Bear Sensory Systems
Bears evolved and diverged beginning in the late Oligocene and early Miocene, about 20–25 million years ago, attaining a wide geographical distribution range. The family Ursidae includes eight extant species, generally classified into three subfamilies: Ailuropodinae (giant panda Ailuropoda melanoleuca), Tremarctinae (Andean bear Tremarctos ornatus), and Ursinae (Malayan or sun bear Helarctos malayanus, sloth bear Melursus ursinus, American black bear Ursus americanus, brown bear Ursus arctos, polar bear Ursus maritimus, and Asiatic black bear Ursus thibetanus). Morphologically and taxonomically, they possess all the traits of carnivores but, with the exception of the polar bear, have diets often comprised primarily of plant matter. Most of the current bear species evolved with a generalist omnivore strategy, which allows them to occupy a broad array of habitats (Robbins et al. 2004).
Diverse habitats and their physical characteristics create challenges that influenced the evolution of sensory structures in bears. Bears must detect meaningful cues and signals through complex and challenging environments. An extreme example of this is the semiaquatic habitat that creates a unique sensory challenges for polar bear, a terrestrial mammal living as a marine mammal, which is not aquatic in the sense of navigating or hunting underwater like pinnipeds yet must still sense and interpret stimuli in both water and on land (Togunov et al. 2017; Lone et al. 2018). Additionally, bears are solitary and non-territorial, and as such, they benefit from conveying multimodal cues to expedite the breeding season, to recognize family and kin, and to avoid conspecifics. Available anatomical, histological, and behavioral evidence suggests that bears are somatosensory specialists, with an excellent olfaction (Togunov et al. 2017), color vision (Bacon and Burghardt 1976), good hearing (Nachtigall et al. 2007; Owen and Bowles 2011), and sense of taste accommodated by gustatory papillae of both herbivorous and carnivorous characteristics (Pastor et al. 2008; Pastor et al. 2011). Bears also possess neuroanatomical correlates for the sensations received by their extremities (e.g., Kamiya and Pirlot 1988). They have been shown to rely mostly on olfaction, audition, and vision, although the significance and relative quality of some modalities remains to be investigated. Along with these commonly recognized senses, bears may also receive and respond to one other type of sensory information: magnetic fields. Evidence suggests that at least two terrestrial carnivores may respond to magnetic fields, and the retinas of bears contain a light-sensitive pigment that may react to magnetic fields (Nießner et al. 2016). However, although some individual bears can navigate without using familiar physical landmarks, the ability of bears to detect magnetic fields has not been tested.
Visual Perception (Vision)
Overall, the eyes of bears are broadly similar to that of most mammals. As in all mammals, the retinas of bears’ eyes contain two general types of receptive cells: rods and cones. Rods are more sensitive to light than cones, which require strong light stimuli. Rods are used to perceive movement, while cones permit the perception of color. Humans and some but not all primates are trichromatic. That is, they possess three kinds of cone cells. It’s been suggested that this type of color vision has evolved to help some primates find fruits. However, although several bear species forage heavily on fruits at least seasonally, no bears possess trichromatic vision: bears do not see color as we do (Peichl 2005).
New research methods have recently revealed more diversity in mammalian photoreceptors than was previously known. Genotyping the areas responsible for the five vertebrate photoreceptor opsins (proteins) has revealed two cone types in the retinas of most diurnal mammals, including bears, making them dichromatic. The relative abundance of the two cone types in bears has not been evaluated, but those two types of cones should permit discrimination of short wavelength hues (violet, blue) from long wavelength hues (green, yellow, orange, red), but not between different long wavelength hues (Peichl 2005). The visual conditions under which polar bears live are unique among bears: the polar bear’s snow- and ice-covered habitat has little variation in color, but great variation in illumination depending on weather and season. In addition, polar bears are semiaquatic, and light travels through water differently than through air. Given these environmental factors, polar bears might be expected to have reduced color vision, or to lack color vision altogether, as do many marine mammals (Peichl 2005), including their most common prey (Levenson et al. 2006). However, behavioral testing of polar bears and analyses of their DNA indicate that their color vision is similar to that of other terrestrial dichromats, with peak responsiveness to both violet-blue and green (Levenson et al. 2006). There has been little other behavioral testing of bears’ ability to discriminate among colors, but giant pandas discriminate green, red, and blue from gray (Kelling et al. 2006), and American black bears discriminate blue and green from gray (Bacon and Burghardt 1976). It is believed the remaining bears have similar abilities.
