REVIEW Voices of the past: a review of Paleozoic and ...

REVIEW

Voices of the past: a review of Paleozoic and Mesozoic animal sounds

Phil Senter*

Department of Natural Sciences, Fayetteville State University, 1200 Murchison Road, Fayetteville, NC 28301, USA

(Received 10 March 2009; final version received 6 May 2009)

Here, I present a review and synthesis of fossil and neontological evidence to find major trends in the pre-Cenozoic evolutionof animal acoustic behaviour. Anatomical, ecological and phylogenetic data support the following scenario. Stridulatinginsects, including crickets, performed the first terrestrial twilight choruses during the Triassic. The twilight chorus wasjoined by water boatmen in the Lower Jurassic, anurans in the Upper Jurassic, geckoes and birds in the Lower Cretaceous,and cicadas and crocodilians in the Upper Cretaceous. Parallel evolution of defensive stridulation took place multiple timeswithin Malacostraca, Arachnida and Coleoptera. Parallel evolution of defensive and courtship-related sound productiontook place in Actinopterygii, possibly as early as the Devonian. Defensive vocalisations by tetrapods probably did notappear until their predators acquired tympanic ears in the Permian. Tympanic ears appeared independently inDiadectomorpha, Seymouriamorpha, Parareptilia, Diapsida and derived Synapsida. Crocodilians and birds acquired vocalorgans independently, and there is no anatomical evidence for vocal ability in bird-line archosaurs basal to the avian cladeOrnithothoraces. Acoustic displays by non-avian dinosaurs were therefore probably non-vocal. Other aspects of theevolution of acoustic behaviour in these and other lineages are also discussed.

Keywords: acoustic behaviour; vocalisation; hearing; Crustacea; Insecta; Orthoptera; Coleoptera; Hemiptera; Crocodylia;Aves; Mammalia

Introduction

The fossil record does not include audio recordings. As a

result, few researchers lose sleep over such questions as

whether Triceratops heard crickets chirping in the evening,

whether Mesozoic treetops resounded with birdsong or

frogsong, or whether the immense corpses of sauropods

were surrounded by the buzzing of bottle flies. Questions

such as these seem silly at first but are nevertheless

worthwhile to ask for three reasons: (1) inferable acoustic

details must be included if the paleontologist is to

accomplish one of paleontology’s main goals: the

reconstruction of the ancient world in as much detail as

possible, (2) acoustic signals are of great importance to

many animals, so the reconstruction of the lifestyles of

ancient organisms must take acoustic signals into

consideration, and (3) many studies have addressed

whether or not extinct animals could hear (e.g. Reisz

1981; Wu 1994; Clack and Allin 2004), so it is reasonable

to ask what they heard.

Bioacoustics, the study of animal sound production

and reception, is a rich field with much to offer the

paleontologist for application to the study of sound

production and reception in fossil animals. Such

application could aptly be called paleobioacoustics. Thus

far, most paleobioacoustical research has been concen-

trated on the study of the evolution of hearing in tetrapod

vertebrates (e.g. Reisz 1981; Allin 1986; Wu 1994; Clack

and Allin 2004; Vater et al. 2004) and the evolution of

sound production in the insect orders Orthoptera and

Hemiptera (e.g. Sweet 1996; Rust et al. 1999; Bethoux and

Nel 2002; Gorochov and Rasnitsyn 2002). However, many

other paleobioacoustical issues can be addressed with

available data from fossil and neontological evidence. For

example, the first appearances of fossils of sound-

producing taxa can be used to constrain the times of

origin of their characteristic sounds. Also, knowledge of

directional selection on extant animal sounds can be used

to infer characteristics of the sounds produced by their

ancestors. In addition, because the functions of animal

sounds depend on their reception by the intended

recipients, information on the evolution of hearing can

be used to constrain the times of origin of certain animal

sounds. For example, one can reasonably infer that certain

courtship sounds, territorial sounds and other sounds

directed at conspecifics were absent in taxa that lacked

appropriate sensory structures. Similarly, one can also

reasonably infer that certain anti-predator sounds were

absent before the appearance of predators with appropriate

sensory structures. Much information pertinent to the

ISSN 0891-2963 print/ISSN 1029-2381 online

q 2008 Taylor & Francis

DOI: 10.1080/08912960903033327

http://www.informaworld.com

*Email: [email protected]

Historical Biology

Vol. 20, No. 4, December 2008, 255–287

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reconstruction of ancient acoustic behaviour has been

published, but before now no attempt has been made to

pool available information to illuminate broad trends in

such behaviour across large geologic time spans. Here,

I present a review of the available literature so as to

perform such a synthesis for the Paleozoic and Mesozoic

Eras.

Major themes in the evolution of aerial soundproduction and reception

Sound reception

Most invertebrates are aquatic, and several lineages have

independently evolved sense organs that perceive water

displacement (Budelmann 1992a,b; Coffin et al. 2004).

However, it is difficult to say whether most possess a true

sense of hearing, both because the definition of ‘hearing’

varies among researchers and because in aquatic environ-

ments the distinctions between sound, vibration and water

flow are blurred (Budelmann 1992b). In any case, among

extant invertebrates acoustic communication is unknown

outside Arthropoda, and there is no reason to believe that the

case was different among extinct invertebrates.

Airborne sound reception is typically accomplishedwith

tympanic ears. In such ears airborne sounds cause vibrations

in a thin membrane, the tympanum (Figure 1), internal to

which is an air-filled chamber; mechanoreceptors that are

linked to the tympanum detect its movement in response to

sounds (Wever 1978; Yager 1999; Kardong 2006). Among

insects, tympanic ears have appeared independently in

Cicadidae (cicadas), Corixidae (water boatmen), Tachinidae

(tachinid flies), Sarcophagidae (flesh flies), Neuroptera

(lacewings), Mantodea (mantises), Cicindelidae

(tiger beetles), Scarabaeidae (scarab beetles), and several

times within Orthoptera (crickets and grasshoppers) and

Lepidoptera (moths and butterflies) (Yager 1999; Flook et al.

2000; Robert and Hoy 2000; Cokl et al. 2006) (Figure 2).

Tympanic ears in cicadas, water boatmen and crickets are

associated with intraspecific acoustic communication

(Bailey 1991; Gerhardt and Huber 2002; Cokl et al. 2006).

Those of tachinid and flesh flies are used to find their cricket

hosts when the latter stridulate (Yager 1999; Robert andHoy

2000). The tympanic ears of lepidopterans, lacewings,

mantises, beetles and grasshoppers are tuned to frequencies

produced by echolocating bats (Mammalia: Chiroptera), the

sounds of which stimulate evasive behaviours in these

insects (Bailey 1991; Yager 1999; Flook et al. 2000). Such

ears are an evolutionary response to predation by bats

(Bailey 1991; Flook et al. 2000) and, like bats, were

therefore absent before the Cenozoic. Courtship sounds of

grasshoppers and lepidopterans are secondary and appeared

after the advent of tympanic hearing in those taxa (Yager

1999), and were therefore absent before the Cenozoic.

In addition to receptors attuned to frequencies used in

intraspecific communication, some cricket ears also have a

Figure 1. Sound production (A–D) and reception (E–H)devices of extant animals. (A) Left cheliped of male ghost crab(Ocypode quadrata), ventral view, showing sound-producingstridulatory structures. (B) Male cicada (Pomponia intermedia)with wings and operculum (exoskeletal covering of tymbal)removed to show sound-producing tymbal. (C) Sagittallysectioned larynx of late-term fetal pig (Sus scrofa) in medialview, showing sound-producing laryngeal vocal cord andlaryngeal cartilages mentioned in text, with edges of airwayoutlined with broken line. (D) Female katydid (Siliquoferagrandis), showing tibial tympanum for reception of airbornesound. (E) Head of toad (Bufo americanus), left dorsolateralview, showing tympanum for reception of airborne sound. (F)Skull of turtle (Trachemys scripta), showing posterior skull

P. Senter256


small number of acoustic receptors for much higher

frequencies produced by echolocating bats (Imaizumi and

Pollack 1999) (Figure 3), a secondary innovation that

presumably appeared after the Cenozoic appearance of bats.

In tetrapod vertebrates with tympanic ears, a bony

connection transmits vibrations from the tympanum to the

inner ear, where resulting fluid vibrations stimulate

mechanoreceptors (Wever 1978; Kardong 2006). This

mechanism appeared independently in Anura (frogs and

toads), Diapsida (lizards, crocodilians, birds and kin)

and Synapsida (mammals and kin) (Clack and Allin 2004),

and apparently also in the extinct tetrapod groups

Seymouriamorpha (Ivakhnenko 1987), Diadectomorpha

(Berman et al. 1992) and Parareptilia (Laurin and Reisz

1995) (Figure 4). Whether the tympanic ears of turtles

(Testudines) appeared independently depends on whether

or not turtles arose from within Diapsida or Parareptilia, an

issue that is disputed (e.g. Rieppel and deBraga 1996; Lee

1997a,b). Osteological evidence, reviewed later in this

embayment and stapes; the embayment houses an air-filled spaceinternal to the tympanum, which is attached to the rim of theembayment, and the stapes conducts auditory vibrations from thetympanum to the inner ear. (G) Skull of snake (Boidae,undetermined species), showing stapes and loosely attachedquadrate bone; the quadrate acts as a tympanum, and the stapes(attached to the quadrate via a cartilaginous extension that is notshown here) conducts auditory vibrations from the quadrate tothe inner ear. ac, arytenoid cartilage; cc, cricoid cartilage; e,embayment; f, file; q, quadrate; s, scraper; st, stapes; t,tympanum; tc, thyroid cartilage; v, vocal cord.

R

Figure 2. Phylogeny of insect orders, after Grimaldi and Engel (2005) showing distribution of sound production and tympanic ears(Dumortier 1963b; Aiken 1985; Yager 1999; Virant-Doberlet and Cokl 2004; Drosopoulos and Claridge 2006). Large symbols indicatewide taxonomic distribution within an order, and small symbols indicate limited taxonomic distribution. Filled circles and squaresindicate occurrence within a family or families with known pre-Cenozoic fossil records. A, expulsion of air through spiracles; B, loudflight buzzing; P, percussion of body parts against substrate; S, stridulation; T, tymbals; t, tympanic ears; W, wing fluttering.

Historical Biology 257


paper, indicates the presence of tympanic ears in all these

groups before the Cenozoic, and in most cases before the

Mesozoic. As with many insect taxa, it is possible that the

original function of tympanic hearing in the various

tetrapod taxa was predator avoidance. The sounds made by

the approach of a large animal often stimulate evasive or

cryptic behaviour in extant reptiles (Greene 1988), birds

and mammals (personal observation). In predatory taxa

hearing may have originally facilitated prey localisation.

Many extant predatory tetrapods rely heavily on chemical

and visual means of prey localisation (Ewer 1973;

Duellman and Trueb 1994; Pough et al. 1998), but some

use hearing to locate prey (Ewer 1973).

Sound production

Methods of animal sound production fall into five main

categories: stridulation, vocalisation, percussion, forced

airflow and the tymbal mechanism. Stridulation, the rubbing

together of body parts, is the most common means of sound

production in arthropods. Usually one of the stridulatory

parts (the file) is ridged, while the other (the scraper or

plectrum) is not (Figure 1). Stridulation has evolved

convergently in several arthropod groups (Figure 2) and is

especially prevalent among groups with highly sclerotised

(hardened) exoskeletons such as Malacostraca (shrimps,

crabs and kin), Arachnida (spiders, scorpions and kin),

Orthoptera (crickets and grasshoppers), Hemiptera (true

bugs) and Coleoptera (beetles) (e.g. Dumortier 1963b).

Unfortunately for paleontology, arthropod fossils are rarely

preserved in enough detail to determine whether or not

stridulatory structures are present. An exception is the taxon

Orthoptera, in which the stridulatory structures are modified

wing veins and can easily be discerned on fossil wings (e.g.

Bethoux and Nel 2002). Stridulation can be effective even if

the intended recipient lacks an auditory apparatus.

