Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii

Toothed whales use intense ultrasonic clicks to echolocate prey and it has been hypothesized that they also acoustically debilitate their prey with these intense sound pulses to facilitate capture. Cephalopods are an important food source for toothed whales, and there has probably been an evolutionary selection pressure on cephalopods to develop a mechanism for detecting and evading sound-emitting toothed whale predators. Ultrasonic detection has evolved in some insects to avoid echolocating bats, and it can be hypothesized that cephalopods might have evolved similar ultrasound detection as an anti-predation measure. We test this hypothesis in the squid Loligo pealeii in a playback experiment using intense echolocation clicks from two squid-eating toothed whale species. Twelve squid were exposed to clicks at two repetition rates (16 and 125 clicks per second) with received sound pressure levels of 199-226 dB re1 microPa (pp) mimicking the sound exposure from an echolocating toothed whale as it approaches and captures prey. We demonstrate that intense ultrasonic clicks do not elicit any detectable anti-predator behaviour in L. pealeii and that clicks with received levels up to 226 dB re1 microPa (pp) do not acoustically debilitate this cephalopod species.     

PORPOISE CLICKS FROM A SPERM WHALE NOSE—CONVERGENT EVOLUTION OF 130 KHZ PULSES IN TOOTHED WHALE SONARS?

ABSTRACT

Small toothed whales of the family Phocoenidae and delphinid genus Cephalorhynchus produce long-duration, narrowband biosonar clicks above 100 kHz, that might be seen as an adaptation for short range echolocation in shallow water. This paper presents data showing that the distantly related, and larger pygmy sperm whale Kogia breviceps (Kogiidae), that is a deep-diving, cephalopod-eating toothed whale, produce narrow-banded high frequency (NBHF) clicks identical to those of Phocoena and Cephalorhynchus (f₀ = 130 kHz, Q_3dB>10, duration > 80 msec). Thus, NBHF biosonar signals have evolved on three independent occasions in the odontocete suborder, but the apparent functional convergence does not relate to anatomical or niche similarity. Rather, it is suggested that a biosonar strategy adapting to a minimum in ocean ambient noise above 100 kHz in concert with high Q auditory filters have led to convergent evolution of the NBHF biosonar clicks. Since these biosonar signals carry all their energy at frequencies above the upper hearing limit of the killer whale Orcinus orca, predator avoidance may also have been a evolutionary shaping factor of the sonar signals from these non-whistling odontocetes.     

Echolocation behaviour adapted to prey in foraging Blainville's beaked whale (Mesoplodon densirostris)

Toothed whales echolocating in the wild generate clicks with low repetition rates to locate prey but then produce rapid sequences of clicks, called buzzes, when attempting to capture prey. However, little is known about the factors that determine clicking rates or how prey type and behaviour influence echolocation-based foraging. Here we study Blainville's beaked whales foraging in deep water using a multi-sensor DTAG that records both outgoing echolocation clicks and echoes returning from mesopelagic prey. We demonstrate that the clicking rate at the beginning of buzzes is related to the distance between whale and prey, supporting the presumption that whales focus on a specific prey target during the buzz. One whale showed a bimodal relationship between target range and clicking rate producing abnormally slow buzz clicks while attempting to capture large echoic targets, probably schooling prey, with echo duration indicating a school diameter of up to 4.3m. These targets were only found when the whale performed tight circling manoeuvres spending up to five times longer in water volumes with large targets than with small targets. The result indicates that toothed whales in the wild can adjust their echolocation behaviour and movement for capture of different prey on the basis of structural echo information.     