The broad pattern in mammals is for vision to evolve in ways that enable the mammal’s ecological niche (Peichl 2005). It’s believed that bears use their visual abilities primarily in foraging and in communication with other bears. Due to the orientation of their eyes, bears have binocular vision, which narrows their field of view but enhances their depth perception. Like other carnivores and many other placental mammals, the eyes of bears contain a reflective layer, the tapetum lucidum, which improves their ability to see under low conditions. In the wild, several if not all bear species display shifts in activity patterns that reveal their ability to use either brightly lit or poorly lit conditions to optimize their foraging success or avoid other individuals of the same species or potentially hazardous individuals from another species, including humans. Bears are often active primarily during the day (diurnal) when humans are not present, and at least two species, the Andean bear and the sun bear, are quite arboreal, but unlike other some other diurnal arboreal mammals (e.g., tree squirrels), their retinas are not cone-heavy. Thus, a bear’s eye functions well at low light levels but without high spatial and temporal acuity.
Auditory Perception (Hearing)
Bears have well-developed external ears with moderately stiff pinnal flanges and are assumed to have good hearing across species. American black and brown bears appear to use auditory cues in salmon streams (Klinka and Reimchen 2002). Polar bears can hear well in air the relatively low frequencies of vocalization produced by seals, their prey (Owen et al. 2016). The behaviors used by bears to locate sound are described as erecting the ears while lifting the head, then visual scanning to follow the source of sound, and sniffing if the sound is of other animals, especially potential prey (Nachtigall et al. 2007).
The anatomy of the auditory region provides important insights about the hearing capacity. Anatomical descriptions of the auditory region exist for some among extant ursid species (giant panda, Andean bear, sloth bear, American black bear, polar bear, and brown bear; Segall 1943), as well as for some extinct bears. Until now, the polar bear and giant panda remain the most studied bear species in terms of auditory perception, investigated using evoked potentials or behaviorally (go, no-go response protocols). The size of the mammalian hearing apparatus increases throughout the class Mammalia in modest proportions with increasing body size. The middle ear ossicles have to withstand the forces produced by the tympanic membrane vibrations. Thus a large mammal with a large tympanic membrane, such as a polar bear, needs massive middle ear ossicles, which in turn results in a decreased capability for the transmission of high-frequency sounds. Therefore, considering their size, polar bears were expected to have moderately good low-frequency hearing; Owen and Bowles (2011) showed in-air best hearing sensitivity between 8 and 14 kHz and its upper limit to be 10–20 kHz lower than that of the small terrestrial carnivores. A decline in functional hearing in polar bears was observed at 125 kHz. Earlier work by Nachtigall et al. (2007) noted good hearing sensitivity of polar bears within a range of 11.2–22.5 kHz: absolute thresholds lower than 27–30·dB. The frequency range of the polar bear’s hearing is wider than in humans, and they can hear well the relatively low frequencies of vocalization produced by seals, in air. Polar bears’ auditory adaptation for underwater hearing remains unknown. Giant pandas have functional hearing into the ultrasonic range, with best sensitivity at 12.5–14.0 kHz and the lower and upper limits at 0.10 and 70 kHz, respectively (Owen et al. 2016). Compared with the polar bear, the giant panda’s hearing is similar, although more sensitive at and above the frequency of 16 kHz. Interestingly, the sensitivity of panda hearing is lower within the range of cub vocalizations, making cubs potentially vulnerable to dampening and fitness-reducing effects of anthropogenic ambient noise. An awareness of the studies species’ acute and relatively wide-frequency hearing, and vulnerability for acoustic signals to be masked by anthropogenic noise during sensitive life stages, should be applied in anthropogenic noise management, as noise may impact bears. In the light of the deleterious potential of noise, additional research on the high-frequency hearing of all bears is needed.