Arthropods often detect the stridulation of conspecifics via

substrate-borne vibrations (Crowson 1981; Gogala 1985,

2006; Barth 2002). Stridulation by prey upon seizure by a

vertebrate or arthropod predator stimulates the predator’s

tactile receptors – and auditory receptors, if present – and

often stimulates the predator to release the prey (Masters

1979; Crowson 1981). In many cases the predator’s release

of the stridulating prey may be a hardwired response to an

honest warning, for stridulating prey items often follow

stridulation with painful stimuli (e.g. stinging) or emission

of noxious chemicals, or are externally tough and therefore

difficult to eat (Masters 1979).

Many tetrapod vertebrates (Tetrapoda) produce sounds

by vocalisation, the vibration of mucosal folds called vocal

cords that extend into the lumen of the respiratory tract

(Figure 1). Vocal cords occur in Anura (frogs and toads),

Ambystoma þ Dicamptodon (mole salamanders), Mam-

malia (mammals), Gekkonidae þ Eublepharidae (geck-

oes), Pituophis melanoleucus (the bull snake), Crocodylia

(crocodilians), and Aves (birds) (Reese 1914; Maslin

1950; Kelemen 1963; Gans and Maderson 1973; King

1989; Young et al. 1995). Morphology, topology and

phylogenetic distribution indicate that vocal cords arose

independently in each of these groups (Figure 5). In all but

Aves the vocal cords are in the larynx (Reese 1914; Maslin

1950; Kelemen 1963; Gans and Maderson 1973; Young

et al. 1995); in birds they are in a unique organ called the

syrinx (King 1989).

Percussion is the hitting of a body part against a

substrate. Examples include nuptial abdomen tapping by

stoneflies (Plecoptera) and booklice (Psocoptera) and the

aquatic head-slap displays of crocodilians (Pearman 1928;

Garrick et al. 1978; Thorbjarnarson 1989; Stewart and

Sandberg 2006). These are discussed in more detail below.

Some insects produce defensive sounds by forcing air

through spiracles (Roth and Hartman 1967; Aiken 1985).

However, sound production by forceful airflow is more

characteristic of the vertebrate taxon Amniota, many

members of which hiss by forced ventilation. Hissing as a

threat device, often directed at potential predators, is

widespread among extant amniotes, including lizards,

snakes, turtles, crocodilians, basal birds and basal

mammals (Greene 1988; Davies 2002; Kear 2005;

Nowak 2005). It may therefore be a behavioural

symplesiomorphy for Amniota. If that is correct, then the

Figure 3. Frequencies of peak hearing ranges (white and greybars) and sound production (black bars) in extant animals. Greybars represent peak hearing ranges in vertebrates lackingstructures that enhance hearing such as tympana or connectionsbetween gas bladder and inner ear; note that hearing is restrictedto low frequencies in such groups. The black bar for snakesrepresents hissing. HS, hearing specialist. Information sources:Autrum 1963; Dumortier 1963c; Tembrock 1963; Vincent 1963;Simmons et al. 1971; Fant 1973; Gans and Wever 1976;Marcellini 1977; Garrick et al. 1978; Wever 1978, 1985; Robbinset al. 1983; Hill and Smith 1984; Aiken 1985; Fay 1988; Young1991; Duellman and Trueb 1994; Frankenberg and Werner 1992;Thorbjarnarson and Hernandez 1993; Michelsen 1998; Imaizumiand Pollack 1999; Ladich and Bass 2003; Young 1991.

P. Senter258


hiss was present by the Pennsylvanian Period (Ruta et al.

2003), at which time no vertebrate predator had yet

acquired tympanic ears (Clack and Allin 2004).

A Pennsylvanian hiss therefore had no value as an

acoustic display unless it exhibited the extraordinary

intensity necessary to be heard with atympanic ears.

If hissing is a behavioural symplesiomorphy of Amniota,

its sound may therefore have originally been the passive

result of a visual, inflationary display, as is the case with

some extant reptiles (Kinney et al. 1998). A hiss can be

produced during inspiration (Kinney et al. 1998; Young

1998) or expiration (Gans and Maderson 1973; Young

1998). Either way, forced inspiration occurs, and this

increases apparent body size in an amniote with movable

ribs (e.g. Kinney et al. 1998). In turtles and birds, hissing is

not accompanied by bodily expansion because their

ribcages do not allow it. However, hissing in the

earliest turtles and birds already had value as an acoustic

display because tympanic ears were present in a variety of

tetrapod predators by the time turtles and birds appeared

(reviewed below).

Tymbals, which are unique to Hemiptera (true bugs),

are series of external folds on the first abdominal segment.

Tymbals are buckled by internal muscles to produce

substrate-borne vibrations (Leston and Pringle 1963;

Gogala 1984; Claridge 1985). In cicadas (Cicadidae),

discussed more fully below, tymbals are coupled with air

bladders to produce airborne sounds.

Figure 4. Phylogeny of vertebrates discussed in this paper, showing independent origins of tympanic ears (T). Extant taxa are indicatedwith common names in parentheses. See text for information sources.



Temporal patterns

Across taxa, certain temporal patterns in sound production

are nearly universal. Animals tend to be noisiest at dawn,

dusk and night, with very little sound production during

the day (Schneider 1967; Marcellini 1977; Garrick et al.

1978; Welty and Baptista 1988; Thorbjarnarson and

Hernandez 1993; Zelick et al. 1999; McCauley and Cato

2000; Gerhardt and Huber 2002). A circannual pattern is

also present across taxa, with more sound production

during summers than during winters (Garrick et al. 1978;

Aiken 1985; Thorbjarnarson and Hernandez 1993; Morton

1996; McCauley and Cato 2000; Gerhardt and Huber

2002). There is no reason to believe that such temporal

patterns were absent before the Cenozoic.

Parallel evolution

Certain body plans are more conducive than others to the

evolution of certain sound-producing or -receiving organs,

and parallel evolution of such structures is common in taxa

with appropriate body plans. For example, posterior and

internal to the tetrapod cheek is a bone called the stapes

(Figure 1) that primitively served as a brace between cheek

and braincase (Clack 1992). Due to its opportune location

the stapes has been coupled with an external tympanum for

transmission of airborne sound to the inner ear in several

tetrapod lineages independently (Clack and Allin 2004)

(Figure 4). Another example of acoustic parallelism in

tetrapods is the parallel evolution of sound-producing

vocal cords within the larynx (Maslin 1950; Kelemen

1963; Gans and Maderson 1973) (Figure 5).

The plesiomorphic presence of laryngeal muscles that

can be evolutionarily co-opted for vocal modulation

makes the larynx a particularly appropriate organ to

modify for vocalisation. The appearance of elytra in

Coleoptera (beetles) and the sclerotisation of the beetle

exoskeleton have also encouraged repeated parallel

evolution of stridulatory structures in Coleoptera, in

which many stridulatory structures are modifications of the

elytra-closing mechanism (Dumortier 1963b). Other

examples of acoustic parallelism include the repeated

independent appearance of trichobothria (sensory hairs

that respond to airborne sounds) within Arachnida (spiders

and kin) and Hemiptera (true bugs), tibial tympana in

Orthoptera (crickets and kin), use of wings for stridulation

in Orthoptera and use of chelipeds for stridulation in

Malacostraca (shrimp and kin) (Dumortier 1963b;

Gwynne 1995; Sweet 1996; Barth 2002; Bethoux and

Nel 2002; Desutter-Grandcolas 2003).

Caveats

Sound-producing structures often fossilise poorly or not at

all. Because of this the inference that a given animal sound

was present during a given geological period is rarely

certain. If a sound producing structure is present in all

extant members of a given crown clade, then it is most

parsimonious to infer that the structure was present in the

common ancestor of the clade. However, confidence in

such inferences cannot always be absolute, because in

some cases the prevalence of acoustic parallelism renders

hypotheses of homology of acoustic structures and

behaviour uncertain even among closely related species.

Even when such an inference is correct, it places only a

tentative bound on the time of origin of the structure,

because the crown clade may have appeared earlier than its

earliest known fossils and also because it may be

impossible to determine whether the structure was present

in fossil members of the lineage that are basal to the crown

clade. Another compounding factor is the fact that some

taxa with extant members are not defined as crown clades.

The earliest members of such taxa therefore do not

necessarily possess the features characteristic of the crown

clade. For these reasons the paleobioacoustical inferences

presented here must be treated as hypotheses to test, rather

than firm conclusions. Nevertheless, available evidence

Figure 5. Phylogenetic distribution of vocal cords in the larynx(L) and syrinx (S) of extant jawed vertebrates. Note the largenumber of intervening taxa without vocal cords, which indicatesmultiple independent origins of vocal cords.

P. Senter260


allows enough inferences to be made to make paleobioa-

coustical studies worthwhile.

Pre-Cenozoic paleobioacoustics of non-insect

invertebrates

Incidental sounds

Extant squid make a popping sound that appears to be due

to fluttering of mantle lips during expulsion of water from

the siphon (Iversen et al. 1963). Although cephalopods are

the only invertebrates outside Arthropoda that possess

organs for unambiguous underwater sound reception

(modified statocysts) (Coffin et al. 2004), there is no

evidence that their locomotor sounds are involved in

communication. Cephalopods appeared during the Upper

Cambrian and stem-group squid (Teuthidea) during the

Upper Triassic (Doyle 1993; King 1993). Squid popping

sounds may therefore have existed as early as the Upper

Triassic, and such sounds may have been present as early

as the Cambrian if other cephalopods made them.

However, no extant teuthid family has a known pre-

Cenozoic fossil record (Doyle 1993), so if popping sounds

are restricted to crown-group squid such sounds may have

been absent from the Mesozoic.

Saltwater mussels (Mollusca: Bivalvia: Mytilidae)

attach themselves to the substrate with protein secretions

from the foot called byssal threads. When a mussel uses its

foot for locomotion, the stretching and breaking of the

byssal threads make loud snapping sounds (Fish and

Mowbray 1970). Summation of the snaps produced by the

various colony members produces a continuous crackling

sound (Fish and Mowbray 1970). The family Mytilidae is

known from as early as the Lower Triassic (Skelton and

Benton 1993). Members of several other bivalve families

use byssal threads as anchors, but only in Mytilidae are the

threads used in locomotion (Ruppert and Barnes 1994), so

we should not expect that the snapping sounds were

present before the appearance of mytilids.

Colonies of sea urchins (Echinodermata: Echinoidea)

make sustained crackling sounds that have been likened to

the sound of something frying (Fish and Mowbray 1970).

Individuals contribute to the sound by movement of spines

and possibly by action of the calcareous feeding apparatus

called Aristotle’s lantern (Fish and Mowbray 1970). Sea

urchins are known from as early as the Upper Ordovician;

their diversity exploded during the Jurassic Period

(Kier 1987), at which time their frying sounds presumably

became more prevalent.

Extant barnacles (Arthropoda: Cirripedia) make crack-

ling sounds during feeding as their appendages scrape

against their calcareous shells (Budelmann 1992a,b). These

sounds are often continuous due to high population density

(Dumortier 1963b). Convergent acquisition of calcareous

shells, and presumably crackling sounds, by various

lineages of barnacles occurred in the Triassic Period and

continued through the Mesozoic (Foster and Buckeridge

1987). Paleozoic barnacles lacked calcareous shells (Wills

1963; Schram 1975; Collins and Rudkin 1981) and

therefore probably did not produce the crackling sounds.

The appendages of non-sessile arthropods sometimes

produce low-amplitude clicking or ticking sounds during

locomotion when the appendages contact the substrate or

other body parts. Arthropods are known from early in the

Cambrian Period (Briggs et al. 1993), so their incidental

locomotor sounds may have been present that early.

Crustaceans (Arthropoda: Crustacea)

Many members of the crustacean taxon Malacostraca

(shrimp, lobsters and crabs) stridulate when seized

(Budelmann 1992a). The taxonomically erratic distri-

bution of malacostracan stridulatory structures, along with

their great variety and lack of transitional forms, suggests

multiple parallel origins of stridulation within the group

(Dumortier 1963b) (Table 1). While most malacostracans

stridulate with hard exoskeletal parts, spiny lobsters

(Palinuridae) stridulate by rubbing a soft plectrum at the

base of the antenna over a file beneath the eye; the

mechanism of the resulting rasping sound resembles that

of the bow and string of a stringed instrument (Patek

2001). The oldest known malacostracans are from the

Upper Devonian (Briggs et al. 1993). The bauplan that

allowed repeated evolution of stridulation was therefore

present that early, and it is possible that anti-predator

Table 1. Malacostracan crustacean families that have stridulating members and are known from before the Cenozoic, and theirstridulatory organs.

