Audiograms of howling monkeys: are extreme loud calls the result of runaway selection?

Abstract

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 sensory ecology of primate food perception, revisited

“…Overall, primates are comparable to other similarly sized mammals in high‐frequency hearing and exhibit reasonable sensitivity to low‐frequency sounds 10,15 . However, the auditory sensitivities of primates can vary widely, sometimes as a function of phylogeny and head‐size constraints, 10,16 or the pressures of natural and sexual selection 17–19 …”

“…10,15 However, the auditory sensitivities of primates can vary widely, sometimes as a function of phylogeny and head-size constraints, 10,16 or the pressures of natural and sexual selection. [17][18][19] The genetic basis of auditory perception was poorly understood and not addressed in Dominy et al's 5 original 2001 review.…”

Noise intensity modulates the responses of mantled howler monkeys to anthropophony

“…Considering that mantled howler monkeys have enhanced auditory sensitivity at lower frequencies compared to other primate species (Ramsier et al, 2019), they may be particularly susceptible to anthropogenic noise, which is typically low-frequency (Barber et al, 2010;Francis et al, 2009). Further understanding of the effects of anthropogenic noise on mantled howler monkeys will require deeper knowledge of the sense of hearing of this species, which remains practically unstudied (Hernández-Salazar et al, 2015).…”

“…However, pygmy marmoset behavior is also not influenced by the intensity of simulated human speech (played back at 30, 60, and 78 dB: Sheehan & Papworth, 2019) and in Bolivian gray titi monkeys, from a total of eight response variables (including fGCM and social proximity), only time spent moving was negatively associated with noise intensity (Hernani Lineros et al, 2020). Considering that mantled howler monkeys have enhanced auditory sensitivity at lower frequencies compared to other primate species (Ramsier et al, 2019), they may be particularly susceptible to anthropogenic noise, which is typically low‐frequency (Barber et al, 2010; Francis et al, 2009). Further understanding of the effects of anthropogenic noise on mantled howler monkeys will require deeper knowledge of the sense of hearing of this species, which remains practically unstudied (Hernández‐Salazar et al, 2015).…”