Marissa A. Ramsier’s research while affiliated with Humboldt State University and other places

The eponymous vocalizations of howling monkeys (genus Alouatta ) are associated with territorial defense and male-male competition, yet the extreme loudness of howls, which are among the loudest vocalizations of any terrestrial mammal, have yet to be fully explained. Loudness facilitates long-distance sound propagation but the effectiveness of any vocal signal depends in part on the auditory capabilities of the intended receiver, and the auditory sensitivities of howling monkeys are unknown. To better understand the evolution of loud calls, we used the auditory brainstem response (ABR) method to estimate the auditory sensitivities of Alouatta palliata . The mean estimated audiogram of four wild-caught adults displayed a w-shaped pattern with two regions of enhanced sensitivity centered at 0.7-1.0 and 11.3 kHz. The lower-frequency region of auditory sensitivity is pitched moderately higher than the fundamental frequencies of howling, whereas the higher-frequency region corresponds well with harmonics in an infant distress call, the wrah-ha . Fitness advantages from detecting infants amid low-frequency background noise, including howling, could explain the incongruity between our ABR thresholds and the fundamental frequencies of howling. Attending to infant calls is expected to enhance reproductive success within an infanticidal genus, and we suggest that the extraordinary loudness of male howling is an indirect (runaway) result of positive feedback between the selective pressures of hearing infant distress calls and deterring infanticide.

The auditory system of nonhuman primates shows evidence of many similarities to humans, such as specializations for the processing of vocalizations overall, processing species-specific vocalizations in particular, and in some cases, the recognition of specific individuals based on call structure. Additionally, nonhuman primates are similar to humans in their excellent localization acuity. Nonhuman primates show differences from humans, though, and not only in the subtleties of the aforementioned abilities. With respect to overall auditory sensitivity, primates have traditionally been portrayed as unspecialized, although there is variation between species. Species in the semiorder Strepsirrhini are, on average, more adept at detecting higher frequencies, whereas the Haplorhini are, on average, more adept at detecting lower frequencies. In addition, a well-supported allometric model explains that smaller headed species with smaller interaural distances need to utilize high-frequency cues for sound localization. Overall auditory sensitivity, particularly to high frequencies, also has been related to increased sociality in some primates. The lack of identification of additional broad trends and relationships between audition and ecology may be partially attributed to the limited dataset, which lacks representation from several major taxonomic subgroups. Additionally, order-wide trends may be minimal given the many possible reasons why enhanced or reduced sensitivity to certain frequency regions may be beneficial for different species. These are just a few of the many facets of primate audition that need to be explored in more depth through additional data gathered via continually evaluated and refined methodologies.

The diverse and well-studied order Primates serves as an excellent model for understanding the evolution of acoustic communication among mammals. Over the past 60 million years, primates have evolved into more than 300 extant species that range from nocturnal to diurnal, arboreal to terrestrial, and solitary to groups of thousands, and they range in body mass from the 30-g pygmy mouse lemur (Microcebus myoxinus) to the 175-kg eastern lowland gorilla (Gorilla beringei graueri). Nonhuman primates vary in their auditory sensitivity and perceptual capabilities and emit a wide range of often complex vocalizations. Some aspects of primate audition and vocalizations have been related to each other and/or phylogeny, anatomy, and ecology, but many aspects have yet to be fully understood. The integration of anatomical and behavioral data on acoustic communication, and the correlates thereof, have significant potential for reconstructing behavior in the fossil record, including that of humans. This volume presents a comprehensive review of nonhuman primate audition and vocal communication to bridge these closely related topics that are often addressed separately. The first section of the book is a discussion of primate sound production, reception, and perception, as well as habitat acoustics in the environmental settings occupied by primates in the wild. The second section focuses on vocal communication in extant primates, including consideration of spectral analyses of primate calls and the evolutionary relationships among hearing, vocal communication, and human language. The goal for this comprehensive approach is to provide new insights into these related topics.

