, lorises, galagos, and pottos have tapetum lucidum. However, all haplorhines lack this structure, despite the tarsiers and one New World monkey genus (owl monkey, Aotus spp.) being nocturnal (Ollivier et al. 2004). In contrast, haplorhine eyes have fovea, which are small pits in the center of the retina that improve central vision and color perception, particularly during daylight. Lemurs and lorises, which are more likely to be active in low light levels, generally lack retinal foveae (Ross 2004).

Olfaction

Although primates are characterized by their increased reliance on vision as a sensory modality compared to other mammals, olfaction is still an important mode of perception, especially for strepsirhines. While primate snout length is reduced and primate faces are flattened compared to other mammals, strepsirhines have longer snouts than haplorhines as well as rhinaria (wet noses), enabling olfactory organs to get better exposure to potential scent compounds in the environment (Epple 1986). Strepsirhine brains also have larger olfactory bulbs than haplorhines, attesting to the greater importance of this sensory system in lemurs, lorises, galagos, and pottos compared to other living primates. Across taxa, primate olfactory ability is characterized by sensitivity, meaning that all primates can detect odorants when at low levels in the environment. Primates are also adept at discriminating between odors, meaning that they can easily tell the difference between different chemical compounds based on scent. In both strepsirhines and haplorhines, smell is enabled by the main and accessory olfactory systems. The main olfactory system allows perception of volatile airborne compounds that might elicit a response from many different animals, such as the esters of ripe fruit. In contrast, the accessory olfactory system perceives more particular nonvolatile compounds emanating from conspecifics, such as pheromones (Liman 2006). The vomeronasal organ (VNO) is the accessory olfactory organ and is located in the nasal septum in vertebrates including some reptiles and mammals including primates. While it is vestigial (nonfunctional) in catarrhines, it is more functional in tarsiers and New World monkeys and is still fully operational and widely used by strepsirhines (Epple 1986).

Primate sense of smell is important for both ecological and social reasons. Across taxa, primates use odor to detect desirable foods (e.g., sugary, fleshy fruit). For example, lemur species including the mouse lemur (Microcebus murinus) and diademed sifaka (Propithecus diadema) and New World monkeys including the white-faced capuchin (Cebus capucinus) and Central American spider monkey (Ateles geoffroyi) use odor to find food items ranging from insects to flowers to ripe fruit for consumption (Nevo and Heymann 2015). Olfaction is also a key component of the social behavior of strepsirhines, tarsiers, and New World monkeys. Urine is used as a type of scent mark in some of these primate groups through urine washing, a behavior where primates direct their urine streams back toward their bodies, then use it to mark substrates like tree branches (Delbarco-Trillo et al. 2011). Urine washing is thought to be especially important in solitary and nocturnal strepsirhines like lorises, galagos, and pottos, while group-living, diurnal lemurs are more dependent on glandular scent secretions (Delbarco-Trillo et al. 2011). Odor is produced by scent glands in various primate body areas, primarily in the genital, sternal, and brachial regions, although scent glands may also be present in palmar, antebrachial, forehead, and chin regions in some species (Epple 1986). Solitary species, like lorises, galagos, pottos, and some lemurs, rub their scent glands on substrates that can retain odor for hours or days, likely lasting until other individuals of the same species pass through the area. These scent marks may signal territory occupancy or sexual receptivity to conspecifics (Delbarco-Trillo et al. 2011). In group-living primate species, scent secretions have myriad social uses. The ring-tailed lemur (Lemur catta), for example, uses scent marks for a range of functions, including indicating territorial boundaries, establishing dominance rank (Kappeler 1998), advertising female estrus, and displaying the quality of potential mating partners (Walker-Bolton and Parga 2017). In New World monkeys such as the moustached tamarin (Saguinus mystax), scent marks are similarly used for identifying social group members and potentially receptive mating partners (Heymann 1998).

