Manatee cognition in the wild: an exploration of the manatee mind and behavior through neuroanatomy, psychophysics, and field observations.

Cognition refers to the mechanisms for acquiring, processing, storing, and acting on information, all of which are critical to understanding the behavior of animals. These mechanisms are poorly known in manatees, especially how they are expressed in the wild. To expand our understanding of manatee cognition, we gathered information from behavioral experimentation in the laboratory, neuroanatomical research, controlled field studies, integrated laboratory and field measurement, and natural history observations (published reports, written surveys, and interviews with knowledgeable observers). Laboratory research, both neuroanatomical and behavioral, provided the most empirical data, primarily on sensory/perceptual capacities. Inferences from these data and narratives from surveys and interviews illuminated possibilities for higher order cognition. Evidence from field measurements was sparse, although substantial amounts of information have been collected from tracking data and to a lesser extent vessel impact studies, which can be used to infer cognitive attributes. Manatees are tactile-auditory specialists with complementary visual and chemosensory abilities. They demonstrate learning characteristics typical of vertebrates. Movement tracking data plus direct observations suggest that they have good spatial cognition, indicated by their ability to traverse complicated water networks and memory for foraging and warm water sites. They engage in a wide range of play-like, object manipulation, and mimetic behaviors, which suggests cognitive capacities beyond basic associative learning. Understanding manatee cognition beyond the laboratory will be necessary for conservation of manatees as they face challenges such as habitat degradation and threats from water-borne vessel traffic. There is a clear need for more direct research in natural settings.

The influence of variations in background noise on Florida manatee (Trichechus manatus latirostris) detection of boat noise and vocalizations.

A manatee's primary modality to detect a vessel on a possible collision course is hearing as underwater visibility is limited in many manatee habitats and their visual acuity is poor. We estimate a Florida manatee's ability to detect the sound of an approaching boat and vocalizations in four different soundscapes in Sarasota Bay, FL. Background noise samples were collected every 5 minutes for a two-week period during winter and summer at each location (2019 or 2020). Sound levels in third octave bands (0.5, 1, 2, 4, and 8 kHz) were measured and compared to manatee auditory hearing thresholds and to sound levels of an approaching boat traveling at a slow, medium, or fast speed. Background sound levels in a wider band (1-20 kHz) were calculated to model vocal communication space at each location. We found that a manatee's estimated ability to detect an approaching boat differs greatly among locations, with time of day, and by season, and that fast boats are predicted to be detected later than slow boats. Latency of boat noise detection is estimated to sharply increase when considering unusually loud background noise levels. We suggest that such uncommonly loud conditions (e.g. 95th percentile sound level), not just typical conditions (median sound level), are important to consider for understanding the problem of manatee-boat collisions. Additionally, background noise impacts estimated vocal communication space and may limit the ability of vocal-mediated mother-calf cohesion. Altogether, a manatee's ability to detect acoustic signals of interest is expected to vary greatly spatially and temporally.

The Relevance of Ecological Transitions to Intelligence in Marine Mammals.

Macphail's comparative approach to intelligence focused on associative processes, an orientation inconsistent with more multifaceted lay and scientific understandings of the term. His ultimate emphasis on associative processes indicated few differences in intelligence among vertebrates. We explore options more attuned to common definitions by considering intelligence in terms of richness of representations of the world, the interconnectivity of those representations, the ability to flexibly change those connections, and knowledge. We focus on marine mammals, represented by the amphibious pinnipeds and the aquatic cetaceans and sirenians, as animals that transitioned from a terrestrial existence to an aquatic one, experiencing major changes in ecological pressures. They adapted with morphological transformations related to streamlining the body, physiological changes in respiration and thermoregulation, and sensory/perceptual changes, including echolocation capabilities and diminished olfaction in many cetaceans, both in-air and underwater visual focus, and enhanced senses of touch in pinnipeds and sirenians. Having a terrestrial foundation on which aquatic capacities were overlaid likely affected their cognitive abilities, especially as a new reliance on sound and touch, and the need to surface to breath changed their interactions with the world. Vocal and behavioral observational learning capabilities in the wild and in laboratory experiments suggest versatility in group coordination. Empirical reports on aspects of intelligent behavior like problem-solving, spatial learning, and concept learning by various species of cetaceans and pinnipeds suggest rich cognitive abilities. The high energy demands of the brain suggest that brain-intelligence relationships might be fruitful areas for study when specific hypotheses are considered, e.g., brain mapping indicates hypertrophy of specific sensory areas in marine mammals. Modern neuroimaging techniques provide ways to study neural connectivity, and the patterns of connections between sensory, motor, and other cortical regions provide a biological framework for exploring how animals represent and flexibly use information in navigating and learning about their environment. At this stage of marine mammal research, it would still be prudent to follow Macphail's caution that it is premature to make strong comparative statements without more empirical evidence, but an approach that includes learning more about how animals flexibly link information across multiple representations could be a productive way of comparing species by allowing them to use their specific strengths within comparative tasks.

