CETACEAN AUDITORY PSYCHOPHYSICS

ABSTRACT

The dolphin continues to capture the imagination of investigators because of its ability to echolocate. Echolocation is essentially a special extension and adaptation of the dolphin's hearing system, coupled with the animal's ability to generate special sounds. Humans have demonstrated the ability to judge room size based on reverberation from a voice, and some of the visually challenged use self-generated sounds to detect large reflective objects. Echolocation represents a highly refined acoustic ability on a broad acoustic sensory continuum. Research on the auditory and echolocation performance of cetaceans has moved forward slowly due to limited animal resources and the general high cost of maintaining these animals in a laboratory environment.

This paper reviews some of the more relevant psychoacoustic data on cetaceans, and concentrates on the bottlenose dolphin Tursiops truncatus. The information presented is not at all exhaustive. Early work with dolphins focused mainly on the animal's ability to use its echolocation system. Once echolocation capability was demonstrated using a blindfolded dolphin, the quest to understand dolphin sonar moved from qualifying the dolphin's echolocation skill to quantifying its basic capabilities.

Psychophysics, and more precisely psychoacoustics, provides the tools to study dolphin echolocation. The procedures, theories and even the apparatuses from the traditional psychoacoustics laboratory are adapted to the dolphin experimental setting to measure and analyze the sensory phenomenon of dolphin echolocation. Basic auditory phenomena such as the audiogram, the effects of masking, critical ratio and critical band, and interaural time and intensity discrimination capabilities have been explored in the dolphin. Additionally, special experiments investigating the psychoacoustics of the echolocation system in particular have been conducted.     

BOOK REVIEWS

Psychoacoustic laboratory studies with live dolphins require considerable resources and are essential for assessing the validity of our models. Computerized numerical modelling methods are a reasonable approach to simulate the vibroacoustic functions of the dolphin biosonar apparatus. In order to validate this approach, we chose a vibroacoustic finite element model to simulate sound production and sound beam formation in the bottlenose dolphin (Tursiops truncatus), based on computed tomography scans from live and postmortem dolphins. The right and left dorsal bursae were assumed to be potential sound sources. The simulations confirm several hypotheses: (1) the shape of the skull plays a role in the formation of the sound transmission beam; (2) the melon appears to concentrate the acoustic energy by a factor of four in the transmitted beam; (3) focusing the sound beam apparently occurs in a series of stages that include contributions from the skull, nasal diverticula, melon and connective tissue structures. An unexpected result is that adjustments to the focus and direction of the sound beam can result from small (millimetre scale) changes in the relative position of the anterior and posterior bursae within each sound generation complex. Comparing our results with those from dolphin psychoacoustic experiments establishes validation of our vibroacoustic model. The potential for varied effects from anthropogenic sound also emphasizes the importance of developing vibroacoustic modelling. These numerical modelling tools complement experimental data for determining exposure thresholds and may allow us to simulate exposure levels, from moderate to extreme, without impacting live animals.     

Comparison of lipids in selected tissues of the Florida manatee (Order Sirenia) and bottlenose dolphin (Order Cetacea; Suborder Odontoceti)

The position, porosity and oil-filled nature of the zygomatic process of the squamosal bone (ZPSB) of the Florida manatee, Trichechus manatus latirostris, suggest that it may have a similar sound conduction function to that of the intramandibular fat body (IMFB) of the bottlenose dolphin, Tursiops truncatus, and other odontocetes. To examine this possibility we determined the lipid composition of the ZPSB and adipose tissue from the dorsal part of the head region of the Florida manatee, and compared it to that of the dolphin IMFB and melon (another fatty area implicated in sound conduction in odontocetes). Lipids from manatee ZPSB and from adipose tissue were composed almost entirely of triacylglycerols. The most abundant fatty acids of the ZPSB were 18:1, 16:0, 14:0 and 16:1. The major fatty acids of the adipose tissue in the head were the four mentioned above, along with 12:0 and 18:0. Manatee samples did not contain isovaleric acid (iso-5:0), which was found in the bottlenose dolphin IMFB and melon, and has been related to sound conduction in dolphins and some other odontocetes. Thus, if manatee tissues are capable of sound conduction, and this process does occur through the ZPSB, a somewhat different suite of lipid components must support this function.     

