Introduction to Primate Hearing and Communication

Fig. 1.1
Taxonomy and geographic location of the major primate groups based on Fleagle (2013). Photos from top to bottom: Ring-tailed lemur (Lemur catta) (iStock.​com/​voraorn); Aye-aye (Daubentonia madagascariensis) (iStock.​com/​javarman3); Slow loris (Nycticebus coucang) (iStock.​com/​GreyCarnation); Tarsier (Carlito sp.) (iStock.​com/​LaserLens); Brown titi monkey (Callicebus brunneus) (iStock.​com/​alexakriesphotog​raphy); White-faced capuchin (Cebus capucinus) (iStock.​com/​DamianPEvans); Rhesus macaque (Macaca mulatta) (iStock.​com/​Donyanedomam); and Chimpanzee (Pan troglodytes) (iStock.​com/​Fotoamator)

Within the strepsirrhines, the infraorder Lorisiformes includes nine genera of nocturnal, insectivorous species that occupy Asia or Africa, such as the slow loris (Nycticebus coucang) and the galago (Galago sp.). The infraorder Lemuriformes includes fifteen genera that have been isolated on the island of Madagascar for approximately 60 million years and have proliferated into many niches. The Lemuriformes are more variable in their behavior and ecology than the Lorisformes, including species such as the aye-aye (Daubentonia madagascariensis) that is nocturnal and solitary and the ring-tailed lemur (Lemur catta) that is diurnal and has social groups containing an average of approximately fifteen individuals (Mittermeier et al. 2010).

The second primate semiorder, Haplorhini, includes two suborders. The suborder Tarsiiformes is made up of three genera of small (about 50–150 g), arboreal, leaping, nocturnal, faunivorous tarsiers (Tarsius sp.) from Asia. Although the tarsiers resemble strepsirrhines more closely in their behavior and appearance, they are grouped with the haplorhines on the basis of several evolutionarily derived features not found in strepsirrhines (Wright et al. 2003).

The haplorhine suborder Anthropoidea includes two infraorders. The infraorder Platyrrhini is composed of the New World monkeys that currently live in Central and South America. They likely arrived around 40 Ma after drifting on debris across the Atlantic Ocean from Africa and have since been isolated from other primates (Poux et al. 2006). The New World monkeys include eighteen genera that range in body size from 100 g to 10 kg, are highly arboreal, and consume mostly fruit and plant materials. All are diurnal except for the owl monkey (Aotus sp.), which is the only nocturnal anthropoid. Most New World monkeys are arboreal quadrupeds, but some, such as the spider monkey (Ateles sp.), practice brachiation, and four genera have fully prehensile tails (Garber et al. 2009).

The second haplorhine infraorder, Catarrhini, includes two major superfamilies. The superfamily Cercopithecoidea (Old World monkeys) includes twenty-three genera from Africa and Asia, approximately 2–31 kg, all of which are diurnal. They show a wide variety of locomotor, social, and dietary habits, ranging from the arboreal, quadrupedal colobus monkeys (e.g., Colobus sp.), which have specialized stomachs for processing plant materials, to the more terrestrial geladas (Theropithecus gelada), which move across the highlands of Ethiopia in hordes of hundreds to thousands of individuals (Campbell et al. 2010).

The other haplorhine superfamily, the Hominoidea, comprises eight extant genera, including apes and humans. Apes are diurnal primates that lack tails and evince complex social relationships and intelligence. The “lesser” apes (about 5–12 kg) are the gibbons (e.g., Hylobates sp.), which are monogamous arboreal brachiators that inhabit Asia. The “great” apes are larger in body size (about 34–175 kg) and include the largely solitary, slow-moving, arboreal clambering orangutans (Pongo) of Asia and the gregarious, omnivorous chimpanzees (Pan sp.) and folivorous gorillas (Gorilla gorilla) of Africa that practice terrestrial knuckle walking and arboreal suspensory behavior (Fleagle 2013).

The earliest humans, also referred to as hominins, diverged from their common ancestor with chimpanzees approximately 6-7 Ma in or near Africa. The earliest traits that defined humans include changes in the dentition (reduction in size of canine teeth) and the adoption of habitual bipedal locomotion. Since the late 1900s, the general thought has been that the driving force in hominin evolution was exploitation of a more open savanna habitat in the face of reduced rainforest habitat, although there is evidence to suggest that the forest still played an important role in early hominin behavior (Wood and Harrison 2011). The earliest hominins, dating to 4–6 Ma, were transitional bipeds but still retained the approximate body and brain size of chimpanzees; there is no evidence of tool use. The Australopithecines (2–4 Ma) were well adapted to bipedalism and had further canine reduction but still retained small body and brain size and limited tool use (Wood and Richmond 2000).