Vocalizations in Bears
The ability of bears to produce sound is strengthened by the presence of epipharyngeal pouches, which are constant and unique features throughout the family Ursidae. The histological structure of the pouches strongly suggests its functional involvement in the respiratory system. Additionally, they can enlarge and retract in response to various states of air inflation, apparently important in ursid phonation (Weissengruber et al. 2001). Bears vocalize during agonistic interactions with conspecifics, for example, to both defend young and secure resources. The agonistic vocalizations include “huffing” (loud deep breathing), “snorting” (loud expelling air through mouth and nostrils), “gurgling” (low-pitched warbling, throaty rumble), and “loud growling.” There have also been other close range vocalizations (e.g., “chuffing”) described for some of the bear species, with suggested but untested functions of appeasement, reassurance, greeting, coaxing, and maintaining contact at close range, most frequently used by females with cubs, by males and females during courtship and mating, and by adults and juveniles during friendly close contacts. Giant pandas will also “bleat” and Andean bears will also “trill,” but other bear species appear not to use these vocalizations. “Humming” has been observed in all bears but the giant panda, sometimes by adult bears but largely restricted to cubs (Baotic et al. 2013; Peters et al. 2007). Cub vocalizations are mainly restricted to nursing and grooming contexts and consist of calls such as “chuffs,” “croaks,” “growls,” “grunts,” and “huffs,” as well as “barks,” “cries,” “screams,” “squalls,” “squawks,” “squeals,” “whimpers,” “woofs,” and “yelps” emitted in distress situations, and “humming” to communicate well-being to the mother.
While relatively little is known about the importance of auditory cues in bear foraging or risk avoidance, compared with other modalities used, vocalizations and their role in intraspecific communication have been thoroughly researched in some bear species. The giant panda is the most studied species in those aspects, with quantitative descriptions of the acoustic structure of male and female bleats showing that they code for sex, age, and size that is important to receivers in reproductive contexts. Individuals perceive and attend to this information when assessing potential rivals and/or mates. Male and female giant pandas can then adjust their behavioral responses according to the age- and size-related information broadcasted by bleats (Charlton et al. 2012). Several previous studies have provided verbal descriptions of other bear vocalizations, but quantitative descriptions, based on the analysis of acoustic properties, are relatively rare (Pokrovskaya 2013; Baotic et al. 2013).
Olfactory Perception (Olfaction)
Adult bears are solitary, which is associated with a greater reliance on olfaction for communication. Although behavioral data suggests that bears use olfaction in foraging, such data also suggests that the most important use of olfaction by bears is in communication with other bears. Olfaction has been most thoroughly studied in the brown bear, polar bear, and giant panda, but indirect behavioral evidence on olfaction has been collected in all bears.
Research on the morphology of olfaction assumes that the relative surface area or size of a physical structure is correlated with the importance of that structure. The nasal cavity of bears, like other mammals, includes a maze of thin bones covered by a thin layer of skin with numerous chemical receptors. These receptors convert airborne molecules into electric impulses that are transmitted to and processed by the bear’s brain. The predatory polar bear has a relatively large portion of its nasal cavity devoted to olfaction, compared to the American black bear, brown bear, and other more omnivorous carnivores. In bears, the relative size of the olfactory bulb, the brain area focused on olfaction, is larger than expected based on the trend seen in other carnivore species (Gittleman 1991), and the size of the bony plate dividing the nasal cavity from the olfactory bulb is larger than would be expected in the American black bear, the brown bear, and especially the polar bear (Bird et al. 2014). Thus, bears appear to rely more on olfaction than do most other carnivores. Airborne compounds stimulate nerve impulses not only in the nasal cavity but also in the vomeronasal organ (VNO), which humans do not possess. The VNO is located on the roof of the oral cavity, and in many mammals, it is important for the reception and processing of compounds involved in intraspecies communication. Only a little research has been done on the morphology and function of the VNO in bears, but the VNO of brown bears and Asiatic black bears is well developed and similar to that of doglike carnivores, except that some gland cells are perhaps uniquely developed in bears.
Olfaction requires the conversion of airborne molecules into nervous impulses. Little is known of this process in most bears, but various proteins which bind airborne molecules are distributed differently in the nasal cavity and in the VNO of brown bears than they are in other mammals. The other limited information available suggests that the molecular mechanisms of olfaction in bears are tuned to compounds linked to foraging and to communication among individual bears.