GEOGRAPHIC VARIATION IN RATES OF VOCAL PRODUCTION OF FREE-RANGING BOTTLENOSE DOLPHINS

Echolocation and whistle production, group sizes, and activities of free-ranging bottlenose dolphins were compared across four regions (Wilmington, NC Intracoastal Waterway [ICW]; Wilmington coastline; Southport, NC coastline; and Sarasota, FL inshore waters). Number of whistles and echolo-cation bouts differed significantly across sites. Dolphins whistled significantly more in Southport than in the other sites, independent of group size. Unlike at the other sites, dolphin vocalizations in Southport did not vary significantly across activities; this difference may be due to the fact that Southport animals were often found behind shrimp-trawling vessels, which may affect their behavior. Resident Sarasota dolphins vocalized significantly less than dolphins at the NC sites. At most sites, echolocation production per dolphin decreased as group size increased, supporting the idea that echolocation information is shared. In the ICW and Sarasota, echolocation production per dolphin was highest while feeding, indicating that echolocation is used in foraging. At all sites but Southport, whistle production per dolphin was highest while socializing, indicating that whistles are used in communication. Overall, these data show that dolphins have different vocal and activity patterns at different sites; thus, caution should be used when extrapolating results from one study site to another.     

The dolphin cochlear nucleus: Topography,histology and functional implications

Despite the outstanding auditory capabilities of dolphins, there is only limited information available on the cytology of the auditory brain stem nuclei in these animals. Here, we investigated the cochlear nuclei (CN) of five brains of common dolphins (Delphinus delphis) and La Plata dolphins (Pontoporia blainvillei) using cell and fiber stain microslide series representing the three main anatomical planes. In general, the CN in dolphins comprise the same set of subnuclei as in other mammals. However, the volume ratio of the dorsal cochlear nucleus (DCN) in relation to the ventral cochlear nucleus (VCN) of dolphins represents a minimum among the mammals examined so far. Because, for example, in cats the DCN is necessary for reflexive orientation of the head and pinnae towards a sound source, the massive restrictions in head movability in dolphins and the absence of outer ears may be correlated with the reduction of the DCN. Moreover, the same set of main neuron types were found in the dolphin CN as in other mammals, including octopus and multipolar cells. Because the latter two types of neurons are thought to be involved in the recognition of complex sounds, including speech, we suggest that, in dolphins, they may be involved in the processing of their communication signals. Comparison of the toothed whale species studied here revealed that large spherical cells were present in the La Plata dolphin but absent in the common dolphin. These neurons are known to be engaged in the processing of low‐frequency sounds in terrestrial mammals. Accordingly, in the common dolphin, the absence of large spherical cells seems to be correlated with a shift of its auditory spectrum into the high‐frequency range above 20 kHz. The existence of large spherical cells in the VCN of the La Plata dolphin, however, is enigmatic asthis species uses frequencies around 130 kHz. J. Morphol. 2011. © 2011 Wiley Periodicals, Inc.     

Precocial development of axial locomotor muscle in bottlenose dolphins (Tursiops truncatus)

At birth, the locomotor muscles of precocial, terrestrial mammals are similar to those of adults in both mass, as a percent of total body mass, and fiber-type composition. It is hypothesized that bottlenose dolphins (Tursiops truncatus), marine mammals that swim from the instant of birth, will also exhibit precocial development of locomotor muscles. Body mass data from neonatal and adult dolphins are used to calculate Grand's (1992) Neural and Muscular Indices of Development. Using these indices, the bottlenose dolphin is a Condition "3.5" neonate, where Condition 4 is the documented extreme of precocial development in terrestrial mammals. Moreover, myosin ATPase (alkaline preincubation) analyses of the epaxial locomotor m. extensor caudae lateralis show that neonatal dolphins have fiber-type profiles very similar to those of adults. Thus, based on mass and myosin ATPase activity, muscle development in dolphins is precocial. However, succinic dehydrogenase and Nile red histochemistry demonstrate that neonatal dolphin muscle has mitochondrial and lipid distributions different from those found in adults. These data suggest that neonates have a lower aerobic capacity than adults. Dolphin neonates may compensate for an apparent lack of aerobic stamina in two ways: 1) by being positively buoyant, with a relatively increased investment of their total body mass in blubber, and 2) by "free-riding" off their mothers. This study investigates quantitatively the development of a dolphin locomotor muscle and offers suggestions about adaptations required for a completely aquatic existence.     