Hearing loss in stranded odontocete dolphins and whales

The causes of dolphin and whale stranding can often be difficult to determine. Because toothed whales rely on echolocation for orientation and feeding, hearing deficits could lead to stranding. We report on the results of auditory evoked potential measurements from eight species of odontocete cetaceans that were found stranded or severely entangled in fishing gear during the period 2004 through 2009. Approximately 57% of the bottlenose dolphins and 36% of the rough-toothed dolphins had significant hearing deficits with a reduction in sensitivity equivalent to severe (70-90 dB) or profound (>90 dB) hearing loss in humans. The only stranded short-finned pilot whale examined had profound hearing loss. No impairments were detected in seven Risso's dolphins from three different stranding events, two pygmy killer whales, one Atlantic spotted dolphin, one spinner dolphin, or a juvenile Gervais' beaked whale. Hearing impairment could play a significant role in some cetacean stranding events, and the hearing of all cetaceans in rehabilitation should be tested.     

Keeping returns optimal: gain control exerted through sensitivity adjustments in the harbour porpoise auditory system

Animals that use echolocation (biosonar) listen to acoustic signals with a large range of intensities, because echo levels vary with the fourth power of the animal's distance to the target. In man-made sonar, engineers apply automatic gain control to stabilize the echo energy levels, thereby rendering them independent of distance to the target. Both toothed whales and bats vary the level of their echolocation clicks to compensate for the distance-related energy loss. By monitoring the auditory brainstem response (ABR) during a psychophysical task, we found that a harbour porpoise (Phocoena phocoena), in addition to adjusting the sound level of the outgoing signals up to 5.4 dB, also reduces its ABR threshold by 6 dB when the target distance doubles. This self-induced threshold shift increases the dynamic range of the biosonar system and compensates for half of the variation of energy that is caused by changes in the distance to the target. In combination with an increased source level as a function of target range, this helps the porpoise to maintain a stable echo-evoked ABR amplitude irrespective of target range, and is therefore probably an important tool enabling porpoises to efficiently analyse and classify received echoes.     

Hearing sensation levels of emitted biosonar clicks in an echolocating Atlantic bottlenose dolphin

Emitted biosonar clicks and auditory evoked potential (AEP) responses triggered by the clicks were synchronously recorded during echolocation in an Atlantic bottlenose dolphin (Tursiops truncatus) trained to wear suction-cup EEG electrodes and to detect targets by echolocation. Three targets with target strengths of -34, -28, and -22 dB were used at distances of 2 to 6.5 m for each target. The AEP responses were sorted according to the corresponding emitted click source levels in 5-dB bins and averaged within each bin to extract biosonar click-related AEPs from noise. The AEP amplitudes were measured peak-to-peak and plotted as a function of click source levels for each target type, distance, and target-present or target-absent condition. Hearing sensation levels of the biosonar clicks were evaluated by comparing the functions of the biosonar click-related AEP amplitude-versus-click source level to a function of external (in free field) click-related AEP amplitude-versus-click sound pressure level. The results indicated that the dolphin's hearing sensation levels to her own biosonar clicks were equal to that of external clicks with sound pressure levels 16 to 36 dB lower than the biosonar click source levels, varying with target type, distance, and condition. These data may be assumed to indicate that the bottlenose dolphin possesses effective protection mechanisms to isolate the self-produced intense biosonar beam from the animal's ears during echolocation.     

Predation by killer whales (Orcinus orca) and the evolution of whistle loss and narrow-band high frequency clicks in odontocetes

A disparate selection of toothed whales (Odontoceti) share striking features of their acoustic repertoires including the absence of whistles and high frequency but weak (low peak-to-peak source level) clicks that have a relatively long duration and a narrow bandwidth. The non-whistling, high frequency click species include members of the family Phocoenidae, members of one genus of delphinids, Cephalorhynchus, the pygmy sperm whale, Kogia breviceps, and apparently the sole member of the family Pontoporiidae. Our review supports the 'acoustic crypsis' hypothesis that killer whale predation risk was the primary selective factor favouring an echolocation and communication system in cephalorhynchids, phocoenids and possibly Pontoporiidae and Kogiidae restricted to sounds that killer whales hear poorly or not at all (< 2 and > 100 kHz).     