Taxon Earliest record Location of scraper Location of file

Calappidae (box crabs) Lower Cretaceous Cheliped CephalothoraxDiogenidae (left-handed hermit crabs) Upper Cretaceous Left cheliped Right chelipedLysiosquillidae (mantis shrimp) Upper Cretaceous Uropods Lower surface of telsonPalinuridae (spiny lobsters) Lower Jurassic Base of antenna Antennular plate below eyePenaeidae (prawns) Lower Triassic First abdominal segment Posterior CephalothoraxSquillidae (mantis shrimp) Upper Cretaceous Uropods Lower surface of telsonXanthidae (mud crabs) Lower Cretaceous Cheliped Walking legs

References: Dumortier 1963b; Briggs et al. 1993; Patek 2001.



stridulation evolved multiple times in Paleozoic and

Mesozoic malacostracan lineages. Stridulatory structures

have been identified on the flanks of members of the

Cretaceous palinurid lobster genus Linuparus (Feldmann

et al. 2007).

A non-stridulatory malacostracan sound is the buzzing

of clawed lobsters (Nephropidae) when seized, accom-

plished by vibrating the carapace (Henniger and Watson

2005). The family is known from as early as the Middle

Jurassic (Briggs et al. 1993).

Arachnids (Arthropoda: Arachnida)

Stridulation in response to disturbance is present in a wide

variety of arachnids, including spiders (Araneae),

scorpions (Scorpiones), whip scorpions (Amblypygi),

windscorpions (Solifugae) and harvestmen (Opiliones)

(Dumortier 1963a,b; Uetz and Stratton 1981; Cloudsley-

Thompson and Constantinou 1984). While the sounds

produced by arachnid stridulation are often of low

intensity and cannot be heard further away than a few

centimetres, in some cases spider and scorpion stridulation

produces a loud buzz or hiss (Uetz and Stratton 1981;

McCormick and Polis 1990). Only six of the many extant

arachnid families with known stridulating members

(Dumortier 1963b; Uetz and Stratton 1981) have known

pre-Cenozoic fossil records, and all six are spider families

(Selden 1993; Penney et al. 2003) (Table 2). However, the

known pre-Cenozoic fossil record of Arachnida is so

spotty that many extant lineages probably existed long

before their known fossil records reveal (Penney et al.

2003). Also, the wide variety of arachnid stridulatory

structures (Dumortier 1963b; Uetz and Stratton 1981;

Hjelle 1990) indicates that parallel evolution of stridula-

tion is rampant in Arachnida, which in turn suggests high

likelihood that many extinct arachnids also stridulated in

response to disturbance. A patch of spines found on a limb

fragment of a Middle Devonian arachnid of unknown

affinity from New York may be a stridulatory structure

(Shear et al. 1987).

The earliest known arachnids are from the Silurian

(Jeram et al. 1990). The earliest known harvestman is from

the Devonian (Dunlop et al. 2003), and the earliest known

solifuge and amblypygid are from the Pennsylvanian

(Selden 1993; Dunlop 1994). The earliest terrestrial

scorpions are from the Devonian (Selden and Dunlop

1998). Basal spiders are known from as early as the Lower

Devonian, with representatives of extant clades present by

the Pennsylvanian (Mesothelae), Middle Triassic (Myga-

lomorphae) and Middle Jurassic (Araneomorphae) (Pen-

ney et al. 2003). Stridulation by or directed toward those

taxa may have been present by those times.

In addition to defensive stridulation, members of

several extant spider families stridulate during courtship or

interspecific aggression (Uetz and Stratton 1981), and the

same is conceivably true of members of extinct spider

families. Some spiders make courtship sounds by means

other than stridulation. Giant crab spiders (Sparassidae)

vibrate their appendages like tuning forks, and crab spiders

(Thomisidae) drum body parts against the substrate

(Uetz and Stratton 1981). Both families were present by

the Cretaceous Period (Grimaldi et al. 2002a,b).

Trichobothria, sensory hairs sensitive to air move-

ments, have evolved convergently in several extant

arachnid taxa (Sissom 1990; Barth 2002). The trichobo-

thria of spiders can detect low-frequency sounds of

10–950Hz, with peak sensitivity from 50 to 120Hz, and

spiders use this ability to locate flying flies and other prey

(Barth 2002). Extant scorpions use trichobothria to detect

air currents caused by prey movements (McCormick and

Polis 1990), but it is uncertain whether their trichobothria

are used for sound reception. Either way, Paleozoic

scorpions lacked trichobothria (Sissom 1990) and there-

fore did not locate prey by means of airborne sound.

Millipedes and centipedes (Arthropoda: Myriapoda)

Some myriapods stridulate in response to disturbance, and

in some cases detached appendages make creaking sounds

by an unknown mechanism, apparently to distract a

predator while the myriapod escapes (Dumortier 1963a,b).

Centipedes (Chilopoda) are known from as early as the

Upper Silurian (Jeram et al. 1990) and millipedes

(Diplopoda) from as early as the Lower Devonian

(Shear 1997). Defensive stridulation by myriapods,

directed at arachnid or centipede predators, may therefore

Table 2. Stridulating spider families that are known from before the Cenozoic, and their known stridulatory organs.


Araneidae (orb weavers) Upper Cretaceous Appendage AbdomenDipluridae (funnel-web tarantulas) Lower Cretaceous Pedipalp CheliceraLinyphiidae (sheet-web weavers) Lower Cretaceous Pedipalp Chelicera

Leg II Leg ISegestriidae (tube-dwelling spiders) Upper Cretaceous – –Theridiidae (comb-footed spiders) Cretaceous Abdomen ProsomaUloboridae (hackled orb weavers) Lower Cretaceous Pedipalp Chelicera

References: Uetz and Stratton 1981; Grimaldi et al. 2002a,b; Penney et al. 2003.

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have existed this early. However, airborne predator-

distracting sounds, such as the creaking of detached

appendages, would have been ineffective against deaf

predators and so were probably absent before terrestrial

tetrapods acquired the ability to hear airborne sounds in

the Permian Period (see below).

The earliest terrestrial animal communities, from the

Silurian Period, included centipedes and arachnids

(Jeram et al. 1990), both of which are predatory.

The earliest known millipedes and basal insects (Insecta)

appeared shortly thereafter, in the Lower Devonian

(Jeram et al. 1990; Shear 1997). Anti-predator stridulation

is known in extant members of all four taxa (Dumortier

1963a,b; Uetz and Stratton 1981) and may therefore have

existed in these early communities. Anti-predator stridula-

tion is most likely to have evolved first in taxa with

especially tough exoskeletons or in taxa capable of

producing unpleasant stimuli such as stings, bites, or

noxious emissions, so that it functioned as an honestwarning

to predators, as in extant arthropods (Masters 1979).

Directions for further research

To my knowledge, stridulatory structures have not been

described in fossil arthropods outside Insecta with the

exception of the Devonian arachnid and the Cretaceous

lobster mentioned above. A search for stridulatory

structures among fossil malacostracans, trilobites, eur-

ypterids and perhaps other pre-Cenozoic arthropods would

be worthwhile. It would also be informative to compare

sound-producing structures across Malacostraca and

Arachnida to determine whether any such structures are

homologous between families or genera.

Pre-Cenozoic insect paleobioacoustics

Stoneflies (Plecoptera)

Intraspecific acoustic communication is characteristic of

the extant stonefly clade Arctoperlaria (Stewart and

Sandberg 2006). After emergence, arctoperlarian stone-

flies perform male-female vibratory duets at aggregation

sites while the males search for the females (Stewart and

Sandberg 2006). The duets consist of vibrations with

species-specific rhythms, produced by audible tapping of

the abdomen on the substrate (Stewart and Sandberg

2006). Tapping duets are known in all extant arctoperlar-

ian families and appear to be a behavioural symplesio-

morphy of the clade (Stewart and Sandberg 2006). If this is

correct then the resulting sounds were present at the time

of origin of the arctoperlarian crown clade, the earliest

known fossils of which are from the Middle Triassic

(Grimaldi and Engel 2005).

Members of some extant stonefly families augment

the courtship tapping with scratching of the abdomen on

the substrate (producing a raspy sound), or rubbing

of specialised abdominal parts on the substrate (producing

a squeak) (Stewart and Sandberg 2006). However, none

of these families has a pre-Cenozoic fossil record

(Sinitshenkova 2002).

Crickets and kin (Orthoptera)

Males of several extant orthopteran taxa stridulate during

courtship by rubbing together specialised parts of the

wings, producing sounds with species-specific rhythms.

Such stridulation often stimulates chorusing and aggres-

sion from nearby males, and the approach of one male too

close to another may elicit a different temporal pattern of

stridulation called a disturbance song (Dumortier 1963a).

Stridulatory wing venation patterns are absent in Paleozoic

orthopterans, the earliest known of which are from the

Pennsylvanian (Bethoux and Nel 2002; Gorochov and

Rasnitsyn 2002). Stridulatory mechanisms on the wings

were present in the extinct, Upper Triassic orthopteran

family Mesoedischiidae and in members of Ensifera

(crickets) from the Upper Triassic and later (Bethoux and

Nel 2002; Gorochov and Rasnitsyn 2002). The earliest

known members of the extant stridulating ensiferan taxa

Gryllidae (true crickets) and Gryllotalpidae (mole crick-

ets) are from the Lower Cretaceous (Ross and Jarzem-

bowski 1993). Stridulation is also characteristic of

‘Prophalangopsidae’ (hump-winged and sagebrush crick-

ets), a taxon that is probably paraphyletic with respect to

Tettigoniidae (katydids) (Desutter-Grandcolas 2003).

‘Prophalangopsids’ are known from as early as the

Lower Jurassic, while katydids, grasshoppers (Acridoi-

dea), and other extant orthopteran families with stridulat-

ing members have no known pre-Cenozoic fossil record

(Ross and Jarzembowski 1993; Rust et al. 1999; Gorochov

and Rasnitsyn 2002).

Extant stridulating crickets simultaneously perceive

both the substrate-borne vibrations (via mechanoreceptors

in the legs) and the airborne sounds (via tibial tympana;

Figure 1) generated by the singing of conspecifics

(Kuhne et al. 1985). Morphological phylogenetic analyses

of extant ensiferans suggest that stridulatory structures and

tibial tympana were absent in the common ancestor of

extant orthopterans and have evolved in parallel a number

of times within the ensiferan crown group (Gwynne 1995;

Desutter-Grandcolas 2003). However, stridulatory wing

venation is present in all members of a long phylogenetic

series of Upper Triassic crickets that are basal to crown

Orthoptera (Bethoux and Nel 2002), which indicates that

stridulatory behaviour is plesiomorphic for Upper Triassic

and later crickets. This suggests that either stridulation was

lost once in the crown clade’s ancestor and then regained

multiple times by its descendants, or that it was present in

the crown clade’s ancestor and was lost multiple times

within the crown clade. The latter interpretation is

supported by a recent molecular phylogenetic analysis,



the results of which differ greatly from those of

morphological phylogenetic analyses (Jost and Shaw

2006). Most of the non-stridulatory extant families are

fossorial (Gwynne 1995), and there may be a connection

between the acquisition of such a lifestyle and the loss of

stridulatory behaviour in crickets.

Gryllacrididae (locust crickets and leaf-rolling crick-

ets) are non-stridulating crickets without tympana, some of

which are fossorial. Males and females duet by drumming

the tarsus or abdomen on the substrate (Hale and Rentz

2001). This family is known from as early as the Upper

Cretaceous (Ross and Jarzembowski 1993).

Among extant orthopterans of various lineages,

females generally prefer male calls that are longer and

occur at higher rates (Gerhardt and Huber 2002).

If selective pressure for these traits has existed long

enough, then within each orthopteran lineage male calls

were originally of shorter duration and occurred at lower

rates than those of their extant descendants.

Rust et al. (1999) used comparison with extant

orthopterans to calculate the dominant frequency of the

stridulatory sounds produced by the wings of a Cenozoic

fossil katydid. The same may be possible with Mesozoic

orthopterans but has not yet been attempted.

