Auditory sensitivity of the tufted capuchin (Sapajus apella), a test of allometric predictions.

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 communication in the pure ultrasound.

Few mammals-cetaceans, domestic cats and select bats and rodents-can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.

A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang.

Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost-effective alternative-the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring-tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally-derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high-frequency limits were comparable. However, at frequencies < or =2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10-dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR- and behaviorally-derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising technique for estimating primate hearing sensitivity, but that additional data are required to explore its efficacy for estimating low-frequency thresholds.

Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis).

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.

Social drive and the evolution of primate hearing.

The structure and function of primate communication have attracted much attention, and vocal signals, in particular, have been studied in detail. As a general rule, larger social groups emit more types of vocal signals, including those conveying the presence of specific types of predators. The adaptive advantages of receiving and responding to alarm calls are expected to exert a selective pressure on the auditory system. Yet, the comparative biology of primate hearing is limited to select species, and little attention has been paid to the effects of social and vocal complexity on hearing. Here, we use the auditory brainstem response method to generate the largest number of standardized audiograms available for any primate radiation. We compared the auditory sensitivities of 11 strepsirrhine species with and without independent contrasts and show that social complexity explains a significant amount of variation in two audiometric parameters-overall sensitivity and high-frequency limit. We verified the generality of this latter result by augmenting our analysis with published data from nine species spanning the primate order. To account for these findings, we develop and test a model of social drive. We hypothesize that social complexity has favoured enhanced hearing sensitivities, especially at higher frequencies.