Echolocation in Blainville’s beaked whales (Mesoplodon densirostris)

Here we use sound and movement recording tags to study how deep-diving Blainville’s beaked whales (Mesoplodon densirostris) use echolocation to forage in their natural mesopelagic habitat. These whales ensonify thousands of organisms per dive but select only about 25 prey for capture. They negotiate their cluttered environment by radiating sound in a narrow 20° field of view which they sample with 1.5–3 clicks per metre travelled requiring only some 60 clicks to locate, select and approach each prey. Sampling rates do not appear to be defined by the range to individual targets, but rather by the movement of the predator. Whales sample faster when they encounter patches of prey allowing them to search new water volumes while turning rapidly to stay within a patch. This implies that the Griffin search–approach–capture model of biosonar foraging must be expanded to account for sampling behaviours adapted to the overall prey distribution. Beaked whales can classify prey at more than 15 m range adopting stereotyped motor patterns when approaching some prey. This long detection range relative to swimming speed facilitates a deliberate mode of sensory-motor operation in which prey and capture tactics can be selected to optimize energy returns during long breath-hold dives.     

The Source Parameters of Echolocation Clicks from Captive and Free-Ranging Yangtze Finless Porpoises (Neophocaena asiaeorientalis asiaeorientalis)

The clicks of Yangtze finless porpoises (Neophocaena asiaeorientalis asiaeorientalis) from 7 individuals in the tank of Baiji aquarium, 2 individuals in a netted pen at Shishou Tian-e-zhou Reserve and 4 free-ranging individuals at Tianxingzhou were recorded using a broadband digital recording system with four element hydrophones. The peak-to-peak apparent source level (ASL__pp) of clicks from individuals at the Baiji aquarium was 167 dB re 1 μPa with mean center frequency of 133 kHz, -3dB bandwidth of 18 kHz and -10 dB duration of 58 μs. The ASL__pp of clicks from individuals at the Shishou Tian-e-zhou Reserve was 180 dB re 1 μPa with mean center frequency of 128 kHz, -3dB bandwidth of 20 kHz and -10 dB duration of 39 μs. The ASL__pp of clicks from individuals at Tianxingzhou was 176 dB re 1 μPa with mean center frequency of 129 kHz, -3dB bandwidth of 15 kHz and -10 dB duration of 48 μs. Differences between the source parameters of clicks among the three groups of finless porpoises suggest these animals adapt to their echolocation signals depending on their surroundings.     

Fossil Dolphin Otekaikea marplesi (Latest Oligocene,New Zealand) Expands the Morphological and Taxonomic Diversity of Oligocene Cetaceans

The Oligocene Epoch was a time of major radiation of the Odontoceti (echolocating toothed whales, dolphins). Fossils reveal many odontocete lineages and considerable structural diversity, but whether the clades include some crown taxa or only archaic groups is contentious. The New Zealand fossil dolphin “Prosqualodon” marplesi (latest Oligocene, ≥23.9 Ma) is here identified as a crown odontocete that represents a new genus, Otekaikea, and adds to the generic diversity of Oligocene odontocetes. Otekaikea marplesi is known only from the holotype, which comprises a partial skeleton from the marine Otekaike Limestone of the Waitaki Valley. Otekaikea marplesi was about 2.5 m long; it had procumbent anterior teeth, and a broad dished face for the nasofacial muscles implicated in production of echolocation sounds. The prominent condyles and unfused cervical vertebrae suggest a flexible neck. A phylogenetic analysis based on morphological features places Otekaikea marplesi in the extinct group Waipatiidae, within the clade Platanistoidea. The phylogeny implies an Oligocene origin for the lineage now represented by the endangered Ganges River dolphin (Platanista gangetica), supporting an Oligocene history for the crown Odontoceti.     