Stridulatory wing structures are also present in members

of the extinct, Middle and Upper Triassic taxon Titanoptera

(¼Mesotitanida). This taxon is closely related to Orthoptera

and consists of large (wingspans up to 40 cm) insects from

Eurasia and Australia (Gorochov and Rasnitsyn 2002;

Grimaldi and Engel 2005).

Roaches (Blattaria)

Roachlike insects from as early as the Carboniferous

Period are often placed in Blattaria, but as a group

Paleozoic ‘roachoids’ are paraphyletic with respect to

Isoptera (termites), Mantodea (mantises), and Blattaria

(true roaches) (Grimaldi and Engel 2005). The earliest

known members of Blattaria sensu stricto are from the

Lower Cretaceous (Grimaldi and Engel 2005). Many

extant roaches make courtship or disturbance sounds by a

variety of means, but most such noisy roaches are

members of Blaberidae (Roth and Hartman 1967), which

is unknown before the Cenozoic (Grimaldi and Engel

2005). Members of other roach families are generally

silent, although one member of Blattellidae, a family

known from the Lower Cretaceous (Grimaldi and Engel

2005), makes a clicking sound before taking flight, and

another blattellid is known to squeak when caught

(Roth and Hartman 1967).

Termites (Isoptera)

Termite soldiers tap their heads on the substrate with a

rhythm that is recognised by conspecifics, in response

to disturbance, most likely as an alarm signal (Kirchner

et al. 1994). This behaviour is taxonomically widespread

within Isoptera and may therefore be a behavioural

symplesiomorphy for the group (Virant-Doberlet and Cokl

2004). Early termites are known from most continents in

the Lower Cretaceous, including Laurasian members of

the extant head-tapping family Termopsidae (Grimaldi

and Engel 2005).

Booklice (Psocoptera)

A widespread behaviour among booklice is the tapping of

the abdomen on the substrate by females to call males; it

makes a ticking or creaking sound (Pearman 1928).

The earliest known booklice are from the Upper Jurassic;

fossils from as early as the Lower Permian have been

attributed to Psocoptera but more likely belong to some

related taxon (Grimaldi and Engel 2005). Extant psocop-

teran families with tapping species and known pre-Cenozoic

fossil records include Psocidae (Upper Jurassic) and

Trogiidae (Upper Cretaceous) (Rasnitsyn 2002).

True bugs (Hemiptera)

Extant hemipterans comprise five major clades: Sternor-

rhyncha (aphids, scale insects and kin), Fulguromorpha

(planthoppers), Coleorrhyncha (peloridiid bugs), Prosor-

rhyncha (water bugs, assassin bugs, stink bugs and kin)

and Clypeomorpha (cicadas, leafhoppers, froghoppers and

kin). Members of the latter four clades possess tymbals,

which are buckled by internal muscles in species-specific

rhythms to produce vibrations called ‘songs’ during

courtship and, in some cases, during copulation

(Leston and Pringle 1963; Gogala 1984; Claridge 1985;

Sweet 1996). Tymbals are absent in Sternorrhyncha, and

their presence in the other four clades suggests that

the presence of tymbals is a synapomorphy that unites the

other four clades into a taxon (hereafter called the

‘tymbaled superclade’ below) that excludes Sternor-

rhyncha (Sweet 1996). That interpretation of hemipteran

phylogeny is supported by molecular systematics

(Campbell et al. 1995; von Dohlen and Moran 1995).

In most members of the tymbaled superclade the

tymbals are simple and do not produce airborne sound but

instead cause vibrations in the substrate, usually a plant

stem (Leston and Pringle 1963; Claridge 1985; Gogala

1984, 1985, 2006; Sweet 1996). Both sexes sing, lack

tympana and perceive the songs of conspecifics via

mechanoreceptors in the legs (Leston and Pringle 1963;

Claridge 1985; Gogala 1985, 2006; Sweet 1996). This

appears to be the plesiomorphic condition for the tymbaled

superclade (Sweet 1996). The earliest known members of

the tymbaled superclade, which is a crown clade, are from

the Lower Permian (Shcherbakov and Popov 2002), and

P. Senter264


the use of tymbals for substrate-borne courtship songs

presumably originated then.

Within the tymbaled superclade are several taxa in

which courtship is modified such that it produces airborne

sounds. The most familiar example is probably the treetop

singing of members of Cicadidae (cicadas), the earliest

known fossils of which are from the Upper Cretaceous

(Turonian) of New Jersey (Grimaldi et al. 2002b). In cicadas

the females have lost the tymbals, so singing is done only by

the males, in which the tymbals are elaborate in comparison

with those of other hemipterans (Leston and Pringle 1963;

Claridge 1985). Air sacs internal to the tymbals amplify the

songs so that they are audible from several meters away and

attract members of both sexes to a congregational area for

reproduction (Dumortier 1963a; Claridge 1985). Cicadas

hear each other’s songs with tympanic ears that are ventral

to the tymbals on the abdomen (Leston and Pringle 1963;

Claridge 1985). After attracting a female, a male cicada

changes the rhythm of his song; in some species he also adds

audible wing-flicking, and in some species the female

responds with wing-flicking of her own (Boulard 2006).

Some cicada species also have stridulatory structures, the

behavioural significance of which is unknown (Boulard

2006). Another enigmatic acoustic behaviour by cicadas is

the drumming of the wings on the substrate in some species,

especially in those that have lost tymbals altogether

(Boulard 2006).

In many members of Prosorrhyncha, the earliest

known members of which are from the Upper Triassic

(Shcherbakov and Popov 2002), tymbal songs are

augmented by simultaneous, audible stridulation, which

adds higher frequencies to the songs (Gogala 1984, 1985,

2006; Sweet 1996). Often, after the female has been

attracted by the male’s calling song, he switches to a

courtship song (Dumortier 1963a). The variety of

stridulatory structures in Prosorrhyncha (Table 3)

indicates that augmentation of tymbal songs with

stridulation arose multiple times in parallel within

Prosorrhyncha (Leston and Pringle 1963). Trichobothria

are present in many prosorrhynchans, fulguromorphs, and

coleorrhynchans, but not in clypeomorphs (Sweet 1996).

They appear to be used as acoustic receptors for low-

frequency, low-amplitude, audible song and differences

between the trichobothria of various taxa suggest that they

appeared in parallel multiple times in the tymbaled

superclade (Sweet 1996).

In the prosorrhynchan taxon Nepomorpha a switch has

occurred from the ancestral hemipteran plant-dwelling

habitat to an aquatic one (Shcherbakov and Popov 2002).

The new habitat required that plant stems be traded for the

watery environment as a medium to carry vibrational

signals to conspecifics. Accordingly, many nepomorphs

stridulate underwater. Among nepomorph families with

known pre-Cenozoic fossil records, stridulation is known

in Corixidae (water boatmen), Naucoridae (creeping water

bugs), Nepidae (waterscorpions), and Notonectidae (back-

swimmers) (Dumortier 1963b). In Corixidae and Noto-

nectidae stridulation by males is known to attract females

(Dumortier 1963a; Cokl et al. 2006). The variety of

nepomorph stridulatory structures (Table 3) suggests that

stridulation arose multiple times independently in

Nepomorpha. Because evolution of stridulation is rampant

in Nepomorpha, it may have been present in extinct

nepomorphs as early as the Upper Triassic, from which

time period the earliest nepomorphs are known (Shcher-

bakov and Popov 2002). Non-stridulatory courtship

sounds (buzzing or chirping) are made by members of

Belostomatidae (giant water bugs) by expulsion of air

Table 3. Prosorrhynchan families that are known from before the Cenozoic with members that are known to stridulate, and theirstridulatory organs.


Alydidae (broad-headed bugs) Upper Jurassic Femur HemelytraAradidae (flat bugs) Lower Cretaceous Hind femur Abdomen

Hind tibia AbdomenCoreidae (leaf-footed bugs) Upper Jurassic Pronotum Fore wingCorixidae (water boatmen) Lower Jurassic Fore tarsus Opposite fore femur

Fore femur HeadCydnidae (burrowing bugs) Lower Jurassic Abdomen Hind wingLygaeidae (seed bugs) Lower Cretaceous Wing Abdomen

Foreleg ProsternumMiridae (plant bugs) Upper Jurassic Hind femur EmboliumNabidae (damsel bugs) Upper Jurassic – –Naucoridae (creeping water bugs) Upper Triassic – –Nepidae (waterscorpions) Upper Jurassic Coxa FemurNotonectidae (backswimmers) Upper Triassic Fore femur Head or fore coxa

Tibia RostrumReduviidae (assassin bugs) Lower Cretaceous Rostrum ProsternumThaumastellidae (no common name) Lower Cretaceous Abdomen Wing

References: Dumortier 1963b; Leston and Pringle 1963; Gogala 1984, 1985, 2006; Aiken 1985; Ross and Jarzembowski 1993; Shcherbakov and Popov 2002.

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through spiracles (Aiken 1985); belostomatids are known

from as early as the Upper Triassic (Ross and

Jarzembowski 1993).

In one nepomorph family, Corixidae (water boatmen) –

known from as early as the Lower Jurassic (Ross and

Jarzembowski 1993) – perception of conspecific stridula-

tion is truly auditory. Water boatmen receive such

vibrations with tympana that are surrounded by air bubbles,

whereas other nepomorphs use atympanic mechanorecep-

tors for reception of water-borne vibrations (Cokl et al.

2006). Unlike the low-amplitude calls of most nepomorphs,

which are audible to humans only if the bug is close to the

listener’s ear, the underwater songs of corixids are quite

loud; resonation by the same air bubbles that enable

tympanic hearing in corixids amplifies the songs so that they

are audible from beyond the shoreline (Aiken 1985).

Courtship sounds are not the only sounds made by

hemipterans. Many clypeomorphs cry audibly when

caught and during rough treatment (Dumortier 1963a;

Leston and Pringle 1963; Claridge 1985). Many prosor-

rhynchans stridulate audibly when caught, including

members of Cydnidae (burrowing bugs), Lygaeidae

(seed bugs) and Reduviidae (assassin bugs) (Dumortier

1963a; Leston and Pringle 1963; Gogala 2006). In some

reduviid species the female stridulates upon being

mounted, deterring the male, if she is unwilling to mate

(Lazzari et al. 2006). Members of the prosorrhynchan

family Coreidae (leaf-footed bugs), the earliest known

members of which are from the Upper Jurassic (Ross and

Jarzembowski 1993), make sounds by unknown means

(Dumortier 1963b); the biological significance of these

sounds is unclear, and they are probably by-products of

locomotion (Gogala 1985). Among members of Sternor-

rhyncha, some colonies of aphids (Aphididae) make

scraping sounds when disturbed (Leston and Pringle

1963). These stridulatory sounds are made by rubbing the

hind tibiae on rough spots on the abdomen (Dumortier

1963a). The earliest known aphids are from the Lower

Cretaceous (Ross and Jarzembowski 1993).

Stridulatory structures are known in some fossil

hemipterans. Members of the stem-hemipteran family

Dysmorphoptilidae possessed a stridulatory apparatus

with a scraper on the hind knee and the file on the

underside of the fore wing; the family is known from the

Upper Permian to the Upper Jurassic (Shcherbakov and

Popov 2002). A similar stridulatory apparatus is present in

Triassic members of the extinct prosorrhynchan family

Ipsviciidae (Shcherbakov and Popov 2002).

Beetles (Coleoptera)

Beetles of many extant families produce sounds, often by

stridulation (Alexander and Moore 1963; Dumortier

1963b). Adult and larval beetles often stridulate in response

to disturbance, although some adult males stridulate

to attract females or repel rival males (Dumortier 1963a;

Rudinsky and Ryker 1976; Aiken 1985). The broad

taxonomic span of families with stridulating members and

the wide variety of stridulatory structures shows that

repeated parallel evolution of stridulation is rampant in

Coleoptera (Table 4). Beetle stridulationmay therefore have

been present as early as the Lower Permian, from which the

earliest beetle fossils are known (Ponomarenko 2002).