The evolution of the genus Homo around 2.5 Ma saw the adoption of consistent tool use, an expansion of brain size, and, eventually, an increase in stature and leg length and a reduction in arm length (Collard and Wood 2007). It was the genus Homo, specifically Homo erectus, that first left Africa approximately 1.8 Ma. The ancestors of the Neandertals (Homo sp.) first emerged in Europe around 500 thousand years ago (Ka) (Arsuaga et al. 2014), and the Neandertals themselves (Homo neanderthalensis) evolved in Europe around 200 Ka, roughly at the same time that modern humans, Homo sapiens, evolved in Africa (McDougall et al. 2005).

1.2 Primate Hearing and Communication

The hearing abilities of primates have been tested experimentally in nearly 10% of species across the order, and these studies have revealed consistent patterns as well as interesting variations (Ramsier and Rauschecker, Chap. 3). Recent studies have shed light on how variation in anatomical structures along the auditory pathway relates to variations in auditory sensitivity (Coleman and Colbert 2010; Nummela, Chap. 2; Quam, Martínez, Rosa, and Arsuaga, Chap. 8). The work of Brown and Waser (1984) represents one of the rare cases of a study that focused on evolutionary relationships between vocal acoustics and audition in primates. There remains much variation in audition within the order that is not fully understood (Ramsier et al. 2012a; Ramsier and Rauschecker, Chap. 3).

Regarding acoustic communication in general, primates are varied and interesting. For early primates, the dense and discontinuous substrates of an arboreal niche may have decreased the utility of olfactory and visual cues for all but close-range communication, which may have been part of the initial pressure that led to the complex nature of acoustic communication among extant primates (Zimmermann, Chap. 5). Within the larger realm of bioacoustics, anthropologists have long been particularly interested in the vocalizations of nonhuman primates as a model for understanding the evolution of and unique aspects of language in humans (Fedurek and Slocombe 2011). The vocalizations of primates are often species specific and function widely, from communicating with group members and potential mates to warning off competitors and predators (Zuberbühler et al. 1997).

Early studies that included consideration of vocalizations mainly focused on qualitative analyses and descriptions. It was not until the middle of the 20th century that researchers began to include recordings and analyses of the acoustic structure of various calls more routinely. By the turn of the millennium, technological advances and new methodological approaches enabled a greater appreciation for how signals are perceived and used by primates. The range of known primate vocalizations has increased dramatically, and it is now possible to readily obtain high-fidelity, broadband recordings (Maciej et al. 2011) that include very high frequency (i.e., ultrasonic) vocalizations (Ramsier et al. 2012b). New data are also emerging that provide evidence for how variations in vocal acoustics are related to anatomy (Fitch 2006).

Studies of vocal communication in wild primate populations continue to reveal new insights into the social and environmental contexts of many primate calls. Across the order, there is evidence that the number and complexity of vocalizations are tied to social complexity, with more social species producing more complex calls of various types (Semple and McComb 2000; Zimmermann, Chap. 5; Snowdon, Chap. 6; Zuberbühler, Chap. 7). Some primates also communicate with other primate species and emit functionally referential vocalizations that can alert other individuals to specific information, such as the type of predator (e.g., aerial versus terrestrial, leopard versus snake) (Seyfarth et al. 1980; Snowdon, Chap. 6; Zuberbühler, Chap. 7). Nevertheless, there is lingering debate as to the degree to which primate vocalizations have informational content or merely reflect the emotional state of the caller. Most primate vocalizations are considered innate with subtle variations due to voluntary changes in the shape of the vocal tract; however, babbling behavior in some primate species does imply vocal learning (Snowdon, Chap. 6). It is largely agreed that nonhuman primates, while sharing similarities with humans in terms of the function of vocalizations, do not evince the level of complexity and plasticity displayed by humans (Zuberbühler, Chap. 7; Quam, Martínez, Rosa, and Arsuaga, Chap. 8). Phylogenetically, neural control of complex movements of the vocal folds is considered important for the emergence of human speech and language (Fitch et al. 2016).

Several studies have explored how selective pressures, such as habitat structure and ambient environmental acoustics, have influenced the structure of vocalizations produced by primates and the auditory sensitivity of the receivers (Maciej et al. 2011; Brown and Waser, Chap. 4). An analysis of the strepsirrhine semiorder supports a sensory drive hypothesis for primate vocalizations: vocalizations are shaped by external factors such as the sounds produced by predators and habitat acoustics (Zimmermann, Chap. 5). Furthermore, Brown et al. (1995) demonstrated that the broader trend of use of lower frequencies in more forested niches applies to nonhuman primates, agreeing with findings for other taxonomic groups.

1.3 Volume Overview

This volume presents a comprehensive review of nonhuman primate audition and vocal communication and bridges these closely related topics that are often addressed separately. The first section of the book (Chapters 24) involves a discussion of functional anatomy and physiology of sound production, reception, and perception in primates, as well as the acoustic properties of their natural habitats.

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Oct 20, 2017 | Posted by in OTOLARYNGOLOGY | Comments Off on Introduction to Primate Hearing and Communication

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