chapter 6: vocal anatomy, acoustic communication, and echolocation

graded calls - not exactly definite …

communication

• simple communication: in organisms that lack a nervous system, without cognitive abilities, e.g. bacteria

• non-informative communication: lack of cognition, e.g. tungara frogs

• passive communication: swim movement, splashes, exhaling, bubbles, flipper strokes

• auto-communication: echolocation

• informative communication: including cognition: alarm calls, waggel dance, language, but also aerial displays like breaching in humpback whales

complex communication

• Groups with complex social systems require more complex communication systems. group size, social networks, and pair bonds in societies

Acoustic communication in the sea

• acoustic sensory modality is favoured:

  • speed of sounds approx. 5 times faster than in air, 1500 m/s (air 340 m/s)

  • compared to light, which only travels 100 m in water - 10 km in air

  • sound travels > 100 km in water - 1 km in air

sound production/vocal anatomy

sound production in marine mammals

aquatic marine mammals

• (cetaceans, sirenians, phocids, walrus) specialised in sound communication and exploration of sea

• = 2-3x more auditory versus optic nerve fibres (than land mammals)

semi-aquatic marine mammals

• (otariids, sea otter, polar bear) communicate mainly in air but phocids in air and underwater

sound production larynx

• pinnipeds (figure below)

  • well developed larynx, used for repsiration and sound production

• differences between

  • species

  • males/females

  • young/older individuals

  • adaptations for diving

• cetaceans: mysticetes unusual laryngeal sac - diverticulum: resonator for sound production

• odontocetes have beak like structure - separated respiratory tract from mouth and esophagus

• blue whale - sound resonator:

  • in Mysticeti, the skull is modified to accommodate palatal baleen plates as a feeding adaptation

    • unusual laryngeal sac (diverticulum) and nasal passages act as resonator

    • auditory bullae of mysticeti are wedged against the skull

    • bone and soft tissue conduction of low-frequency sound

    • two blow holes

dolphin - larynx

• toothed whales: different than terrestrials - artenoid and eppiglottal cartilages elongated to beak-like structure, which separates the respiratory tract from the mouth/oesophagus - reduces risk of choking: breath and swallow at same time

• dolphins may produce sounds also in larynx for communication

• but most sound production in nasal passages

sound production odontocetes

• the skull of odontoceti is shaped is shaped to accommodate a melon (or junk in sperm in whale), facial muscles, the monkey lips/dorsal bursae (MLDB) complex, and nasal sacs for directional sound generation associated with echolocation and social interaction

• only one blow hole

• the bullae are not fused to the skull but suspended in a spongy mucosa (peripullar plexus) by ligaments - no bone conduction

dolphins nasal passage

• whistles, calls and click are produced in head by bilaterally MLDB and nasal sacs in soft tissue nares

• air is forced between a pair of MLDB - rapidly open and close (vibrate) → produce sounds (clicks and whistles)

• the phonic lips are two parallel ridges of transverse, keratinized tissue with fine grooves that direct flow into the vestibular air space for recycling (i.e. not expelled through the nares)

• airflow is under voluntary control - variety of sounds is possible

• the two MLDBs can function independently → two different sounds simultaneously (= two voced calls)

• also clicks are produced independently from whistles

• the melon contains lipids that are impedance-matched to sea water - sounds are produced by air moving past the vibrating monkey lips acoustically separated form the melon, which focuses and directs sounds into water.

• higher frequencies are more focused than lower frequencies

sound production sperm whales

• loudest sound in animal kingdom

• junk homologous to melon

• spermaceti organ like right posterior dorsal bursa in other odontoceti

• single pair of phonic lips located in right nasal passage beneath blowhole

• produces high-intensity sonic clicks (400 hz to 15khz and up to 235 db)

• clicks several paths in head:

  • part of sound - put the front of the head, remainder travels backward through spermaceti organ to air sac adjacent to skull reflected back through the junk - focuses the beam out the front of the head

    • part of this sound beam is reflected a 2nd time by distal air sac at front of the head

    • it travels 2nd time to frontal air sac - reflected through junk - out the front of the head

• hunting and prey detection, clicks 1-2s intervals - increase in repetition → whale approaches potential prey at very close range, repetition rate so fast that individual clicks cannot be distinguished (buzzing, → creak

sound production pinnipeds

• pinniped vocalizations are sonic, diverse and vary by species, sex, age and season - social communication

• in air - often roars, growl, barks, snorts, whimpers, and whistles - exhaling through larynx, vocalizations → pursed lips or nostrils

• underwater vocalizations - moving air between the lungs and oharynx, which causes membranes in trachea to vibrate without expelling air through the mouth or nostrils

• there is sound variation between species:

  • larynx, two voiced, movements in mouth and tongue, lips (whistle/walrus), pharangyeal sac in their necks (gong/walrus)

  • phocids: tracheal mechanisms, vocal folds (weddel seals)

  • vibration of dorsal tracheal membrane (bearded seals)

  • air sacs on right side (ribbon seals)