Bears commonly receive olfactory information from other bears through sniffing, in which airborne molecules are brought into the nasal cavity. Individual bears are known to sniff others’ feces, urine, deposits on marked trees, and footprints. This behavior has been reported by male and female bears of all ages, but it is most often reported from adult males, especially during the mating season (Clapham et al. 2014). Another behavior, called flehmen, brings airborne molecules into contact with the VNO. Flehmen involves raising the upper lip, closing the nostrils, and inhaling through the open mouth. Flehmen has been reported in all bears but sloth bears, which presumably perform it; flehmen is almost always performed by male bears, not females.
Bears use various diverse and complex behaviors to release compounds with olfactory information. These behaviors vary across species with individual age, sex, reproductive status, and perhaps dominance status and population density. Individual bears of several species are known to claw, bite, or rub their chest, neck, shoulders, head, back, or flanks on woody vegetation or surrogates that humans place in bear habitat (e.g., wooden power poles). In addition, American black bears, Andean bears, brown bears, and sloth bears are now known or strongly suspected to actively deposit molecules with their feet in a behavior called pede marking (Owen et al. 2014; Sergiel et al. 2017). Giant pandas may also deposit scents with their feet, but individual pandas more obviously communicate with others by depositing anogenital secretions as high as possible against vertical substrates by performing a handstand.
Giant pandas possess a well-developed anogenital gland which produces unique secretions, while other bears release secretions from less well-developed anogenital sacs (Rosell et al. 2010). The skin of the footpads and between the toes of brown bears and polar bears contains prominent glandular cells (Owen et al. 2014; Sergiel et al. 2017). Glandular cells on the backs of adult male brown bears produce an oily substance only just before and during the breeding season. It is unknown whether this is so in other bears.
Brown bear feet produce compounds that could differentiate males from females (Sergiel et al. 2017). Scents produced by giant pandas may vary among males and females and in various ways between the breeding and non-breeding season (Wilson et al. 2019). Variation of scents in giant panda urine and anogenital secretions may contain information about the sex, age, reproductive status, and perhaps even individual identity of the panda producing the odors (Zhou et al. 2019). Similarly, anogenital secretions of brown bears contain enough variation to differentiate males from females (Rosell et al. 2010). The urine of female brown bears and female Andean bears releases airborne compounds that vary seasonally with levels of reproductive hormones.
Knowledge of what bears perceive through olfaction is incomplete. Giant pandas of both sexes and all ages can discriminate conspecific sex via the scent of urine (White et al. 2004). Similarly, subadult brown bears appear to differentiate between anogenital secretions of adult male and adult female brown bears (Jojola et al. 2012). Finally, male polar bears differentiate the sex and reproductive condition of other polar bears through their pedal scents (Owen et al. 2014).
Some researchers have explored the use of olfaction to repel American black bears, brown bears, and polar bears, with mixed success for ammonia and with the most consistent success for red pepper spray (Smith et al. 2008). Food-based scents have been used to attract Andean bears, American black bears, and brown bears for research and management purposes, but it’s not well-known how the response to those attractants varies within and among bear populations and with the individual bear’s past experiences. The compounds which bears use to learn about their environment and other bears must be readily airborne, but they must also persist over time. The life span of these compounds depends not only on molecular characteristics but also on environmental factors such as airflow and humidity. There has been a little theoretical and empirical research on how environmental factors affect olfaction by polar bears (Togunov et al. 2017), but those predictions might be dramatically different in the forested habitats in which most other bears live.