Feeding aggregation and aggressive interaction between bottlenose (Tursiops truncatus) and Commerson’s dolphins (Cephalorhynchus commersonii) in Patagonia,Argentina

We report the first recorded interactions between bottlenose dolphin (Tursiops truncatus) and Commerson’s dolphins (Cephalorhynchus commersonii). The diurnal behavioral patterns of bottlenose dolphins in Bahía Engaño, Argentina, were similar to those described for other coastal populations around the world. The majority of the feeding bouts were recorded near the mouth the Chubut River. When not feeding near the river, bottlenose dolphins generally swam along the coast, and interactions with Commerson’s dolphins were recorded very close to the shore on two occasions during a 3-year period. In the first event, both species were feeding on a fish school. The second interaction was aggressive in nature, involving one juvenile and three adult bottlenose dolphins with several Commerson’s dolphins. Two of the adult bottlenose dolphins attacked the Commerson’s dolphins. We propose that the observed behavior represented defense of the juvenile bottlenose dolphin.

     

Occurrence of Indo-Pacific bottlenose dolphins (Tursiops aduncus) off the Wild Coast of South Africa using photographic identification

The present study represents the first reported boat-based photographic identification study of Indo-Pacific bottlenose dolphins (Tursiops aduncus) off the Wild Coast of southeast South Africa. This area is known for the annual sardine run, which attracts apex predators to the region during the austral winter. Dedicated photo-identification surveys were conducted along this coast at three different study sites in February, June, and November of each year from 2014 to 2016. During 47 surveys, 136 bottlenose dolphin groups were encountered, an estimated 4,474 dolphins observed, and 2,149 individuals were identified. Although most individuals (N = 1,770, 82.4%) were only observed once, some were resighted 2–7 times (N = 379, 17.6%), with an average of 305 days (range: 88–705 days) between resightings. The majority of bottlenose dolphins were resighted within the same study site (N = 192), indicating some degree of residency. However, 65 individuals were observed at two different study sites, indicating individual movements along the coast. Our findings contrast earlier suggestions that bottlenose dolphins only use the Wild Coast during the sardine run, as we found large number of animals year-round with some level of site fidelity. This highlights the importance of the Wild Coast to bottlenose dolphins and provides further information on their status off southeastern South Africa.     

Long-term passive acoustics to assess spatial and temporal vocalization patterns of Atlantic common bottlenose dolphins (Tursiops truncatus) in the May River estuary,South Carolina

Passive acoustics has been used extensively to study bottlenose dolphins; yet very few studies have examined the spatial, temporal, and environmental influences on vocalization types (echolocation, burst pulse sounds, and whistles), and few are long-term and provide high temporal resolution over multiple years. We used data from 2013 to 2018 to establish baseline acoustic patterns for bottlenose dolphins in the May River estuary, South Carolina. We deployed acoustic recorders at six stations during 2013–2014 and three stations during 2015–2018, with locations spanning the entire estuary (headwaters to the mouth). We discovered that acoustic detection of dolphins varied not only spatially, but also yearly, monthly, and tidally. Higher numbers of echolocation bouts, burst pulse sounds, and whistles were detected at the mouth as compared to the headwaters. At the mouth, vocalization detections were greatest in fall and winter for multiple years, and echolocation detection was greatest during falling and low tides. This study provides an example of another tool, long-term passive acoustics monitoring, to better understand spatial and temporal distribution of dolphins in a typical salt marsh estuary, that can be applied to other ecosystems throughout the southeastern United States and globally.     

High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon

Isovaleric acid (iso5:0) is an unusual fatty acid that is important for echolocation and hearing in acoustic tissues of some odontocetes, but its functional significance in blubber is unknown. We examined patterns of accumulation of this compound in blubber in 30 species of odontocetes ( n=299). Iso5:0 concentrations in blubber varied with phylogeny, ontogeny and body topography. Iso5:0 accumulated in greater quantities in superficial/outer blubber than in deep/inner blubber. In the outer blubber of northern right whale and Hector's dolphins, iso5:0 accounted for one-third to one-half of all fatty acids. Total blubber burden of iso5:0 in harbour porpoises represented up to 15 times the amount deposited in the melon. The composition of the melon does not change during starvation in harbour porpoises, supporting the hypothesis that lipids in melon are conserved for a specific function. Some odontocetes continually deposit iso5:0 in blubber after levels in melon have reached asymptotic levels, suggesting independent control of iso5:0 synthesis and storage in these compartments. Dolphins and porpoises inhabiting cold waters possess higher concentrations of iso5:0 in their outer blubber layers than species from warmer regions. We propose that this relationship represents an adaptive secondary role for iso5:0 in maintaining blubber flexibility in cold environments.     