New World monkeys are a diverse primate group and a model for understanding hearing in mammals. However, comparable audiograms do not exist for the larger monkeys, making it difficult to test the hypothesized relationship between interaural distance and high-frequency hearing limit (i.e., the allometric model). Here, the auditory brainstem response (ABR) method is used to assess auditory sensitivity in four tufted capuchins (Sapajus apella), a large monkey with a large interaural distance. A primate-typical four-peak pattern in the ABR waveforms was found with peak latencies from ca. 2 to 12 ms after stimulus onset. Response amplitude decreased linearly with decreasing stimulus level (mean r² = 0.93, standard deviation 0.14). Individual variation in each threshold was moderate (mean ± 7 dB). The 10-dB bandwidth of enhanced sensitivity was 2–16 kHz—a range comparable to smaller monkeys and congruent with the bandwidth of their vocal repertoire. In accord with the general principles of the allometric model, the 60-dB high-frequency limit of S. apella (26 kHz) is lower than those of smaller-headed monkeys; however, it is substantially lower than 44.7 kHz, the value predicted by the allometric model. These findings and other exceptions to the allometric model warrant cautious application and further investigation of other potential selective factors.

Primate bioacoustics includes the study of sounds produced or received by primates, including the acoustic structure of such sounds, underlying mechanisms of production and reception/perception, associated meanings/behaviors, and the influence of habitat structure. The majority of data on primate bioacoustics are focused on vocalizations, both to aid in interpreting the behavior of nonhuman primates, and for comparative purposes in the quest to understand the evolution of human speech and language. Comparably little attention has been paid to the other aspects of primate bioacoustics; however, it is clear that habitat structure may have played an important role in the evolution of primate vocalizations, that primates as a whole are adept at detecting the location of sound sources, and that there may be complex coevolutionary relationships between vocal acoustics, sociality, size, and audition.

Primate Hearing and Communication provides unique insights into the evolution of hearing and communication in primates, including humans. · Introduction to Primate Hearing and Communication Marissa A. Ramsier and Rolf M. Quam · The Primate Peripheral Auditory System and the Evolution of Primate Hearing SirpaNummela · Primate Audition: Reception, Perception, and Ecology Marissa A. Ramsier and Josef P. Rauschecker · Primate Habitat Acoustics Charles H. Brown and Peter M. Waser · Evolutionary Origins of Primate Vocal Communication: Diversity, Flexibility, and Complexity of Vocalizations in Basal Primates Elke Zimmermann · Vocal Communication in Family-Living and Pair-Bonded Primates Charles T. Snowdon · The Primate Roots of Human Language Klaus Zuberbühler · Evolution of Hearing and Language in Fossil Hominins Rolf M. Quam, Ignacio Martínez, Manuel Rosa, and Juan Luis Arsuaga Rolf M. Quam is Associate Professor in the Department of Anthropology, Binghamton University (SUNY), Binghamton, NY Marissa A. Ramsier is Assistant Professor in the Department of Anthropology, Humboldt State University, Arcata, CA Richard R. Fay is Distinguished Research Professor of Psychology at Loyola University of Chicago Arthur N. Popper is Professor Emeritus and Research Professor in the Department of Biology at the University of Maryland, College Park

The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.

Hearing is a crucial element of primate behavior and ecology. Beginning in 1969, traditional behavioral testing methods produced comparable audiograms for five strepsirhine taxa. Variation in this relatively small data set can be explained in part by head size, but relationships with social behavior and ecology have been elusive. Recently, with the use of auditory brainstem response (ABR) methods, standardized audiograms have been published for eleven strepsirhine species. Within this data set, social complexity explains a significant amount of the variation in auditory sensitivity, possibly because sociality favored an enhanced ability to detect conspecific vocalizations such as high frequency alarm calls. These findings shed light on the comparative biology of primate hearing and enable a reconstruction of the ancestral strepsirhine audiogram.