CONFERENCE REPORT

ABSTRACT

Sperm whale Physeter macrocephalus L. clicks have been studied for nearly fifty years, during which time great efforts have been made to understand the functions and production mechanisms of this sound. Other than clicks, sperm whales may also produce low intensity sounds arranged in short sequences, named trumpets, which have been recorded occasionally in the past by few groups of researchers. Sperm whale recordings collected in the Mediterranean Sea with a towed array and digital tags were used to describe the temporal and spectral characteristics of trumpets. This sound is made of a series of repeated units, around 0.2 s long, arranged in short sequences lasting between 0.6 s to 3.5 s. Each of these units comprises an amplitude modulated tonal waveform with a complex harmonic structure, and a spectrum composed of a low frequency component at 500 Hz and a mid-frequency component at 3 kHz. The apparent source level could be estimated for one of the trumpets and was estimated to be 172 dB_pp re: 1μPa at lm with energy flux density of 147 dB re: 1μ Pa²s.     

Highly Directional Sonar Beam of Narwhals (Monodon monoceros) Measured with a Vertical 16 Hydrophone Array

Recordings of narwhal (Monodon monoceros) echolocation signals were made using a linear 16 hydrophone array in the pack ice of Baffin Bay, West Greenland in 2013 at eleven sites. An average -3 dB beam width of 5.0° makes the narwhal click the most directional biosonar signal reported for any species to date. The beam shows a dorsal-ventral asymmetry with a narrower beam above the beam axis. This may be an evolutionary advantage for toothed whales to reduce echoes from the water surface or sea ice surface. Source level measurements show narwhal click intensities of up to 222 dB pp re 1 μPa, with a mean apparent source level of 215 dB pp re 1 μPa. During ascents and descents the narwhals perform scanning in the vertical plane with their sonar beam. This study provides valuable information for reference sonar parameters of narwhals and for the use of acoustic monitoring in the Arctic.     

Click-based echolocation in bats: not so primitive after all

Echolocating bats of the genus Rousettus produce click sonar signals, using their tongue (lingual echolocation). These signals are often considered rudimentary and are believed to enable only crude performance. However, the main argument supporting this belief, namely the click’s reported long duration, was recently shown to be an artifact. In fact, the sonar clicks of Rousettus bats are extremely short, ~50–100 μs, similar to dolphin vocalizations. Here, we present a comparison between the sonar systems of the ‘model species’ of laryngeal echolocation, the big brown bat (Eptesicus fuscus), and that of lingual echolocation, the Egyptian fruit bat (Rousettus aegyptiacus). We show experimentally that in tasks, such as accurate landing or detection of medium-sized objects, click-based echolocation enables performance similar to laryngeal echolocators. Further, we describe a sophisticated behavioral strategy for biosonar beam steering in clicking bats. Finally, theoretical analyses of the signal design—focusing on their autocorrelations and wideband ambiguity functions—predict that in some aspects, such as target ranging and Doppler-tolerance, click-based echolocation might outperform laryngeal echolocation. Therefore, we suggest that click-based echolocation in bats should be regarded as a viable echolocation strategy, which is in fact similar to the biosonar used by most echolocating animals, including whales and dolphins.     

Odontocete occurrence in relation to changes in oceanography at a remote equatorial Pacific seamount

Seamounts are considered hot spots of biodiversity and can aggregate pelagic predators and their prey. Passive acoustic monitoring was conducted over 3 mo in 2012 to document the occurrence of odontocetes near a seamount chain in the central equatorial Pacific in relation to oceanographic changes over time. Beaked whale echolocation signals were most frequently encountered. The main beaked whale signal was an unknown type, BW38, which resembled signals produced by Blainville's beaked whales. It had high occurrence during high sea surface temperature and low sea surface salinity. Cuvier's beaked whales were the second most detected. They had an opposite pattern and were encountered more often when sea surface temperature was low and net primary productivity was high. Risso's dolphins and short‐finned pilot whales had high acoustic densities, and echolocated predominantly at night. Risso's dolphins occurred more often during low sea surface height deviation. False killer whales were less frequently detected and mostly occurred during the day. Sperm whale detections were fewer than expected and associated with high chlorophyll a. Short duration Kogiidae encounters occurred on average every third day. These types of long‐term site studies are an informative tool to comparatively assess species composition, relative abundance, and relationship to oceanographic changes.     