Various beetles are also known to make non-

stridulatory sounds. Female members of Anobiidae

(death-watch beetles), a family known from as early as

the Lower Cretaceous (Ross and Jarzembowski 1993),

attract males by drumming the head on the substrate

(Dumortier 1963a). In some members of Buprestidae

(metallic wood-boring beetles), a family known from as

early as the Middle Jurassic (Ross and Jarzembowski

1993), members of both sexes drum their abdomens on the

substrate and answer each other’s drumming in like

manner (Crowson 1981). Drumming of body parts against

the substrate is also known in Cerambycidae (long-horned

beetles) (Crowson 1981), the earliest known members of

which are from the Lower Cretaceous (Ross and

Jarzembowski 1993). Some cerambycids also make

purring sounds by vibrating the body within a crevice in

bark (Dumortier 1963b). Larvae of some members of

Dytiscidae (predaceous diving beetles), a family known

from as early as the Upper Jurassic (Ponomarenko 2002),

squeak by expelling air through spiracles when disturbed

(Aiken 1985). Larvae of some members of Hydrophilidae

(water scavenger beetles), a taxon known from as early as

the Upper Triassic (Ponomarenko 2002), hiss by an

unknown mechanism upon disturbance (Aiken 1985).

Members of Elateridae (click beetles), produce a loud

click by snapping a spine on the prosternum into a notch

on the mesosternum, which suddenly flexes and bounces

the beetle and is used to right the beetle when upside-down

or to make it difficult for predators to hold (Grimaldi and

Engel 2005); the earliest known elaterids are from the

Upper Triassic (Ponomarenko 2002). The wings of

members of Scarabaeidae (scarab beetles), a family

known from as early as the Lower Jurassic (Ponomarenko

2002), often buzz loudly during flight. The exoskeletons of

these beetles are particularly tough, so it is possible that

the loud scarabaeid flight buzz is an honest warning of

culinary difficulty to potential predators.

Lacewings and kin (Neuropterida)

The supraordinal insect taxon Neuropterida includes the

order Raphidioptera (snakeflies) and the sister orders

Megaloptera (dobsonflies and alderflies) and Neuroptera

(lacewings). Courtship in all extant families of Raphi-

dioptera and Megaloptera involves abdominal tremulation,

sensed via substrate- (stem- or leaf-) borne vibrations with

species-specific rhythms; in Corydalidae (dobsonflies)

P. Senter266


only the males tremulate, but in Sialidae (alderflies) and

Raphidioptera the sexes perform tremulatory duets

(Henry 2006). While tremulation does not produce

airborne sounds, it is often accompanied by audible wing

fluttering in Raphidioptera or by audible drumming of the

abdomen on the substrate in Sialidae, and is replaced by

audible wing fluttering in some species of Corydalidae

(Henry 2006).

Among lacewings, wing fluttering during courtship is

known in Coniopterygidae (dustywings) and Berothidae

(beaded lacewings) (Henry 2006), known from as early as

the Upper Jurassic and the Lower Cretaceous respectively

(Grimaldi and Engel 2005). Tremulation, wing fluttering

and abdominal drumming during courtship are all known

in Chrysopidae (green lacewings) (Henry 2006), a family

known from as early as the Lower Cretaceous (Grimaldi

and Engel 2005).

Among lacewings, tremulation is absent in all but three

derived families, the relationships between which suggest

an independent origin of tremulation in each (Henry 2006).

The presence of tremulation in Raphidioptera and

Megaloptera but not basal Neuroptera makes it unclear

whether tremulation appeared independently in the three

neuropterid orders or was present in the common

neuropterid ancestor, lost in ancestral lacewings, and

then regained in derived lacewings. If tremulation was

present in the neuropterid ancestor, then it (and possibly

the accompanying sounds of drumming and/or wing

fluttering) existed as early as the Permian Period, from

which the earliest neuropterid fossils are known

(Grimaldi and Engel 2005). If tremulation evolved

separately in the three orders, then the times of origin of

its separate appearances are less clear. Snakeflies are

known from the Lower Jurassic, but the earliest known

member of an extant family is from the Tertiary (Grimaldi

and Engel 2005). Megalopterans are known from as early

as the Upper Triassic, but extant megalopteran families are

unknown before the Middle Jurassic (Grimaldi and Engel

2005). Estimated times of origin of tremulation and

accompanying sounds in Raphidioptera and Megaloptera

therefore depend on whether tremulation was present in

each order’s ancestor or only in members of extant

tremulating families. It is plausible that the neuropterid

bauplan encouraged repeated evolution of tremulation,

just as the beetle bauplan encouraged repeated evolution of

stridulation. It is therefore possible that these neuropterid

Table 4. Beetle families that are known from before the Cenozoic in which adults are known to stridulate, and their stridulatory organs,where known.


Anobiidae (death-watch beetles) Lower Cretaceous Prosternum GulaBruchidae (seed beetles) Upper Jurassic – –Buprestidae (metallic wood-boring beetles) Upper Jurassic – –Carabidae (ground beetles) Lower Jurassic Elytra Abdomen

Femur ElytraCerambycidae (long-horned beetles) Lower Cretaceous Pronotum Mesonotum

Elytra HindfemurMetasternum Coax

Chrysomelidae (leaf beetles) Upper Jurassic Prosternum GulaPronotum MesonotumElytra Abdomen

Curculionidae (weevils) Lower Cretaceous Elytra AbdomenAbdomen Elytra

Dytiscidae (predaceous diving beetles) Upper Jurassic Wing AbdomenEndomychidae (handsome fungus beetles) Upper Cretaceous Pronotum HeadHeteroceridae (variegated mud-loving beetles) Lower Cretaceous Femur AbdomenHydrophilidae (water scavenger beetles) Upper Triassic Elytra AbdomenLucanidae (stag beetles) Upper Jurassic Elytra HindfemurNemonychidae (no common name) Upper Jurassic – –Nitidulidae (sap beetles) Middle Jurassic Pronotum HeadPassalidae (bessbugs) Lower Cretaceous Abdomen WingScarabaeidae (scarab beetles) Lower Jurassic Elytra Abdomen

Elytra HindfemurCoax MetasternumAbdomen ElytraAbdomen WingFemur Elytra

Scolytidae (bark beetles and ambrosia beetles) Lower Cretaceous Prosternum GulaAbdomen Elytra

Silphidae (carrion beetles) Lower Jurassic Elytra Abdomen

References: Dumortier 1963b; Ross and Jarzembowski 1993; Ponomarenko 2002; Wessel 2006.

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behaviours and their accompanying sounds appeared

multiple times before and during the Cenozoic.

Wasps, bees and ants (Hymenoptera)

Wasps (Hymenoptera) are known from as early as the

Upper Triassic (Grimaldi and Engel 2005). The wasp clade

Aculeata, known from as early as the Upper Jurassic, is

characterised by modification of the ovipositor into a sting

(Grimaldi and Engel 2005). Aculeates tend to buzz audibly

in flight, and it is possible that, as with the stridulatory

sounds of certain other insects, the flight fuzz deters

potential predators by warning them of the painful

consequences of predatory attempts.

Aculeate flight sounds also serve social functions. Some

male braconid wasps (Braconidae) also use their wings to

make courtship sounds when near females (Sotavalta 1963);

braconids are known from as early as the Lower Cretaceous

(Ross and Jarzembowski 1993). Members of Vespidae,

which includes hornets and kin, are known to buzz with

their wings during flight and during copulation (O’Neill

2001); vespids are known from as early as the Lower

Cretaceous (Ross and Jarzembowski 1993). In some

members of Sphecidae (mud daubers and kin), a family

known from as early as the Lower Cretaceous (Ross and

Jarzembowski 1993), males use buzzing as an acoustic

threat when defending the nest against marauders or rival

males (O’Neill 2001); males of some sphecid species also

locate virgin females by the loud buzz made by the females

as they dig themselves out of the ground. The buzzing of

bees (Apoidea) cannot be heard by fellow bees during flight,

but in some bees, once females have alighted, males use the

flight buzz to court them (Sotavalta 1963). The earliest

known bee is from the Lower Cretaceous (Poinar and

Danforth 2006). Reports of pre-Cretaceous bee body and

trace fossils exist, but the former have been reidentified as

indeterminate insects and the latter are more likely beetle

than bee traces (Engel 2001).

A variety of sounds are known in extant bees,

particularly those of the closely related tribes Apini

(honeybees and kin), Bombini (bumblebees and kin) and

Meliponini (stingless bees). Sounds that have been

described as tooting, quacking, hissing and piping serve

various social functions in Apini and Bombini (Hrncir et al.

2006), but neither taxon is known from before the Cenozoic

(Engel 2001). Stingless bees are known from the Upper

Cretaceous (Engel 2001). Stingless bees share with Apini

and Bombini the tendency for foragers to use thoracic

pulsation to make sounds that stimulate nestmates to fly out

– sometimes after first buzzing in response – and collect

food (Hrncir et al. 2006). If thoracic pulsation is a

behavioural symplesiomorphy for stingless bees, honeybees

and bumblebees, then it was present at least as early as the

Upper Cretaceous. Bees lack tympanic ears and sense the

sounds of conspecifics via substrate-borne vibrations and via

mechanoreceptors in the antennae that detect air movement

caused by the vibrations of the wings of conspecifics

engaging in thoracic pulsation (Hrncir et al. 2006).

Ants (Formicidae) are also members of Aculeata.

The earliest known ants are from the Cretaceous Period

and include members of four extant subfamilies:

Ponerinae (trap-jaw ants and kin), Dolichoderinae (cone

ants and kin), Formicinae (carpenter ants, wood ants and

kin), and Myrmicinae (harvester ants, fire ants and kin)

(Moreau et al. 2006). The earliest known fossil records of

the former two subfamilies are from the Lower

Cretaceous, and those of the latter two are from the

Upper Cretaceous (Moreau et al. 2006). Some dolicho-

derine and formicine ant workers tap their mandibles and

abdomens on the substrate to produce alarm sounds in

response to nest disturbance (Holldobler and Wilson

1990). Stridulation is used by ponerine and myrmicine

ants – especially in soil-dwelling species – for group

cohesion, warning of danger, as a call for help by wounded

or imperiled individuals, and as a signal by females to

males that copulation is complete (Dumortier 1963a;

Holldobler and Wilson 1990). Stridulation occurs by

rubbing the last segment of the petiole against the striated

dorsal edge of the first segment of the gaster in Ponerinae

and Myrmicinae (Dumortier 1963b); in some myrmicines

this is coupled with the rubbing of a second, ventral

stridulatory apparatus at the joint between the same two

segments (Dumortier 1963b). In small ant species

stridulation is inaudible to humans further away than a

few centimetres, but in large members of Ponerinae and

Myrmicinae it can be audible further away (Dumortier

1963b,c). Ants themselves are deaf to airborne sounds and

detect conspecific stridulation via substrate-borne

vibrations (Holldobler and Wilson 1990).

Stridulation between edges of abdominal segments is

also known in some members of Mutillidae (velvet-ants)

(Dumortier 1963b; O’Neill 2001), an aculeate family

known from as early as the Upper Cretaceous (Ross and

Jarzembowski 1993). In some species the male makes a

honking sound by vibrations of the wings and thorax as he

approaches the female, and both members of the pair

alternately stridulate during copulation (O’Neill 2001).

Flies, gnats and mosquitoes (Diptera)

Dipterans are known from as early as the Middle Triassic

(Blagoderov et al. 2002). Audible wing vibration by the

male during mounting is widespread in Diptera (Kanmiya

2006). In addition, many dipterans use flight sounds as a

means of intraspecific communication. Male mosquitoes

(Culicidae) have a hearing apparatus in the antennae,

which is used to find the female by her flight hum and to

keep together in all-male swarms (Sotavalta 1963); the

earliest known mosquitoes are from the Cretaceous

(Grimaldi et al. 2002a,b). Male hover flies (Syrphidae)

P. Senter268


court females by flying with a high-pitched hum over a

female on a flower (Sotavalta 1963); the earliest known

hover flies are from the Upper Cretaceous (Blagoderov

et al. 2002).