Use of a serum-based glomerular filtration rate prediction equation to assess renal function by age, sex, fasting, and health status in bottlenose dolphins (Tursiops truncatus)

Glomerular filtration rate (GFR) is a direct measurement of renal function. Although clearance tests using 24‐h urine collection or blood sample series are gold standards for measuring GFR, serum‐based prediction of GFR based upon the Modification of Diet in Renal Disease (MDRD) Study equation is acceptable for routine use in human adults. The purpose of our study was to assess the ability for a modified MDRD Study equation to predict expected changes in GFR in bottlenose dolphins (Tursiops truncatus) using a healthy dolphin population represented by 1,103 routine serum samples collected from 50 dolphins of all age groups, years 1998–2005. Predicted GFR was also calculated from serum collected from a 32‐yr‐old male dolphin with end‐stage renal disease. The dolphin‐adjusted MDRD equation predicted GFR changes in our population that paralleled what has previously been reported in other mammals, including decreasing predicted GFR with age (P < 0.01), higher predicted GFR in dolphins that had recently eaten (P < 0.01), and rapidly decreasing predicted GFR in the animal with end‐stage renal disease. We conclude that a serum‐based GFR prediction equation may be a feasible means of detecting and tracking renal function in bottlenose dolphins.     

The reliability of pigment pattern‐based identification of wild bottlenose dolphins

Long‐term studies often rely on natural markings for individual identification across time. The primary method for identification in small cetaceans relies on dorsal fin shape, scars, and other natural markings. However, dorsal fin markings can vary substantially over time and the dorsal fin can become unrecognizable after an encounter with a boat or shark. Although dorsal fins have the advantage in that they always break the water surface when the cetacean breathes, other physical features, such as body scars and pigmentation patterns can supplement. The goal of this study was to explore the use of dorso‐lateral pigment patterns to identify wild bottlenose dolphins. We employed photographic pigment matching tests to determine if pigmentation patterns showed (1) longitudinal consistency and (2) bilateral symmetry using a 30 yr photographic database of bottlenose dolphins (Tursiops aduncus). We compared experienced dolphin researchers and inexperienced undergraduate student subjects in their ability to accurately match images. Both experienced and inexperienced subjects correctly matched dolphin individuals at a rate significantly above chance, even though they only had 10 s to make the match. These results demonstrate that pigment patterns can be used to reliably identify individual wild bottlenose dolphins, and likely other small cetacean species at other sites.     

Shark bite injuries on three inshore dolphin species in tropical northwestern Australia

Predation risk has a profound influence on the behavior of marine mammals, affecting grouping patterns and habitat use. Dolphins frequently bear evidence of shark bites, which can provide an indirect measure of predation pressure. Using photo‐identification data, we investigated the prevalence of shark bites on three sympatric species of inshore dolphin, the Australian snubfin (Orcaella heinsohni), Australian humpback (Sousa sahulensis), and Indo‐Pacific bottlenose dolphin (Tursiops aduncus), among four study sites in northwestern Australia. Bite prevalence varied markedly between species, with 72% of snubfin, 46% of humpback, and 18% of bottlenose dolphins exhibiting evidence of shark bites. Binomial logistic regression confirmed a high likelihood of bite presence on snubfin dolphins, and at one particular site for snubfin and bottlenose dolphins. The prevalence of tiger shark (Galeocerdo cuvier) bites on snubfin dolphins was high, and bites attributed to other carcharhinid sharks were observed on all species. While acknowledging methodological differences with other studies, the prevalence of shark bites on snubfin dolphins is among the highest reported for any dolphins, suggesting predation risk represents an important but varying influence thereon. This study provides a baseline for future investigations into the affect of predation risk on the behavioral ecology of these sympatric species.     

Morphology of the odontocete melon and its implications for acoustic function

Toothed whales (crown Odontoceti) are unique among mammals in their ability to echolocate underwater, using specialized tissue structures. The melon, a structure composed of fat and connective tissue, is an important component in the production of an echolocation beam; it is known to focus high frequency, short duration echolocation clicks. Here, we report on the morphology of the odontocete melon to provide a comprehensive understanding of melon structure across odontocete taxa. This study examined nine odontocete species (12 individual specimens), from five of the ten extant odontocete families. We established standardized definitions using computed tomography scans of the melon to investigate structure without losing geometric integrity. The morphological features that relate to the focusing capacity of the melon include internal density topography, melon size and shape, and relationship to other forehead structures. The potential for melon structure to act as a filter is discussed: establishing a lower limit to the frequency of sounds that can be propagated through the head. Collectively, the results of this study provide a robust, quantitative and comparative framework for evaluating tissue structures that form a key component of the echolocation apparatus.     