• hooded seals: inflatable nasal hood and septum (balloon): visual and acoustic display

sound production sirenians

• sirenians - vocal folds in larynx → variety of sonic vocalization

  • manatee class (e.g., chirp-squeaks, squeals, and creams)

    • 0.5-18 khz

    • peak frequencies of 1-8 khz social communication and mother calf recognition

    • sounds are acoustically coupled to the water through fat pads in the neck

  • dugong calls (chirp-squeaks, barks, and trills)

    • frequency range of 2-18 khz

    • peak frequencies of 1-8 khz

sound production sea otter and polar bears

• polar bear: laryngeeal mechanisms of terrestrial mammals, lip vibration - no underwater vocalisations

• sea otters - no underwater vocalisation

  • aerial vocalizations short - range communication (e.g. scremas, whistles, whines, hisses, snarls, coos, grunts, squeals, squeaks)

  • new-bord pups routinely - high-frequency cry in distress or seeking attention

  • adults produce hih-intensity long distances (up to 1 km) screams, when distressed or female / pup separated

  • territorial males produce high-intenisty screams when interacting with females

echolocation

• autocommunication

  • signals/sounds are sent out to create a returning echo form obstacles

    • echo is transformed in auditory cortex into map

    • information about location, size, and composition of the environment / prey

  • mostly high frequency clicks and sweeps

  • animals explore and orient in dark environments

  • animals: bats, odontocetes, shrews, birds ( swiftlets and oilbirds)

bottlenose dolphin

• first studies by Witlow Au (1993) described accurate echolocation by bottlenose dolphins using high-frequency clicks

• narrow sonar beam - directional click to detect small objects

• high frequency clicks (>100khz) broad-band (30-40 lhz), high oeak (> 220 db) short (50-80 µs)

• detection range 72 m, detection size 2.5 cm

• brain is capable of very rapid auditory processing, integrating 0.25 ms interval inputs

• inter click interval (ICI) equals round trip and lag time: wait for echo to return and process before emitting new signal

• search (ICI) internvals slow and regularly - when closing in on target ICI intervals are shorter - buzz

• ICI = RT (round trip - echo) + LT (lag time / processing time, targets 20-12 m → LT 19—45 ms)

special cases

• belugas ICI’s less than return time: process whole click trains in brain

• porpoises 5-10x longer (150-600 µs) but half bandwidth (10-20 khz), less loud (150-170db), very high frequencies (above 100 khz), inner ears that are specialized for high frequency audition

sperm whale

• clicks lower frequency (8 khz), detect bottom and squid at depth > 400m

Mysticetes ?

• low frequency echolocation?

• bowhead whales use echoes from calls to detect ice obstacle

do seals use echolocation?

• experiments with captive hooded and harp seals showed some high frequency clicks but echolocation was not proven

• instead found cod clicks

vocal communication and vocal learning

vocal repertoires (VR)

• what is a vocal repertoire?

  • it refers to the range and variety of sounds an animal species or individual is able to produce for communication

  • it can be in the form of clicks, whistles, or moans, sometimes specific calls with patterns

• what do specific calls mean?

• how many kinds of utterances and calls are there? what do they sound/look like?

• challenges of large data sets of analysis with vocal repertoires: example: Norwegian pilot whales and norwegina killer whales (vester PhD 2017)

VR driving factors

• phylogeny, habitat; geographical separation; sexual selection; predator pressure

• social complexity hypothesis of communication

  • “groups with complex social systems require more complex communication system”

  • group size, social networks and pair bonds in societies

• context: e.g. food association calls, manipulation / arousal / information about food

VR driving factors in the sea

• habitat: favourable sound transmissions in the sea versus air

  • speed of sound 1500 m/s (340 m/s), transmission loss 60 times less, low light conditions

• echolocation development in toothed whales

• social whales: large and complex group structures

  • large repertoires: signature whistles bottlenose dolphins

    • complex repertoires:

      • sperm whale codas

      • humpback whale songs

      • killer whale dialects

form calls to repertoires - acoustic structures

• vocal classes - spectrogram: clicks, pulsed calls, whistles, other calls distinguished by their frequency harmonics, sidebands, noisy parts, etc.

• problems with naming - often arbitrary and anthropocentric

• but vocalisations are context. and situation dependent: coarse behavioural categories such as feeding, socialising, travelling; these give rough vocalisation patters - fine scale behaviour needed but difficult to observe underwater (drones and D-tags give new data possibilities)

• long distance calls are loud, stereo typed, simple structure, repetitive and temporally patterned (rhythm, strong ordering) - low frequency calls of fin whales and blue whales suited to travel thousands of kilometers

• short range signals - acoustically more complex, encode information through subtle variations - multimodal: information to receiver, distance, direction, identity, experience…

• repetition or increased amplitude and frequency against noise

• syntactical rules in humpback whale songs:

  • “song drift” or cultural evolution of whale songs → the shape and pitch (frequency) of the phrases changes gradually year by year, even though the over structure (duration and rhythm) remains fairly consistent.

