Research

Dissertation Research

Greater Caribbean manatee (Trichechus manatus manatus) hearing: Using air conduction and bone conduction hearing tests to establish hearing acuity

Manatees are listed as vulnerable on the International Union for Conservation of Nature (IUCN) red list of threatened species (Runge et al., 2017). Manatees live close to human developments and swim in the same waters where recreational watersports are enjoyed. However, their interactions with humans result not only in increasing annual mortalities but also invoke multiple sources of noise infiltrating their habitats continuously. To develop recommendations, enhance hearing protection, and guide noise regulations, we need to gather data feasibly and appropriately on manatee hearing acuity (hearing range and auditory threshold). This proposed research will influence noise regulations for manatees in the following ways:

1. The largest study of manatee hearing.

2. Expand current research by including a subspecies with hearing acuity not previously tested.

3. Examine the feasibility of a new approach, BC-BAER, to evaluate the hearing acuity of manatees.

4. Use two different mechanisms of hearing: air conduction and bone conduction to determine what hearing conduction mechanism is better suited for testing manatee hearing.

Prior to the last 10 years, manatees were considered minimally vocal animals. However, recent findings suggest they communicate through vocal sounds more than previously thought (Brady et al., 2022). As we increasingly understand the importance of sound for the biological fitness of manatees, knowledge of their hearing abilities becomes imperative so we can determine how human activities (e.g., noise pollution) have an impact on their hearing, communication, and/or their behavior. Therefore, we need a comprehensive understanding of hearing abilities for communication within the manatee family.

Presently, there is limited information on hearing acuity across different species of manatees. Hearing acuity has been tested behaviorally (Gaspard et al., 2012; Gerstein et al., 1999) and using Air-Conduction Brainstem Auditory Evoked Response (AC-BAER; a passive hearing test) (Bullock et al., 1982; Mann et al.,2005) on a small sample (n=4) of captive male Florida manatees (T. manatus latirostris). Only one (female) Amazonian manatee (T. inunguis) has been tested using the passive AC-BAER (Klishin et al., 1990), and no African (T. senegelensis) or Greater Caribbean (T. m. manatus) manatees have been tested. The wide variation in hearing acuity currently found in manatees (Gaspard et al., 2012; Gerstein et al., 1999) may be due to the ability of manatees to close their external ear canals, similar to phocid seals, based on their fully aquatic lifestyle and direct phylogenetic relatedness to elephants who can close their external ear canals (Lucke et al., 2016; Moore et al., 2022). However, no bone conduction (BC)-BAER (passive testing that circumvents a closed ear canal) has been used to test manatee hearing.

The purpose of this study is to increase our understanding of manatee hearing by studying the hearing abilities of Greater Caribbean manatees using a novel approach of AC-BAER with the addition of BC-BAER and to determine what hearing conduction mechanism is better suited for testing manatee hearing.

Other Ongoing Research

Gray seals (Halichoerus grypus) and offshore windfarm noise: Using bone conduction hearing tests to establish hearing thresholds

Gray seals (Halichoerus grypus) outer ears close when sedated, requiring appropriate methods to test hearing, circumventing the outer and middle ear (air conduction). Anthropogenic noise exposure (e.g., offshore windfarms) in the marine environment is a risk to seals, requiring appropriate methods for testing hearing. Bone Conduction Brainstem Auditory Evoked Response (BC-BAER) was investigated in six gray seals to characterize responses elicited by different acoustic stimuli, evaluate the potential of using BC-BAER to estimate hearing sensitivity, and best placement of the bone transducer. Seals were tested in December 2023 and February 2024 during ongoing research at the Sea Mammal Research Unit, University of St. Andrews, Scotland. Gated tone bursts and broadband click stimuli were presented to characterize evoked responses. Visual identification of Wave V estimated hearing thresholds. Best placement of the bone transducer was determined between the mastoid and zygomatic process. BC-BAER measurements in six seals using gated tone bursts had responses from 250-8000 Hz, the limits of the RadioEar-B71 bone transducer. Average threshold values were 47.33 re dB 20 µPa for tone bursts at 4000 Hz, the maximum sensitivity of frequencies tested. Measurements using clicks in three seals had average threshold values of 52.67 re dB 20 µPa. The recording of BC-BAER is a viable means of studying hearing in gray seals with the best placement of the RadioEar-B71 bone transducer being the zygomatic process.

Exploring Cheetah (Acinonyx jubatus) Auditory Sensitivity from 0.125-10 kHz using Auditory Brainstem Response

The auditory brainstem response (ABR) to gated tone burst of five frequencies ranging from 0.125-10 kHz as well as broadband click stimuli was recorded in two cheetahs (Acinonyx jubatus). The cheetah ABR consisted of five waves that were visible within the first 10 ms for all stimuli presented. The amplitude of wave III and V varied depending on intensity and frequency of stimuli. No clear pattern was present among wave amplitudes of wave III/V, frequency, or stimulus intensity. The latency of waves III-V of the cheetah increased as stimulus intensity decreased, similar to other mammals. Frequency specific thresholds obtained from two cheetahs using ABR were combined to construct an audiogram of cheetah hearing. Auditory sensitivity had no sharp increase at any frequency, with the greatest range of sensitivity recorded being from 4-10 kHz. Overall, we observed that the cheetah audiogram has a similar shape to other mammals, specifically the domestic cat and polar bear. We report, for the first time, hearing estimates from two cheetahs.

Review of Mammal Hearing Ranges

In this review, I am compiling all research published to date in which the hearing ranges of "normal hearing" non-human mammals have been studied.

Previous Work

Manatees are herbivorous aquatic mammals found in the coastal and inland waters of the Atlantic Ocean. All three manatee species are currently listed as vulnerable on the IUCN red list and there still remains much unknown about their ecology. It is currently unknown what sensory modalities manatees use to locate their food in the wild. A literature review of the Paenungulata clade (sirenians, proboscideans, and hyracoideans) was conducted in order to compare and contrast what is known about the sensory modalities of the clade, to better understand the sensory modalities of manatees, particularly the ones they use to locate their food. Manatees have a higher frequency range for hearing than elephants, who have the best low-frequency hearing range known to mammals; hearing range of hyrax is unknown. All members of Paenungulata have vibrissae assisting in tactile abilities and potentially compensate for other senses such as hearing or vision. The ability to smell in manatees and hyrax is unknown, but elephants have been found to have an excellent sense of smell. Manatees, elephants, and hyrax have dichromatic vision. A preliminary experiment was designed to test manatee feeding modalities in the wild.

The objectives of this study were to determine if the proposed methodology, modified for an aquatic environment from Renda & Roux (2017), was capable of testing manatee sensory use by limiting the sensory cues provided. Sensory modalities used in locating food were tested in two ways: when they know where the food is located, within a short distance, and when the food is placed randomly throughout their habitat, at long distances.

In this study, we were able to show that the experimental design works, and provide preliminary data. In the short distance dichotomous choice trials, the percent of correct choices were 67% for the chemoreception + vision, 60% for chemoreception only, and 60% for vision only, with 50% being the rate of chance. For long distance experiments, the mean minimum time in hours it took manatees to consume the food placed randomly along their habitat of San San-Pond Sak River, Panama was 12.0 hours for chemoreception + vision, more than 22 hours for chemoreception only, and 6.89 hours for the control (no box). Due to the small sample size, no definitive conclusion could be made as to which sensory modality manatees use to find food, but our results support the idea that manatees use multiple modalities, chemoreception + vision, to locate food. Additional trials are needed in order to perform statistical analysis on the data.