Blubber morphology in wild bottlenose dolphins (Tursiops truncatus) from the Southeastern United States: influence of geographic location, age class, and reproductive state

This study investigated blubber morphology and correlations of histological measurements with ontogeny, geography, and reproductive state in live, wild bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Surgical skin-blubber biopsies (N=74) were collected from dolphins during capture-release studies conducted in two geographic locations: Charleston, SC (N=38) and Indian River Lagoon, FL (N=36). Histological analysis of blubber revealed stratification into superficial, middle, and deep layers. Adipocytes of the middle blubber were 1.6x larger in Charleston subadults than in Indian River Lagoon subadults (4,590+/-340 compared to 2,833+/-335 microm2 per cell). Charleston subadult dolphins contained higher levels of total blubber lipids than Charleston adult animals (49.3%+/-1.9% compared to 34.2%+/-1.7%), and this difference was manifested in more adipocytes in the middle blubber layer (19.2+/-0.9 compared to 14.9+/-0.5 cells per field). However, dolphins from Indian River Lagoon did not exhibit this pattern, and the adipocyte cell counts of subadults were approximately equal to those of the adults (16.0+/-1.4 compared to 13.4+/-0.8 cells per field). The colder year-round water temperatures in Charleston compared to Indian River Lagoon may explain these differences. Adipocytes in the deep blubber layer were significantly smaller in lactating and simultaneously pregnant and lactating animals compared to pregnant dolphins (840+/-179, 627+/-333, and 2,776+/-586 microm2 per cell, respectively). Total blubber lipid content and adipocyte size in the deep blubber of mothers with calves decreased linearly with calf length. Lactating females may utilize lipids from the deep blubber during periods of increased energetic demands associated with offspring care. This study demonstrates that ontogeny, geography, and reproductive state may influence morphological parameters such as structural fiber densities and adipocyte numbers and sizes, measured in bottlenose dolphin blubber.     

LOW FREQUENCY NARROW-BAND SOUNDS PRODUCED BY BOTTLENOSE DOLPHINS

We present a new sound type recorded from bottlenose dolphins, Tursiops truncatus , in eastern Australian waters: low-frequency, narrow-band (LFN) harmonic sounds (defined as less than 2 kHz). Most of these sounds were of frequencies less than 1 kHz and were recorded commonly from socializing dolphins. These sounds differ significantly from narrow-band whistles, which are higher in frequency and longer in duration. The absence of these sounds in most studies of the acoustic behavior of bottlenose dolphins may reflect geographic differences in repertoires or result from insufficient sampling. Alternatively, these sounds may have been ignored where the focus of research was on other sound types.     

Why Do Dolphins Form Mixed‐Species Associations in the Azores?

Mixed‐species associations are temporary associations between individuals of different species that are often observed in birds, primates and cetaceans. They have been interpreted as a strategy to reduce predation risk, enhance foraging success and/or provide a social advantage. In the archipelago of the Azores, four species of dolphins are commonly involved in mixed‐species associations: the common dolphin, Delphinus delphis, the bottlenose dolphin, Tursiops truncatus, the striped dolphin, Stenella coeruleoalba, and the spotted dolphin, Stenella frontalis. In order to understand the reasons why dolphins associate, we analysed field data collected since 1999 by research scientists and trained observers placed onboard fishing vessels. In total, 113 mixed‐species groups were observed out of 5720 sightings. The temporal distribution, habitat (water depth, distance to the coast), behaviour (i.e. feeding, travelling, socializing), size and composition of mixed‐species groups were compared with those of single‐species groups. Results did not support the predation avoidance hypothesis and gave little support to the social advantage hypothesis. The foraging advantage hypothesis was the most convincing. However, the benefits of mixed‐species associations appeared to depend on the species. Associations were likely to be opportunistic in the larger bottlenose dolphin, while there seemed to be some evolutionary constraints favouring associations in the rarer striped dolphin. Comparison with previous studies suggests that the formation of mixed‐species groups depends on several environmental factors, and therefore may constitute an adaptive response.     

OBITUARIES

ABSTRACT

Prey often exhibit avoidance behaviors when predators are present. We observed diminished loudness of mating choruses of male silver perch Bairdiella chrysoura in spawning areas when vocalizing bottlenose dolphins Tursiops truncatus, which hunt fish acoustically, were present. Experimental playback of bottlenose dolphin sounds revealed that male silver perch mating calls were reduced by an average of 9 dB. This “acoustical avoidance” behavior, demonstrated previously for interactions involving bats hunting insects and frogs, may also be a common phenomenon in acoustically mediated predator-prey interactions in the sea.