Other dipteran families with audible flight sounds and

known pre-Cenozoic fossils include Bombyliidae (bee

flies), Tabanidae (horse flies), and bottle flies (Calliphor-

idae). The oldest known members of Bombyliidae and

Tabanidae are from the Lower Cretaceous, and the oldest

known member of Calliphoridae is from the Upper

Cretaceous (Blagoderov et al. 2002). In some dipterans,

morphology and flight sounds mimic those of stinging

hymenopterans, apparently to deter predators (Chapman

1975). Such mimicry is unlikely to have arisen before the

appearance of stinging hymenopterans, which occurred in

the Upper Jurassic (Grimaldi and Engel 2005).


Restudy of fossil insects – especially those that are well

preserved in amber – to search for potentially overlooked

bioacoustical structures might be worthwhile. A search for

stridulatory structures, highly sclerotised ventral surfaces

(for percussion), and other sound-producing structures

could prove informative. Phylogenetic studies to deter-

mine homologies between sound-producing parts could be

used to constrain phylogenetic levels at which homologous

sound production occurred within given insect taxa, and

fossils could then be used to constrain the times of origin

of such sounds. For this, a set of reliable phylogenies

incorporating these fossil taxa would be necessary to

determine historical homology as opposed to convergence.

It would also be interesting to examine sound-producing

and auditory parts of extant insects for correlations

between morphology and dominant frequencies, and to

apply the results to fossils to determine more precisely the

nature of the sounds produced and heard by fossil insects

(e.g. Rust et al. 1999).

Pre-Cenozoic vertebrate paleobioacoustics

Non-bony fishes

In vertebrates the inner ear exhibits a number of separate

neuromast organs, some of which are used for 3D

orientation and some of which are used for sound reception

(Ladich and Popper 2004). Sound reception has not been

demonstrated in the basal taxa Myxini (hagfishes) and

Petromyzontida (lampreys) but is present in Gnathosto-

mata (jawed vertebrates) (Ladich and Popper 2004). It may

have appeared independently in cartilaginous fishes

(Gnathostomata: Chondrichthyes) and bony fishes

(Gnathostomata: Osteichthyes) because the former use a

neuromast organ called the macula neglecta for hearing,

whereas in the latter the macula neglecta is reduced

or absent and other parts of the inner ear are used for

hearing (Popper et al. 1992; Ladich and Popper 2004).

Cartilaginous fishes are generally silent (Hueter et al.

2004). An exception is the cownose ray (Rhinoptera

bonasus), which emits clicks in response to a human touch

(Fish and Mowbray 1970). The cownose ray is a member

of the family Myliobatidae, the earliest known members of

which are from the latest Cretaceous (Campanian-

Maastrichtian) (Cappetta 1987).

Hearing has been demonstrated in Elasmobranchii

(sharks and rays) but has not been studied in Holocephali

(ratfishes). Elasmobranchs are known from as early as the

Lower Devonian (Cappetta et al. 1993), so it is possible

that anti-predator sounds directed at them existed by the

late Paleozoic.

Lobe-finned fishes (Osteichthyes: Sarcopterygii)

Extant lungfishes (Sarcopterygii: Dipnoi) are generally

silent, although the Australian lungfish (Neoceratodus

forsteri) is known to breathe air noisily and to do it more

frequently during the breeding season, sometimes in

concert in the evening (Kemp 1986). The sound is more

likely incidental than of use in intraspecific communi-

cation, because lungfishes lack specialisations for airborne

sound reception. Incidental air-breathing sounds that

resemble whistling and clucking are also known in extant

salamanders (Maslin 1950), so the phenomenon is not

limited to sarcopterygians outside Tetrapoda. Sarcopter-

ygians are known from as early as the Upper Silurian

(Zhu et al. 2009), so the incidental sounds of air their

breathing may have existed that early.

Ray-finned bony fishes (Osteichthyes: Actinopterygii)

Many actinopterygian taxa produce grunts, clicks, squeaks,

whistles and other sounds for intraspecific communication

and when disturbed or apprehended (Fish and Mowbray

1970; Myrberg 1981; Ladich and Bass 2003). Such sounds

are typically produced by muscular vibration of the gas

bladder, but in some species sound production is

accomplished by tendon snapping, pectoral girdle vibration,

stridulation of pharyngeal teeth, or other methods (Ladich

and Bass 2003). Actinopterygian acoustic behaviour has

been studied mainly in teleosts (Teleostei). Not all teleosts

are known to make sounds, and the variety of their sound

production mechanisms indicates that acoustic communi-

cation evolved independently in several lineages (Schneider

1967; Ladich and Bass 2003). In addition to teleosts,

acoustic communication is known in basal ray-finned

groups such as sturgeons (Acipenseridae) and bichirs

(Polypteridae) (Johnston and Phillips 2003; Ladich and

Bass 2003). Although the known fossil records of extant

ray-finned fish families that communicate acoustically go

back no further than the Upper Jurassic (Table 5), those



families phylogenetically bracket taxa from as early as the

Upper Devonian (Carroll 1988; Grande and Bemis 1996).

The sounds of actinopterygian communication may there-

fore have existed through the late Paleozoic and Mesozoic.

Basal ray-finned fishes must have been present by the

Upper Silurian, because Sarcopterygii, the sister taxon to

Actinpterygii, was present then (Zhu et al. 2009). The lungs

of extant basal actinopterygians may be homologous with

those of lungfishes (Kardong 2006), in which case the

sound of noisy air-breathing by ray-finned fishes may have

existed alongside that of their lobe-finned counterparts as

early as the Upper Silurian.

Underwater hearing is present in actinopterygians in

general. A number of teleost taxa, known as hearing

specialists, independently evolved connections between

the gas bladder and the inner ear (Ladich and Bass 2003).

This increases the upper frequency range through which

underwater sounds can be heard (Yan et al. 2000; Ladich

and Bass 2003). Accordingly, sounds made by hearing

specialist fishes are of higher frequency than those of other

fishes (Figure 3) (Ladich and Bass 2003). Hearing

specialist taxa include Otophysi (carp, catfishes and kin),

Anabantoidea (gouramis and kin), Mormyridae (mormyr-

ids) and Holocentridae (squirrelfishes) (Ladich and Bass

2003). Hearing specialist fishes typically inhabit quiet,

shallow water, which enhances high-frequency sound

transmission (Ladich and Bass 2003). It stands to reason,

then, that high-frequency acoustic behaviour of fossil

actinopterygians would have been more prevalent in quiet,

shallow water than in noisy or deep water. The earliest

known members of extant hearing specialist fish taxa are

from the Upper Cretaceous (Table 5).

Basal tetrapods (Tetrapoda)

In basal tetrapods a bone called the stapes served as a brace

between the palate and braincase (Clack 1992). The stapes of

most extant frogs (Anura) and amniotes (Amniota) has been

reoriented so that it couples the inner ear to a tympanum,

enabling detection of airborne sounds. The sound-sensitive

region of the inner ear is homologous in Anura and Amniota

(Fritzsch 1992) but its coupling to a tympanum evolved

separately in the ancestors of extant frogs, diapsids

(Amniota: Diapsida) and mammals (Amniota: Mammalia)

(Bolt and Lombard 1985; Carroll 1991; Clack and Allin

2004) (Figure 4). The earliest tetrapod skulls exhibit

posterior notches that are often called otic (ear) notches

because they superficially resemble the posterior skull

notches that house tympana in extant frogs and amniotes.

However, early tetrapod stapedial and otic morphology are

inconsistent with tympanic hearing (Clack et al. 2003).

The bony architecture of the notches indicates that they

housed spiracles, not tympana (Brazeau and Ahlberg 2006).

Even so, early tetrapod inner ears probably detected low-

frequency water- and substrate-borne sounds, as do the

atympanic ears of extant fishes, salamanders and caecilians

(Smotherman and Narins 2004; McCormick 1999; Ladich

and Bass 2003).

The early tetrapod Ichthyostega exhibits otic modifi-

cations analogous to those of hearing-specialist fishes.

Uniquely among basal tetrapods, its skull appears to have

had an air-filled otic chamber and a mobile stapes with a

morphology and position conducive to sound conduction

from the air-filled chamber to the inner ear (Clack et al.

2003). The otic chamber apparently functioned as a

resonator for high-frequency sounds, as does the gas bladder

of hearing specialist fishes, which raises the possibility of

high-frequency sonic communication in Ichthyostega.

Among members of Lissamphibia (the smallest clade

including extant amphibians and all taxa phylogenetically

bracketed by them), tympanic ears are present inmost extant

frogs (Anura) but are absent in basal frogs (Ascaphidae and

Leiopelmatidae), caecilians (Gymnophiona) and salaman-

ders (Caudata) (Bogert 1958; Smotherman and Narins

2004). This suggests that the lissamphibian ancestor lacked

tympanic ears and that within Lissamphibia tympanic ears

are a synapomorphy of derived frogs. This interpretation is

compatible with all three of the competing hypotheses of

lissamphibian origins. According to one hypothesis,

Lissamphibia arose from within the otherwise Paleozoic

Table 5. Families of sound-producing fishes that are known from before the Cenozoic, and details about their sounds.

Family Earliest record Description of sound Function of sound Mechanism, if known

Acipenseridae (sturgeons) Upper Cretaceous Squeak, chirp, knock, groan – –Albulidae (bonefishes) Upper Cretaceous Click, scratch, knock R –Ariidae (HS) (marine catfishes) Upper Cretaceous Grunt, creak, yelp R EElopidae (tarpons) Upper Jurassic Thump R SGadidae (cods) Upper Cretaceous Grunt A, C, G, R INHolocentridae (HS) (squirrelfishes) Upper Cretaceous Staccato, grunt A, R, G EMyliobatidae (eagle rays) Upper Cretaceous Click R IOphidiidae (cusk-eels) Upper Cretaceous – – –Polypteridae (bichirs) Upper Cretaceous Thump, moan A, R I

A, aggression; C, courtship; E, contraction of extrinsic swim bladder muscles; G, group coordination; HS, hearing specialist; I, sound produced by unknown internal mechanism;IN, contraction of intrinsic swim bladder muscles; R, response to predator, human touch, or startling; S, sound made by swimming. References: Myrberg 1981; Cappetta 1987;Ladich and Tadler 1988; Arratia 1993; Meunier and Gayet 1993; Nolf and Stringer 1993; Patterson 1993; Schwarzhans 1993; Stewart 1993; Johnston and Phillips 2003; Ladichand Bass 2003; Wilson et al. 2003.

P. Senter270


clade Lepospondyli (Laurin and Reisz 1995, 1997, 1999;

Laurin 1998; Vallin and Laurin 2004). According to the

second hypothesis, Lissamphibia arose from within the

otherwise mostly Paleozoic and Triassic clade Temnospon-

dyli (Milner 1988; Trueb and Cloutier 1991; Ruta et al.

2003). According to the third hypothesis, frogs and

salamanders arose from within tymnospondyli but caeci-

lians arose from within Lepospondyli (Carroll 2007;

Anderson et al. 2008). Lepospondyls show no osteological

evidence of tympanic ears (Clack and Allin 2004). Many

temnospondyls exhibit posterior cranial notches that have

been interpreted as having housed tympana (Clack and Allin

2004). However, recent studies show that the morphology of

the temporal area and the massive size of the stapes in

temnospondyls are incompatible with the presence of a

tympanum; the notchesmore likely housed spiracles (Laurin

1998; Laurin and Soler-Gijon 2006). The common ancestor

of extant amphibians therefore lacked tympanic ears,

regardless of which phylogenetic hypothesis is correct.

Many large temnospondyls had large heads like those of

extant crocodilians (Romer 1947), which acoustically

advertise presence by slapping their heads on the water

(Vliet 1989; Thorbjarnarson 1991; Thorbjarnarson and

Hernandez 1993). It is therefore tempting to imagine large-

headed temnospondyls employing the same communication

device. Had they done so, their underwater hearing would

have detected the sound and their lateral line systems

(Romer 1947) would have detected the location of its source

(Coombs and Braun 2003), even without tympana.

However, the extreme proximity between shoulder girdle

and skull in temnospondyls and other non-amniote tetrapods

made the neck extremely short (Romer 1947), so it is

unlikely that they could have raised their heads enough to

have performed crocodilian-style head-slaps.

This does not necessarily mean that extinct temnos-

pondyls and other basal tetrapods were silent. It is possible

that they performed other activities involving audible

water displacement. Also, several extant salamander

species – which lack tympanic ears – produce airborne

anti-predator sounds in response to capture (Maslin 1950).