Detection of hydrodynamic stimuli by the postcranial body of Florida manatees (Trichechus manatus latirostris).

Manatees live in shallow, frequently turbid waters. The sensory means by which they navigate in these conditions are unknown. Poor visual acuity, lack of echolocation, and modest chemosensation suggest that other modalities play an important role. Rich innervation of sensory hairs that cover the entire body and enlarged somatosensory areas of the brain suggest that tactile senses are good candidates. Previous tests of detection of underwater vibratory stimuli indicated that they use passive movement of the hairs to detect particle displacements in the vicinity of a micron or less for frequencies from 10 to 150 Hz. In the current study, hydrodynamic stimuli were created by a sinusoidally oscillating sphere that generated a dipole field at frequencies from 5 to 150 Hz. Go/no-go tests of manatee postcranial mechanoreception of hydrodynamic stimuli indicated excellent sensitivity but about an order of magnitude less than the facial region. When the vibrissae were trimmed, detection thresholds were elevated, suggesting that the vibrissae were an important means by which detection occurred. Manatees were also highly accurate in two-choice directional discrimination: greater than 90% correct at all frequencies tested. We hypothesize that manatees utilize vibrissae as a three-dimensional array to detect and localize low-frequency hydrodynamic stimuli.

Eight-choice sound localization by manatees: performance abilities and head related transfer functions.

Two experiments investigated the ability and means by which two male Florida manatees (Trichechus manatus latirostris) may determine the direction of a sound source. An eight-choice discrimination paradigm was used to determine the subjects' sound localization abilities of five signal conditions covering a range of frequencies, durations, and levels. Subjects performed above the 12.5% chance level for all broadband frequencies and were able to localize sounds over a large level range. Errors were typically located to either side of the signal source location when presented in the front 180° but were more dispersed when presented from locations behind the subject. Front-to-back confusions were few and accuracy was greater when signals originated from the front 180°. Head-related transfer functions were measured to determine if frequencies were filtered by the manatee body to create frequency-specific interaural level differences (ILDs). ILDs were found for all frequencies as a function of source location, although they were largest with frequencies above 18 kHz and when signals originated to either side of the subjects. Larger ILDs were found when the signals originated behind the subjects. A shadowing-effect produced by the body may explain the relatively low occurrence of front-back confusions in the localization study.

Detection of hydrodynamic stimuli by the Florida manatee (Trichechus manatus latirostris).

Florida manatees inhabit the coastal and inland waters of the peninsular state. They have little difficulty navigating the turbid waterways, which often contain obstacles that they must circumnavigate. Anatomical and behavioral research suggests that the vibrissae and associated follicle-sinus complexes that manatees possess over their entire body form a sensory array system for detecting hydrodynamic stimuli analogous to the lateral line system of fish. This is consistent with data highlighting that manatees are tactile specialists, evidenced by their specialized facial morphology and use of their vibrissae during feeding and active investigation/manipulation of objects. Two Florida manatees were tested in a go/no-go procedure using a staircase method to assess their ability to detect low-frequency water movement. Hydrodynamic vibrations were created by a sinusoidally oscillating sphere that generated a dipole field at frequencies from 5 to 150 Hz, which are below the apparent functional hearing limit of the manatee. The manatees detected particle displacement of less than 1 µm for frequencies of 15-150 Hz and of less than a nanometer at 150 Hz. Restricting the facial vibrissae with various size mesh openings indicated that the specialized sensory hairs played an important role in the manatee's exquisite tactile sensitivity.

Underwater hearing in the loggerhead turtle (Caretta caretta): a comparison of behavioral and auditory evoked potential audiograms.

The purpose of this study was to compare underwater behavioral and auditory evoked potential (AEP) audiograms in a single captive adult loggerhead sea turtle (Caretta caretta). The behavioral audiogram was collected using a go/no-go response procedure and a modified staircase method of threshold determination. AEP thresholds were measured using subdermal electrodes placed beneath the frontoparietal scale, dorsal to the midbrain. Both methods showed the loggerhead sea turtle to have low frequency hearing with best sensitivity between 100 and 400 Hz. AEP testing yielded thresholds from 100 to 1131 Hz with best sensitivity at 200 and 400 Hz (110 dB re. 1 µPa). Behavioral testing using 2 s tonal stimuli yielded underwater thresholds from 50 to 800 Hz with best sensitivity at 100 Hz (98 dB re. 1 µPa). Behavioral thresholds averaged 8 dB lower than AEP thresholds from 100 to 400 Hz and 5 dB higher at 800 Hz. The results suggest that AEP testing can be a good alternative to measuring a behavioral audiogram with wild or untrained marine turtles and when time is a crucial factor.