Gustation

Primates rely on their sense of taste to help them select nutritious food items and reject harmful substances. Taste bud receptor cells convey information to the brain through gustatory nerves, allowing primates to obtain sensory information about items in their mouths. Through the sensory taste buds, details are provided about the temperature, texture, and composition of potentially edible items. Primates can perceive tastes including sweet, salty, umami (savory), bitter, and sour; they demonstrate general affinities for some tastes (sweet, salty, umami) but aversion for others (bitter, sour) (Liman 2006). Taste preferences show clear fitness benefits, with foods high in nutritive content usually featuring preferred sweet, salty, and/or umami tastes (Liman 2006). Primate avoidance of bitter and sour tastes is adaptive in preventing them from ingesting harmful or poisonous substances, such as spoiled food or plant toxins like tannins and alkaloids (Liman 2006). Across primate taxa, taste receptors show similarities but also some differences, with tasting perceptions more alike in closely related species and less alike in more distantly related groups. For example, Old World monkeys like the olive baboon (Papio anubis) and pigtailed macaque (Macaca nemestrina) showed greater preference for sour tastes than New World monkeys like the common squirrel monkey (Saimiri sciureus) and Central American spider monkey (Ateles geoffroyi) (Laska et al. 2003).

Audition

Primates use hearing to navigate their habitats and to monitor for the presence of predators, prey (e.g., insects), and conspecifics in the area around them. Most natural sounds are made by living organisms as they vocalize or move through their environments, and being able to perceive and interpret these sounds is a key component of primate survival (Heffner 2004). Greater hearing sensitivity is linked to greater social complexity in most mammals, and primates also share this tendency (Ramsier et al. 2012). Similarly to other mammals, all primates have good sound localization ability (i.e., ability to detect where sound is coming from) and can hear low-pitched sounds at and below 125 Hz (Heffner 2004). Although primate species across taxa can generally hear low frequencies, large-bodied primates like Old World monkeys, apes, and humans tend to perceive a range of frequencies (sound pitches) that is lower than smaller primates. Conversely, smaller-bodied primates such as New World monkeys, tarsiers, and strepsirhines have hearing ranges that perceive generally higher pitches, with some even perceiving and making ultrasonic vocal sounds (Ramsier et al. 2012). This correlation between relative body size and auditory frequency hearing range is a general pattern seen throughout mammals (Heffner 2004) and may be optimized for perception of species-specific vocalization frequency ranges as well as for sound localization in very small species. The generally strong ability of primates to localize sound is thought to be adaptive given their forward-facing eyes and narrower range of vision compared to other mammals (Heffner 2004). When they hear an unexpected noise, primates need to know the direction in which to turn their head in order to see what is creating the auditory disturbance and to then make the decision to flee if necessary.

Primate auditory systems are well-adapted to respond to potential threats. In addition to perceiving noises that predators make through movement and vocalization, group-living species have also evolved alarm calls, which are used to alert other group members to the presence of a threat in the area (Ramsier et al. 2012). Many social species across taxa have also evolved referential calls, meaning that vocalizations refer to a specific predator type (i.e., snake or eagle) or a predator’s direction of approach (i.e., terrestrial vs. aerial). Primates ranging from lemurs (e.g., ring-tailed lemur, Lemur catta; Bolt et al. 2015) to New World monkeys (e.g., white-faced capuchin, Cebus capucinus; Digweed et al. 2005) to Old World monkeys (e.g., vervet monkey, Chlorocebus pygerythrus; Seyfarth et al. 1980) are known to have referential predator vocalizations that conspecifics hear and respond to, even when predators are not visible.

All living primates use vocalizations to communicate, including both solitary and group-living species. Vocalizations allow individuals to stay in touch with conspecifics even when out of visual range, such as in dense forest environments. Solitary species generally have smaller vocal repertoires than social species, but both use sound to convey information about the occupancy of an area, likely to prevent competition by spacing out individuals and groups (Ramsier et al. 2012). Group-living species have larger repertoires and greater vocal complexity, mirroring the larger range of ecological and social interactions that they engage in with conspecifics (Ramsier et al. 2012). In addition to predatory threat response, primates may vocalize to avoid separation from social groups, to maintain proximity to preferred companions within groups (e.g., contact calls, Bolt and Tennenhouse 2017), to advertise the location of food resources to other group members (e.g., food calls, Heffner 2004), to defend mates, rich food resources, or territories from other groups (e.g., long calls, Bolt et al. 2019), or to establish dominance ranks and attract mates through honest displays (e.g., advertisement calls, Bolt 2013). This reliance of primate social behavior on sound-based communication has shaped primate auditory systems, ensuring that primates can hear each other in addition to environmental stimuli.