Such defensive sound production may have evolved

convergently in extinct basal tetrapods after the appear-

ance of tympanic ears in their predators. Many extant

lissamphibians that make such sounds produce noxious

chemicals that discourage or even kill predators (Duell-

man and Trueb 1994). Others, such as amphiumas

(Amphiumidae), can deliver a painful bite. Lissamphibian

anti-predator sounds may therefore be honest warnings to

predators (Duellman and Trueb 1994), as is the case with

stridulating insects (Masters 1979). Noxious chemical

production in extinct temnospondyls cannot be evaluated,

but cranial and dental morphology of many temnospondyls

indicates the ability to produce a nasty bite, so they may

have made honest warning sounds. While the earliest

known predators with tympanic ears are Lower Permian

seymouriamorphs (Ivakhnenko 1987) (Figure 6), basal

tetrapod anti-predator sounds directed at fishes may have

existed before then.

Mechanisms of defensive sound production in extant

salamanders are listed in Table 6. Among extant salamander

families, Cryptobranchidae (giant salamanders) and

Amphiumidae (amphiumas) have a pre-Cenozoic fossil

record. The former are known from the Middle Jurassic of

China (Gao and Shubin 2003) and the latter from the Upper

Cretaceous of North America (Milner 1993). It is therefore

possible that their characteristic defensive sounds existed

before the Cenozoic.

Arthropod stridulation in response to seizure by

tetrapod predators began at the earliest in the Mississip-

pian, at which time the earliest insectivorous tetrapods

Figure 6. Estimated times of origin of sounds and tympanic earsin various animal lineages. See text for information sources.RPE, rampant parallel evolution of.



appeared (Hotton et al. 1997). Mississippian tetrapods

lacked tympanic ears (see below) and therefore would

have been deterred by the substrate-transmitted mechan-

ical vibrations produced by stridulation, rather than by the

resulting sounds. Predator deterrence by airborne stridu-

latory sounds would have been effective only after the

appearance of tympanic ears in predatory tetrapods in the

Permian (see below).

Frogs (Lissamphibia: Anura)

In lunged fishes, including lungfishes, the glottis (the

opening in the pharynx that leads to the lung) is ringed by a

muscular sphincter that closes the glottis (Negus 1949).

To this arrangement tetrapods have added the larynx

(Figure 1), an organ made of cartilage bodies (arytenoid

cartilages cranially and cricoid cartilages caudally) that

function as attachment sites formuscles that open the glottis

(Negus 1949;Kelemen 1963). In anurans paired vocal cords

extend into the lumen from the arytenoid part of the larynx

and are vibrated to produce vocalisation during forced

expulsion of air from the lungs (Kelemen 1963), or during

inspiration in Bombina (Duellman and Trueb 1994).

Members of Pipidae (clawed frogs) are exceptions; they

lack vocal cords but produce a clicking noise by means of

the sudden popping movement of a pair of articulating

cartilage disks attached to bony rods inside the larynx

(Duellman and Trueb 1994). In most frogs, males possess a

gular vocal sac that resonates and radiates the sound

(Duellman and Trueb 1994).

Members of most families of anurans make anti-

predator distress calls when disturbed (Bogert 1958). This

is true even of basal taxa such as Leiopelma in which

tympana, vocal sacs and courtship vocalisations are absent

(Bogert 1958). Mesozoic anurans may therefore have

made anti-predator sounds before they acquired tympanic

ears. Basal crown-group frogs are known from the Upper

Jurassic of Argentina (Henrici 1998), so anuran anti-

predator sounds may have existed that early.

Tympanic ears and chorusing behaviour are present in

the anuran clades Discoglossidae (midwife toads),

Mesobatrachia (spadefoot toads, clawed frogs and their

relatives) and Neobatrachia (typical frogs, tree frogs, true

toads and their relatives), and therefore may be

symplesiomorphies of higher anurans. Discoglossoids

and mesobatrachians are known from Laurasia as early as

the Upper Jurassic (Henrici 1998) and from Gondwana as

early as the Early Cretaceous (Baez et al. 2000). Anuran

chorusing therefore likely arose on those landmasses by

those times. The only known Mesozoic members of

Neobatrachia are South American members of Leptodac-

tylidae from the Upper Cretaceous (Sanchiz 1998).

Because no members of arboreal anuran clades are

known from the Mesozoic, we can safely infer that

Mesozoic anuran choruses took place at ground level.

During choruses, male anurans call to attract mates

(advertisement calls) and also emit special aggressive calls

in response to the loud vocalisations of nearby male

neighbours (Schwartz 2001). Aggressive calls may differ

qualitatively or quantitatively from advertisement calls

(Schwartz 2001). Females of many anuran species prefer

males whose calls are louder, delivered at higher rates, and

delivered for longer periods; in fact, male anurans often

increase these parameters in their own calls in response to

the calls of rivals (Schwartz 2001). If such directional

selection by female choice was present through anuran

geological history, then Mesozoic anuran calls exhibited

lower amplitude, rate and duration than extant anuran calls.

During choruses, male frogs tend to vocalise during the

silences between calls of nearby conspecifics – or, for

species with multi-note calls, if the songs overlap, notes are

sung by one individual between the notes sung by another

(Schwartz 2001). Such vocal alternation enables males to

detect each other’s calls and enables females to discriminate

between individual males’ calls (Schwartz 2001). If vocal

alternation during anuran chorusing evolved by means of

directional selection, we can safely infer that it was absent

or poor in the earliest anuran choruses.

Table 6. Mechanisms of defensive sound production by extant salamanders (Maslin 1950).

Family Description of sound Mechanism (if known)

Ambystomatidae (mole salamanders) Grunt Laryngeal vocal cordsClick, kissing sound Forcefully opening mouth (sound produced by

breakage of moist seal around mouth)Amphiumidae (amphiumas) Whistle, peep Forcing air through gill slits

Cryptobranchidae (giant salamanders)Cry similar to that of ahuman infant

–

Dicamptodontidae (mole salamanders) Bark Laryngeal vocal cordsPlethodontidae (lungless salamanders) Squeak –Proteidae (mudpuppies) Hiss –

Salamandridae (newts and kin) Peep, squeak, kissing soundForcefully opening mouth (sound produced bybreakage of moist seal around mouth)

Sirenidae (sirens) Croak, hiss –

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Extinct basal tetrapods with tympanic ears

Skull and the stapes morphology preclude tympana in

most basal tetrapods, including basal amniotes (Reisz

1981; Carroll 1991; Laurin 1998; Clack and Allin 2004;

Laurin and Soler-Gijon 2006), but there were exceptions.

A rodlike stapes oriented toward a strongly embayed

posterior skull notch suggests a tympanic ear in the Lower

and Upper Permian taxon Seymouriamorpha (Ivakhnenko

1987), which is phylogenetically intermediate between

Temnospondyli and Amniota (Laurin 1998; Laurin and

Reisz 1999; Ruta et al. 2003) (Figure 4). A posterior skull

embayment that suggests a tympanum is also present in the

Upper Carboniferous and Lower Permian taxon Diadecto-

morpha (Berman et al. 1992). Diadectomorpha is

phylogenetically positioned immediately outside Amniota

(Laurin and Reisz 1995; Ruta et al. 2003) (Figure 4).

A reduced stapes and a posterior skull embayment that

suggest a tympanum are present in most members of

Parareptilia, a clade of dumpy-looking basal amniotes

from the Permian and Triassic (Carroll and Lindsay 1985;

Laurin and Reisz 1995; Tsuji 2006; Muller and Tsuji

2007). The embayment is absent in Mesosauridae, the

most basal parareptilian group, and its presence is a

synapomorphy of higher parareptiles (Laurin and Reisz

1995; Tsuji 2006). Within Parareptilia the otic embayment

is particularly well developed in the Upper Permian and

Triassic clade Procolophonoidea and a Middle Permian

clade informally called ‘nycteroleters’ (Carroll and

Lindsay 1985; Muller and Tsuji 2007). The orbits are

enlarged in both groups, suggesting crepuscular or

nocturnal habits, hence occupation of a visually compro-

mised niche, to which the enhanced auditory apparatus

may be functionally related (Muller and Tsuji 2007).

Taxa without tympanic ears fill the phylogenetic gaps

between Seymouriamorpha, Diadectomorpha and Pararep-

tilia, and also between these taxa and other amniote taxa

with tympanic ears (Figure 4). Such ears therefore appeared

independently in each group. The presence of tympanic ears

in Seymouriamorpha, Diadectomorpha and Parareptilia

made possible the use of airborne sounds in intraspecific

communication. However, there is no certainty that it

occurred. These groups may have used their tympanic ears

for other functions instead of (or in addition to) intraspecific

communication. Seymouriamorphs were carnivorous

(Hotton et al. 1997) and may therefore have used hearing

to locate prey. A prey-locating function is unlikely in the

largely herbivorous clades Diadectomorpha and Pararepti-

lia. All three taxa may have used hearing for predator

avoidance, as do extant reptiles (Greene 1988).

Lower Permian seymouriamorphs are the earliest

known animals with tympanic ears that preyed on

vertebrates. The earliest airborne, anti-predator sounds

made by vertebrates may therefore have been directed at

Lower Permian seymouriamorphs.

Turtles (Reptilia: Testudines)

Turtles and tortoises are usually silent but do occasionally

make sounds by unknown means. During copulation or

while chasing the female, males often make sounds that

have been described as grunts, groans, moans, bellows and

roars (Gans and Maderson 1973; Auffenberg 1977). Such

mating sounds are little studied but are known from such a

wide taxonomic spectrum of turtle families (Campbell and

Evans 1972; Gans and Maderson 1973) that all extant

turtles are phylogenetically bracketed by taxa known to

produce mating sounds (Shaffer et al. 1997). This suggests

that turtle mating sounds were present in the common

ancestor of crown group turtles, which appeared in the

Lower Jurassic (Rougier et al. 1995). Osteological

correlates of hearing in extant turtles are also present in

the Upper Triassic and Lower Jurassic family Australo-

chelidae, the sister taxon to the turtle crown clade

(Gaffney and Kitching 1990). The situation is ambiguous

in the Upper Triassic taxon Proganochelys, the most basal

known fossil turtle, because of poor preservation in the

relevant region of the skull (Gaffney 1990).

The morphology of the tympanic region of the turtle

skull strongly resembles that of some parareptiles, and the

same pair of bones (squamosal and quadratojugal) supports

the tympanum in both groups (Carroll and Lindsay 1985;

Laurin and Reisz 1995; Rougier et al. 1995; Tsuji 2006).

If turtles arose from within Parareptilia (Laurin and Reisz

1995; Lee 1997a,b), then the tympanic ears of turtles are

probably homologous with those of parareptiles. This

introduces the possibility that parareptiles made turtle-like

courtship and mating sounds, in which case such sounds

may have existed as early as the Permian.

While some phylogenetic analyses of morphological

data place turtles within Parareptilia (Laurin and Reisz

1995; Lee 1997a,b), others place them just outside Diapsida

(Gauthier et al. 1988) or within crown Diapsida (Rieppel

and deBraga 1996; deBraga and Rieppel 1997). Curiously,

molecular analyses usually place them within or closely

related to the diapsid taxon Archosauria (Mannen et al.

1997; Platz and Conlon 1997; Hedges and Poling 1999;

Zardoya and Meyer 2001), for which there is no

documented morphological support, although one recent

molecular study places turtles in a phylogenetic position

compatible with parareptile status (Frost et al. 2006). If

turtles are diapsids then their tympanic ears are homologous

with those of other diapsids and not with those of

parareptiles.