Audiogram and auditory critical ratios of two Florida manatees (Trichechus manatus latirostris).

Manatees inhabit turbid, shallow-water environments and have been shown to have poor visual acuity. Previous studies on hearing have demonstrated that manatees possess good hearing and sound localization abilities. The goals of this research were to determine the hearing abilities of two captive subjects and measure critical ratios to understand the capacity of manatees to detect tonal signals, such as manatee vocalizations, in the presence of noise. This study was also undertaken to better understand individual variability, which has been encountered during behavioral research with manatees. Two Florida manatees (Trichechus manatus latirostris) were tested in a go/no-go paradigm using a modified staircase method, with incorporated 'catch' trials at a 1:1 ratio, to assess their ability to detect single-frequency tonal stimuli. The behavioral audiograms indicated that the manatees' auditory frequency detection for tonal stimuli ranged from 0.25 to 90.5 kHz, with peak sensitivity extending from 8 to 32 kHz. Critical ratios, thresholds for tone detection in the presence of background masking noise, were determined with one-octave wide noise bands, 7-12 dB (spectrum level) above the thresholds determined for the audiogram under quiet conditions. Manatees appear to have quite low critical ratios, especially at 8 kHz, where the ratio was 18.3 dB for one manatee. This suggests that manatee hearing is sensitive in the presence of background noise and that they may have relatively narrow filters in the tested frequency range.

Manatee vibrissae: evidence for a "lateral line" function.

Aquatic mammals use vibrissae to detect hydrodynamic stimuli over a range from 5 to 150 Hz, similar to the range detected by lateral line systems in fishes and amphibians. Manatees possess ∼5,300 vibrissae distributed over the body, innervated by ∼209,000 axons. This extensive innervation devoted to vibrissae follicles is reflected in enlarged, elaborate somatosensory regions of the gracile, cuneate, and Bischoff's brain-stem nuclei, ventrobasal thalamus, and presumptive somatosensory cortex. Our preliminary psychophysical testing indicates that in Florida and Antillean manatees the Weber fraction for detection thresholds for grating textures ranges from 0.025 to 0.14. At the lower end of this range, sensitivity is comparable to human index finger thresholds. For hydrodynamic stimuli of 5-150 Hz, detection threshold levels for manatees using facial or postfacial vibrissae were substantially lower than those reported for harbor seals and similar to reports of sensitivity for the lateral line systems of some fish. Our findings suggest that the facial and postfacial vibrissae are used to detect hydrodynamic stimuli, whereas only the facial vibrissae are used for direct contact investigation.

Four-choice sound localization abilities of two Florida manatees, Trichechus manatus latirostris.

The absolute sound localization abilities of two Florida manatees (Trichechus manatus latirostris) were measured using a four-choice discrimination paradigm, with test locations positioned at 45 deg., 90 deg., 270 deg. and 315 deg. angles relative to subjects facing 0 deg. Three broadband signals were tested at four durations (200, 500, 1000, 3000 ms), including a stimulus that spanned a wide range of frequencies (0.2-20 kHz), one stimulus that was restricted to frequencies with wavelengths shorter than their interaural time distances (6-20 kHz) and one that was limited to those with wavelengths longer than their interaural time distances (0.2-2 kHz). Two 3000 ms tonal signals were tested, including a 4 kHz stimulus, which is the midpoint of the 2.5-5.9 kHz fundamental frequency range of manatee vocalizations and a 16 kHz stimulus, which is in the range of manatee best-hearing sensitivity. Percentage correct within the broadband conditions ranged from 79% to 93% for Subject 1 and from 51% to 93% for Subject 2. Both performed above chance with the tonal signals but had much lower accuracy than with broadband signals, with Subject 1 at 44% and 33% and Subject 2 at 49% and 32% at the 4 kHz and 16 kHz conditions, respectively. These results demonstrate that manatees are able to localize frequency bands with wavelengths that are both shorter and longer than their interaural time distances and suggest that they have the ability to localize both manatee vocalizations and recreational boat engine noises.

Temporal resolution of the Florida manatee (Trichechus manatus latirostris) auditory system.

Auditory evoked potential (AEP) measurements of two Florida manatees (Trichechus manatus latirostris) were measured in response to amplitude modulated tones. The AEP measurements showed weak responses to test stimuli from 4 kHz to 40 kHz. The manatee modulation rate transfer function (MRTF) is maximally sensitive to 150 and 600 Hz amplitude modulation (AM) rates. The 600 Hz AM rate is midway between the AM sensitivities of terrestrial mammals (chinchillas, gerbils, and humans) (80-150 Hz) and dolphins (1,000-1,200 Hz). Audiograms estimated from the input-output functions of the EPs greatly underestimate behavioral hearing thresholds measured in two other manatees. This underestimation is probably due to the electrodes being located several centimeters from the brain.