To See or Not to See: Investigating Detectability of Ganges River Dolphins Using a Combined Visual-Acoustic Survey

Detection of animals during visual surveys is rarely perfect or constant, and failure to account for imperfect detectability affects the accuracy of abundance estimates. Freshwater cetaceans are among the most threatened group of mammals, and visual surveys are a commonly employed method for estimating population size despite concerns over imperfect and unquantified detectability. We used a combined visual-acoustic survey to estimate detectability of Ganges River dolphins (Platanista gangetica gangetica) in four waterways of southern Bangladesh. The combined visual-acoustic survey resulted in consistently higher detectability than a single observer-team visual survey, thereby improving power to detect trends. Visual detectability was particularly low for dolphins close to meanders where these habitat features temporarily block the view of the preceding river surface. This systematic bias in detectability during visual-only surveys may lead researchers to underestimate the importance of heavily meandering river reaches. Although the benefits of acoustic surveys are increasingly recognised for marine cetaceans, they have not been widely used for monitoring abundance of freshwater cetaceans due to perceived costs and technical skill requirements. We show that acoustic surveys are in fact a relatively cost-effective approach for surveying freshwater cetaceans, once it is acknowledged that methods that do not account for imperfect detectability are of limited value for monitoring.     

The modulation rate transfer function of a harbour porpoise (Phocoena phocoena)

During echolocation, toothed whales produce ultrasonic clicks at extremely rapid rates and listen for the returning echoes. The auditory brainstem response (ABR) duration was evaluated in terms of latency between single peaks: 5.5 ms (from peak I to VII), 3.4 ms (I–VI), and 1.4 ms (II–IV). In comparison to the killer whale and the bottlenose dolphin, the ABR of the harbour porpoise has shorter intervals between the peaks and consequently a shorter ABR duration. This indicates that the ABR duration and peak latencies are possibly related to the relative size of the auditory structures of the central nervous system and thus to the animal’s size. The ABR to a sinusoidal amplitude modulated stimulus at 125 kHz (sensitivity threshold 63 dB re 1 μPa rms) was evaluated to determine the modulation rate transfer function of a harbour porpoise. The ABR showed distinct envelope following responses up to a modulation rate of 1,900 Hz. The corresponding calculated equivalent rectangular duration of 263 μs indicates a good temporal resolution in the harbour porpoise auditory system similar to the one for the bottlenose dolphin. The results explain how the harbour porpoise can follow clicks and echoes during echolocation with very short inter click intervals.     

Anisakis spp. in toothed and baleen whales from Japanese waters with notes on their potential role as biological tags

In this study, Anisakis nematodes isolated from toothed and baleen whales from localities around Japan were molecularly (PCR-RFLP) identified. In Wakayama, common bottlenose dolphins (Tursiops truncatus) were infected with A. simplex sensu stricto (s.s.), A. typica and A. pegreffii, while A. typica was the only species found in pantropical spotted dolphin (Stenella attenuata) and striped dolphin (S. coeruleoalba). Offshore common minke whales (Balaenoptera acutorostrata) and sei whales (B. borealis) were almost exclusively infected with A. simplex s.s.. However, in common minke whales from two Hokkaido localities, mature worms mostly consisted of A. simplex s.s. in some individuals and of A. pegreffii in others, but immature worms were mainly A. simplex s.s.. Gross and histopathological examination on gastric mucosa attached by anisakids resulted in mild and superficial reactions by the two baleen whale species in contrast to severe inflammatory reaction associated with ulcer formations by common bottlenose dolphin. Host specificity and adaptability of Anisakis spp. in these baleen and toothed whales were discussed from the points of view of adult worm size, worm population and pathological reactions by hosts. Interestingly, most of the common minke whales predominantly harboring mature A. pegreffii adults belonged to the Yellow Sea – East China Sea stock (J stock), which migrates through the Sea of Japan, whereas most of those mainly parasitized by mature A. simplex s.s. adults were from the Okhotsk Sea – West Pacific stock (O stock), mostly inhabiting the Pacific side, suggesting that these sibling species may have utility as biological tags to differentiate whale stocks. These results represent the first definitive host records for A. pegreffi in the Northwestern Pacific Ocean.     