  • these vocal patterns show syntax, repetition, and gradual changes

  • the same phrase type progressively year to year. Each year’s song builds on the previous one, creating a slow cultural drift in the population’s song

  • the spectrograms are a visual representation of how a specific humpback whale song phrase evolves over 5 years.

  • the phrase stays recognizable, but gradually shifts in frequency and structure, demonstrating how cultural transmission and vocal learning shape whale song over time.

  • this applies to the whole population. the song kind of gets remixed

individual differences in marine mammals vocalisation

• differences in vocal tracts lead to vocal differences “voice cues” but underwater high pressure changes vocal signals - need for vocal control and vocal learning in marine mammals

• vocal learning is well documented for odontocetes, myticetes and pinnipeds

• but there are also differences due to geographical separation, or sex and age related

• examples:

  • acoustic mimicry:

    • a captive beluga whale was able to mimic the voice of its trainer, confusing people around it

  • vocal learning:

    • dialects of resident orcas in BC

    • signature whistles in bottlenose dolphins

    • humback whale song

    • geographical variances: most seals

    • humpback songs = reflects cultural change

VR odontocetes

• odontoceti produce species-specific, frequency-modulated sonic and ultrasonic sounds such as whistles (1-120 khx), pulsed sounds “calls” (1-60 khz) and click (10-300 khz) for communication and echolocation

VR types

whistles

• tonal whistles: variable structures all dolphins

• stero-typed whistles: re-occuring stable structure bottlenose dolphins, all dolphins

• ultrasonic whistles: main energy 20-60 khz (>90 khz) killer whales and long-finned pilot whales

stereo-typed pulsed calls

• tonal calls, simple to complex calls

• combination of calls

• two voiced calls

  • a type of vocalisation where the animals produces two different sounds simultaneously, often at different frequencies.

  • dolphins and some whales have two sets of sound producing structures in their nasal passages called phonic lips. these can work independently, allowing the animal to produce two distinct tones at once.

• distinct calls (e.g. signature whistles, dialects)

pulsed calls

• variations of call- graded information may carry information on emotional state, alertness, excitement, hierarchy, danger, food…

• other calls without distinct structures such as buzzes, grunts, squeaks

combination of calls and other utterances

• calls are oten compromised as patterned combinations (weddel seals, humpback whale songs, pilot whales…) and often combined with other displays (e.g. hooded seals, jaw clapping dolphins…)

• killer whale call type combinations:

call types/sub-types

• Norwegian killer whales: 88 call types, 36 sub types

• norwegian long-finned pilot whale: 129 call types, 25 subtypes

combination of call types

• pilot whale call combinations

  • graded vocalisations and distinct structures

clicks

• main vocalisation

  • echolocation

  • but also communication

  • buzzes - e.g. killer whales

    • help to herd herring?

    • part of calls

• not well studied

• sperm whales examples of “click communication”

  • echolocation clicks

  • clusters (3-20) of clicks called codas - social communication, reflect dialects of female groups

  • large males make a “slow click” or “clang” to announce themselves to female groups

vocal repertoires - context

group signature - dialects

• sperm whale codas - context sensitive and combinatorial vocalisation

  • clans have their own set of codas

• killer whale group dialects: in Canada, each group has its own call type set, related groups share call types

  • avoid inbreeding

• pilot whale group dialects: first results show group specific call types but under investigation

communication - dolphin groups

• recognition of the individual signature whistles

• new borns learn mothers signature whistle (SW), within 3 months develop their own SW

  • announce themselves

  • addressed by others

  • used in the absence of the owner of the SW

communication - behavioural context

• Norwegian killer whales: salmon feeding and carousel feeding

  • carousel feeding:

    • it is when (in this scenario killer whales) a group of orcas swims in circles around a school of fish, driving them into a dense, rotating ball called a bait ball, near the surface or against the shore

    • some orcas may blow bubbles or slap the surface of the water to keep the fish disoriented and confined.

    • the orcas then take turns swimming through the bait ball to eat, usually in an organized manner, hence the name carousel

    • this method requires high levels of coordination and social communication among group members

• icelanding carousel feeding orcas similar to Norwegian orcas

• mother-calf communication

  • contact calls

  • distress calls

  • mother contact call for calves in long finned pilot whales

• male-male competition

  • aggressive calls

  • distress calls

  • often accompanied with aerial displays such as clapping, inflated hoods, jaw claps, etc

vocal repertoires mysticetes

• they produce a variety of amplitude-and frequency modulated calls-moans, growls, or simple songs

• frequency range is 7 hz in the blue whale to 24 khz in humbpack whale songs

communication - long distance

• sounds that have wavelength longer than the whale and maybe used for long-distance (thousands of km) communication

  • fin whale and blue whale low frequency calls travel more than 1000 km

  • signals are loud, stereotypes, spectrally simple, long repetitive, and temporally patterned = shaped by sexual selection (complex)

noise pollution

communication - conservation

• most marine mammals only visible 1-10% at surface = acoustic monitoring useful tool to estimate distribution and abundance

• man made noise can interfere and become a problem for marine mammals

• in the past 50 years, there has been an increase in the noise in the ocean 20 x

• seismic surveys, noise from boat traffic