Tactile Perception (Touch)
While the senses of vision, hearing, olfaction, and taste have their own organs, the sense of touch depends on sensory nerve endings distributed over the entire body. There are sensory nerves connected to each hair follicle, pain and temperature receptors scattered throughout the skin, and motor nerves that innervate the erector pili muscles and glands. This rich innervation is crucial to sense the environment and react accordingly. The extent of innervation depends on the nature of the tissue, but mammalian skin and skin-related tissues are relatively highly innervated with apparent regional differences. Specialized skin cells (Merkel cells) involved in touch sensation reside in the epidermis, passing mechanical stimuli on to sensory neurons. In some mammals, including bears, they are concentrated in the paws and vibrissae (whiskers). Whiskers are specialized sensory structures relaying vibrotactile information from the environment to the central nervous system. Most mammals possess them, with location, numbers, and function varying across species. Many mammals use them for active discrimination of tactile cues (e.g., rodents, felids, and many pinnipeds), but in bears vibrissal movement is relatively passive, and the hair shafts of vibrissal follicle-sinus complexes are reduced in size, similar as in dogs and other canids (Marshall et al. 2006). Deeper in the skin there are corpuscular receptors, of which Meissner corpuscles (tactile corpuscles) respond to light touch and Pacinian corpuscles (lamellated corpuscles) respond to vibrations. These receptors tend to be concentrated in the most touch-sensitive body regions of mammals, such as fingers, palms, and paws.
Bears appear to be quite “manual” and use their paws for foraging and manipulating food, exploring, and marking. Both American black bears and brown bears were observed to use tactile (and acoustical) cues when shifting from visually oriented foraging during the day to foraging in the darkness while fishing for salmon in forest streams (Klinka and Reimchen 2002). In addition to foraging, tactile senses are relevant to various social behaviors, orientation, and navigation. In bears, relatively extensive touching and rubbing is observed during play and in maternal, sexual, and social contexts. Tactile contacts are also present during aggressive interactions.
Bears’ sense of taste is thought to be primarily used in foraging. Although polar bears are primarily carnivorous, giant pandas are almost entirely herbivorous, and sloth bears are primarily insectivorous, the other four bear species are omnivorous with diets that vary among species, among populations, and even among individuals. Bears’ taste receptors are located within their mouths in small structures (papillae) with both herbivorous and carnivorous characteristics (Pastor et al. 2008, 2011). Research into the nutritional ecology of bears has improved our understanding of the complexity and function of foraging across bear species, but that research alone does not reveal the sensory cues by which bears select their diet. It’s thought that most mammals use different receptors to perceive five classes of taste: sweet, umami, bitter, salty, and sour. Selective foraging by bears can be very fine-scaled, which may reflect temporally variable chemical and nutritional characteristics of potential food items, which bears presumably detect through differences in flavor. Genetic analyses have suggested that, in general, as the diets of various mammals have changed, their sense of taste has also changed. However, it’s unclear that differences in diet among the different bear species are reflected by differences in their sense of taste. In addition, although some marine carnivores have lost the ability to taste sweet, bitter, and perhaps umami flavors, those functions have not yet been evaluated in the semi-marine bear, the polar bear. In experimental tests, Andean bears, known to eat at least 300 species of plants and 40 species of animals, have preferred foods containing sugars and some other sweeteners (Jiang et al. 2012).
Although incomplete, the most-developed research linking a bear’s sense of taste, foraging, and nutritional ecology has been conducted in the giant panda. Giant pandas only rarely eat meat, and it’s been suggested that they’ve lost the perception of umami (Zhao et al. 2010), which reflects amino acids in foods. Molecular and behavioral evidence indicates that giant pandas, similar to Andean bears, taste simple sugars and prefer foods with them (Jiang et al. 2014). That preference may mediate the seasonal shifts in foraging preference among wild giant pandas for bamboo culm versus bamboo leaves, coinciding with seasonal shifts in the relative abundance of sugars and nondigestible fiber in those plant tissues (Knott et al. 2017). In addition to sweet flavors, bamboo also includes bitter-tasting compounds. Consistent with the potential for bitter flavors to be important cues for the giant panda, the giant panda possesses genes for bitter taste receptors that are not found in several carnivores that do not feed on bitter-tasting foods, including the polar bear (Shan et al. 2018); it is not known bears with more diverse diets perceive or respond to bitter flavors.
There have been attempts to use bears’ sense of taste (e.g., reaction to capsaicin as in hot peppers) to repel them from potential sources of conflict with people and to teach them to avoid anthropogenic food sources. These attempts have not been consistently successful and have revealed complex interactions among sensory systems; although pepper spray may repel brown bears and polar bears when in an aerosol form, the non-aerosol form of that same mixture may attract bears, possibly through its flavor (Smith et al. 2008).
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