The beluga whale produces two pulses to form its sonar signal

Odontocete cetaceans use biosonar clicks to acoustically probe their aquatic environment with an aptitude unmatched by man-made sonar. A cornerstone of this ability is their use of short, broadband pulses produced in the region of the upper nasal passages. Here we provide empirical evidence that a beluga whale (Delphinapterus leucas) uses two signal generators simultaneously when echolocating. We show that the pulses of the two generators are combined as they are transmitted through the melon to produce a single echolocation click emitted from the front of the animal. Generating two pulses probably offers the beluga the ability to control the energy and frequency distribution of the emitted click and may allow it to acoustically steer its echolocation beam.     

Geographic differences in Blainville's beaked whale (Mesoplodon densirostris) echolocation clicks

Aim

Understanding cetacean species' distributions and population structure over space and time is necessary for effective conservation and management. Geographic differences in acoustic signals may provide a line of evidence for population-level discrimination in some cetacean species. We use acoustic recordings collected over broad spatial and temporal scales to investigate whether global variability in echolocation click peak frequency could elucidate population structure in Blainville's beaked whale (Mesoplodon densirostris), a cryptic species well-studied acoustically.

Location

North Pacific, Western North Atlantic and Gulf of Mexico.

Time period

2004–2021.

Major taxa studied

Blainville's beaked whale.

Methods

Passive acoustic data were collected at 76 sites and 150 cumulative years of data were analysed to extract beaked whale echolocation clicks. Using an automated detector and subsequent weighted network clustering on spectral content and interclick interval of clicks, we determined the properties of a primary cluster of clicks with similar characteristics per site. These were compared within regions and across ocean basins and evaluated for suitability as population-level indicators.

Results

Spectral averages obtained from primary clusters of echolocation clicks identified at each site were similar in overall shape but varied in peak frequency by up to 8 kHz. We identified a latitudinal cline, with higher peak frequencies occurring in lower latitudes.

Main conclusions

It may be possible to acoustically delineate populations of Blainville's beaked whales. The documented negative correlation between signal peak frequency and latitude could relate to body size. Body size has been shown to influence signal frequency, with lower frequencies produced by larger animals, which are subsequently more common in higher latitudes for some species, although data are lacking to adequately investigate this for beaked whales. Prey size and depth may shape frequency content of echolocation signals, and larger prey items may occur in higher latitudes, resulting in lower signal frequencies of their predators.     

No deep diving: evidence of predation on epipelagic fish for a stem beaked whale from the Late Miocene of Peru

Although modern beaked whales (Ziphiidae) are known to be highly specialized toothed whales that predominantly feed at great depths upon benthic and benthopelagic prey, only limited palaeontological data document this major ecological shift. We report on a ziphiid–fish assemblage from the Late Miocene of Peru that we interpret as the first direct evidence of a predator–prey relationship between a ziphiid and epipelagic fish. Preserved in a dolomite concretion, a skeleton of the stem ziphiid Messapicetus gregarius was discovered together with numerous skeletons of a clupeiform fish closely related to the epipelagic extant Pacific sardine (Sardinops sagax). Based on the position of fish individuals along the head and chest regions of the ziphiid, the lack of digestion marks on fish remains and the homogeneous size of individuals, we propose that this assemblage results from the death of the whale (possibly via toxin poisoning) shortly after the capture of prey from a single school. Together with morphological data and the frequent discovery of fossil crown ziphiids in deep-sea deposits, this exceptional record supports the hypothesis that only more derived ziphiids were regular deep divers and that the extinction of epipelagic forms may coincide with the radiation of true dolphins.