Tactile System

Primates have an enhanced sense of touch and better grip capability compared to other mammals. This impacts their ability to find and ingest food, to make and use tools, to socialize at close range, and to travel, particularly in arboreal environments. In contrast to other mammals, primates have dermatoglyphs (distinctive lines, whorls, and ridges on fingers, toes, and the palms of hands and feet), pentadactyly (five fingers and toes), and nails instead of claws in most species, which work together to give primates greater sensitivity in perceiving the properties of objects and substrates in their environments. Primates also have opposable thumbs, divergent big toes, and power and precision grips, which give them better ability to manipulate their environments through strength and dexterity. Power grips involve simultaneous grasping by the digits and the palm, thus applying force from the whole hand or foot to manipulate objects. In contrast, precision grips involve fine-motor skill interactions with pressure applied by individual digits to a small area, thus manipulating objects with accuracy and control. All primates have robust power grips, while precision grips are better developed in monkeys, apes, and humans than in strepsirhines. The interaction between these two types of grip capability along with primates’ more refined sense of touch enables a broader range of social, locomotory, and foraging behaviors than seen in most other mammals.

Touch is important in primate social behavior, with prolonged tactile contact (e.g., resting while in body contact) and grooming (manipulation of the fur using hands or teeth) being key components in maintaining inter-individual relationships and in reducing individual stress levels (Dunbar 2010). Social grooming (grooming another individual) is important in group-living species, while both group-living and solitary species engage in self-grooming. In monkeys, apes, and humans, greater manual dexterity has led to more grooming using the hands, while strepsirhines use toothcombs (dental structures with outward-facing front teeth) to groom themselves and others (Dunbar 2010).

Their ability to touch and grip enables primates to travel effectively through arboreal environments; for example, by using branches and vines as supports, by leaping between trees, and by balancing at the ends of small branches without falling to the ground (Smith 1924; Sussman 1991). The fingers, toes, and palms of their hands and feet are hairless with textured skin ridges and whorls (dermatoglyphs) to increase friction and gripping power during movement between substrates. Some New World monkeys have additionally evolved prehensile tails, which are arboreal adaptations for dense forest environments. These are also seen in some other mammals, particularly those endemic to South America (e.g., opposums, Order Didelphimorphia and anteaters, Suborder Vermilingua). Prehensile tails act as extra limbs, providing further gripping power for arboreal monkeys and increasing their ability to locate and harvest food while suspended in the trees.

Increased sensitivity, dexterity, and strength in hands and feet also mean that primates should be able to make and use more sophisticated tools than other animal species, and tool use is present in living primates ranging from some strepsirhines (e.g., brown lemurs, Eulemur spp.) to New World monkeys (e.g., capuchins, Cebus spp.) to catarrhines (e.g., macaques, Macaca spp.; baboons, Papio spp.; great apes, Gorilla spp., Pongo spp., and Pan spp.; Bentley-Condit and Smith 2010). Among other functions, primates use tools to acquire hidden or inaccessible food sources. For example, primates employ hammers and anvils to crack open nuts (e.g., common chimpanzees, Pan troglodytes; capuchin monkeys, Cebus spp.; macaques, Macaca spp.; Bentley-Condit and Smith 2010). They also utilize modified sticks to harvest termites, ants, or bees from inside mounds (e.g., common chimpanzees, Pan troglodytes; Sumatran orangutans, Pongo abelii; Bentley-Condit and Smith 2010). Primates may also use their hands and feet to harvest foods like insects or small vertebrates that are hidden in tree holes, palm fronds, or under bark. These uses of tools and digits substantially improve primate extractive foraging ability, thus increasing the range of ecological niches that primates can inhabit and demonstrating the strong adaptive function of the enhanced primate tactile system.

Conclusion

Primates rely on their sensory systems for both environmental and social reasons; they use their senses to perceive food, predators, and their habitats, and to interact with conspecifics. Their large and complex brains with highly developed sensory abilities give them adaptive advantages, with a reduced sense of smell and enhanced vision and touch compared to other mammals allowing them to occupy new roles in their environments. The sophistication of primate sensory systems is foundational to the behavioral and ecological intelligence of this mammalian order.

Cross-References

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Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of WaterlooWaterlooCanada

Section editors and affiliations

  • Ivo Jacobs
    • 1
  1. 1.Department of Cognitive ScienceLund UniversityLundSweden