Lizards and kin (Diapsida: Lepidosauromorpha)

Within the amniote taxon Diapsida are two major clades:

Lepidosauromorpha (lizards, tuataras and extinct kin) and

Archosauromorpha (crocodilians, birds and extinct kin,

including dinosaurs and pterosaurs) (Benton 1985)

(Figure 4). Extinct diapsids basal to the clade



Lepidosauromorpha þ Archosauromorpha lacked tympanic

ears (Reisz 1981; Clack and Allin 2004). Extant lepidosaur-

omorphs and archosauromorphs possess tympanic ears,

except for some in which tympanic ears have been lost:

snakes (Serpentes), amphisbaenians (Amphisbaenia), Cali-

fornia legless lizards (Anniella), chameleons (Chamaeleoni-

dae) and tuataras (Sphenodon) (Wever 1978). Most such

groups are subterranean and therefore have no need for

airbornehearing (Wever 1978).Whilemost extant snakes are

not subterranean, their ancestors probablywere subterranean

or aquatic (Apesteguıa and Zaher 2006; Palci and Caldwell

2007), so their lack of tympanic ears is a vestige of ancestry.

Basal lepidosauromorphs and archosauromorphs exhi-

bit osteological evidence of tympanic ears (posteriorly

embayed quadrate, thin stapes) (Gregory 1945; Robinson

1962; Kuhn-Schnyder and Peyer 1973; Carroll 1975;

Gow 1975; Evans 1980; Dilkes 1998), which suggests

inheritance from a common ancestor. A recently published

inference that the two lineages acquired tympanic ears

separately is based on the assumption that the basal diapsid

Youngina – which lacks evidence for tympanic ears – is a

basal lepidosauromorph (Clack and Allin 2004). However,

recent phylogenetic analyses place Youngina outside the

lepidosauromorph-archosauromorph clade (Laurin 1991;

Rieppel and deBraga 1996; Lee 1997a,b; Modesto and

Reisz 2002; Senter 2004). Enlarged orbits in basal

lepidosauromorphs and archosauromorphs (Robinson

1962; Kuhn-Schnyder and Peyer 1973; Carroll 1975;

Gow 1975; Evans 1980, Evans 1991; Modesto and Reisz

2002) suggest crepuscular or nocturnal habits, an

interpretation supported by the fact that a reconstructed

ancestral archosaur visual pigment seems made for low

light levels (Chang et al. 2002). As with parareptiles

(Muller and Tsuji 2007), the enhancement of hearing in

these animals may be functionally related to ancestral

occupation of a visually compromised niche.

The earliest known lepidosauromorphs and archosaur-

omorphs are from the Upper Permian (Carroll 1975; Evans

and King 1993). Whether or not the two groups acquired

airborne hearing independently, it was present in both by

then. Anti-predator sounds directed at diapsids may

therefore have appeared in the Upper Permian. The small,

peglike teeth of many basal diapsids, including basal

lepidosauromorphs and basal archosauromorphs, suggest

a diet of invertebrates (Colbert 1970; Carroll 1975;

Gow 1975; Evans 1980). Anti-predator sounds directed at

Permian diapsids may therefore have included stridulation

by arachnids and beetles.

The ability to hear airborne sounds allows acoustic

communication, but among extant lizard families with

Mesozoic records only geckoes (Gekkonidae and Euble-

pharidae) vocalise. Using laryngeal vocal cords, geckoes

make sounds that are described as squeaks, growls and

barks, which carry only for a few meters in some cases and

as far as 20m in others (Gans and Maderson 1973;

Marcellini 1977). Single chirps are used for threat calls

(when lunging at a predator or conspecific rival) and

distress calls (upon being attacked or grasped), both in

nocturnal and diurnal geckoes (Marcellini 1977). Tem-

porally patterned multiple chirps are used by nocturnal

geckoes, usually males, in intraspecific social situations

(Marcellini 1977). Multiple chirps are produced at the

beginning of the nocturnal activity period, and may be

uttered in response to other individuals’ calls, in response

to the sight of rival males, and during courtship (Marcellini

1977). Multiple chirp calls vary between species and

appear to be related to spacing and territory (Marcellini

1977). The earliest known geckoes are from the Aptian-

Albian (Lower Cretaceous) of Mongolia (Alifanov 1989),

and it is possible that gecko calls were present then.

The lepidosauromorph taxon Sphenodontia is today

represented by only one genus: Sphenodon (tuataras).

Tuataras croak loudly when disturbed (Gans and Wever

1976). Sphenodontians are known from as early as the

Upper Triassic (Fraser 1982). Sphenodon lacks tympana

and has lost the embayment in the quadrate bone that is

associated with the tympanum in lizards. The embayment

is present in basal sphenodontians (Evans 1980; Fraser

1982; Wu 1994) but was lost in the lineage leading to

Sphenodon by the Lower Jurassic (Reynoso and Clark

1998). The loss of tympanic ears indicates that the use of

airborne sounds for intraspecific communication was not

important in the lineage.

Without tympanic ears extant tuataras have trouble

hearing airborne sounds over 1 kHz but can hear their own

croaks, which are of appropriate frequency (Gans and

Wever 1976) (Figure 3). Tuataras are not known to vocalise

for intraspecific communication, but the fact that they

can hear their own voices suggests that they have the

equipmentwithwhich to do so, evenwithout tympanic ears.

This fact might tempt the researcher to conclude that basal,

terrestrial tetrapods without tympanic ears may have used

low-frequency vocalisations for intraspecific communi-

cation. However, such temptation should be resisted.

The loss of the tympanum in extant reptiles results not only

in a limitation of auditory sensitivity to low-frequency

sounds (Figure 3), but also results in an inability to hear

such sounds except at very high amplitudes (Wever 1978).

Snakes are exceptions to this rule, because they can hear

low-frequency sounds at low amplitudes (Wever 1978).

However, the example of the snake’s ear is inapplicable to

basal tetrapods, for two reasons. First, the quadrate bone of

a snake’s skull (Figure 1) is so loose that it vibrates

freely and has essentially become a bony tympanum

(Wever 1978), whereas no posterior skull bonewas loose in

basal tetrapods. Second, the stapes of a snake is slender and

contacts the quadrate as if contacting a tympanum (Wever

1978) (Figure 1), whereas the basal tetrapod stapes was a

robust, solid brace between the bones of the cheek or palate

and the braincase (Carroll 1986; Clack 1992).

P. Senter274


Mesozoic marine reptiles

Stapedial and posterior skull morphology indicate

retention of tympanic ears in Nothosauria, a marine

archosauromorph clade from the Triassic Period

(Carroll and Gaskill 1985). This indicates an ability to

hear airborne sounds in these animals, despite their aquatic

habits. In Plesiosauria, a Mesozoic marine taxon closely

related to Nothosauria, a thin stapes suggests evolution

from an ancestor with tympanic ears (Hetherington 2008).

However, posterior skull morphology indicates that the

tympanum was lost in Plesiosauria (Carpenter 1997;

Storrs 1997; Hetherington 2008).

A tympanic notch is absent in the Mesozoic marine

taxon Ichthyosauria (Maisch 1997), which may or may not

be a member of Diapsida (Maisch 1997; Motani et al.

1998). The ichthyosaur stapes is robust and serves as a

brace between the cheek and braincase (Hetherington

2008), as in basal amniotes (Clack and Allin 2004). This

suggests that ichthyosaur ancestors never passed through a

stage with tympanic ears. The lack of tympanic ears in

plesiosaurs and ichthyosaurs does not necessarily mean

that they were deaf to underwater sounds but does indicate

a lack of importance of airborne sounds to them.

Mosasauridae, a marine family of Upper Cretaceous

lizards, retained tympanic ears, but they were modified for

underwater sound reception. The tympanum was often

ossified, increasing resistance to rupture in deep water

(Russell 1967). The middle ear cavity was encased in bone

and lacked acoustic isolation from the rest of the skull,

allowing the skull to conduct sound to the middle ear

(Hetherington 2008). Underwater hearing was therefore

apparently important to mosasaurs. It is impossible to

know, however, whether mosasaur hearing was of

importance in prey localisation, avoidance of dangerous

animals emitting honest sonic warnings, intraspecific

communication, or a combination of factors.

Crocodilians and kin (Archosauromorpha: Archosauria:Crurotarsi)

Basal diapsids appear to have been insectivorous, but the

serrated, ziphodont teeth of the archosauromorph clade

Archosauriformes indicate a switch to a diet of vertebrates

(Senter 2003). Archosauriformes exploded in diversity in

the Triassic Period but at least one of its basal members

was present in the Upper Permian (Hughes 1963). Anti-

predator sounds from vertebrates, directed at archosauri-

forms, may therefore have been present that early.

Members of Archosauria, the archosauriform crown

clade, are known from as early as the Middle Triassic

(Sereno 1991). Archosauria includes two major lineages,

Crurotarsi and Ornithodira (Sereno 1991) (Figure 4).

Crurotarsi includes crocodilians (Crocodylia) and several

extinct, mostly Triassic taxa (Sereno 1991). Ornithodira

includes dinosaurs (Dinosauria) – including birds (Aves)

– and pterosaurs (Pterosauria) and a few other extinct

forms (Sereno 1991). The vocal organ in extant members

of Crurotarsi (crocodilians) is the larynx, whereas in extant

members of Ornithodira (birds) it is the syrinx. Because

the larynx and syrinx are not homologous, it is most

parsimonious to infer that vocalisation arose indepen-

dently in the two lineages, in which case their common

ancestor lacked vocal ability.

Crocodilians vocalise by vibrating three mucosal

folds – absent in the avian larynx (McLelland 1989a,b) –

that project into the laryngeal lumen under part of the

arytenoid cartilage (Reese 1914). Unlike the avian syrinx

(see below), the crocodilian vocal organ leaves no trace of

its presence on fossil skeletons, so it is impossible to know

whether vocalisation was present further down the

crurotarsian tree than Crocodylia. We therefore cannot

know whether the Triassic and Jurassic Periods were filled

with the roaring of basal crurotarsians.

On the other hand, we can infer that the homologous

acoustic behaviours of gharials (Gavialidae), crocodiles

(Crocodylidae), alligators and caimans (Alligatoridae)

were present in their common ancestor (Senter 2008),

which appeared in the Upper Cretaceous (Brochu 2003).

Juvenile crocodilians of all three groups squeak or grunt

when disturbed, sometimes even from within the egg if the

nest is disturbed, and the sound attracts adults

(Modha 1967; Whitaker and Basu 1982; Cintra 1989;

Whitaker and Whitaker 1989). Adult males of all three

groups engage in head-slapping, in which the head is

raised and then slammed downward onto the water’s

surface to create a loud splash that is often followed by a

hiss in gharials or a roar in alligators and crocodiles

(Garrick et al. 1978; Whitaker and Basu 1982;

Thorbjarnarson 1991; Thorbjarnarson and Hernandez

1993). The head-slap is used in displays of presence and

dominance and in courtship (Garrick et al. 1978;

Thorbjarnarson 1989; Whitaker and Whitaker 1989).

Courtship in gharials, alligators and crocodiles also

involves geysering (shooting jets of water upward from

the nostrils, which are held just below the surface) and

blowing bubbles in the water with the mouth (Garrick et al.

1978; Whitaker and Basu 1982; Thorbjarnarson 1989;

Whitaker and Whitaker 1989; Thorbjarnarson and

Hernandez 1993). Narial geysering is also used as a

territorial display (Modha 1967; Garrick et al. 1978).

Territorial fights between crocodilian males often involve

loud splashing as bodies are hurled against each other

(Modha 1967; Singh and Rao 1990).

The above are all water-based behaviours that would

obviously have been absent in the terrestrial precursors of

Crocodylia. Aquatic or semi-aquatic habits are character-

istic of a large clade, Neosuchia, which includes

Crocodylia and several extinct Mesozoic taxa

(Clark 1994). If the aquatic acoustic behaviours of

crocodilians were present further down neosuchian



phylogeny, they may have been present as early as the

Upper Jurassic, from which the earliest non-marine

neosuchians are known (Carroll 1988).

Most phylogenetic analyses place the marine taxon

Thalattosuchia within Neosuchia (e.g. Clark 1994; Ortega

et al. 2000; Sereno et al. 2001; Company et al. 2005).

Thalattosuchians, known from as early as the Lower

Jurassic (Carroll 1988), had narrow snouts (Clark 1994).

Thalattosuchian head-slapping, if it occurred, would

therefore have been weak for the sake of protecting the

narrow snout, as in the extant gharial (Whitaker and Basu

1982). Snouts were wider in most other extinct

neosuchians (Clark 1994), allowing strong head-slaps.

Head-slaps, if present, would have been particularly

impressive in the gigantic taxa Sarcosuchus and Deino-

suchus, in each of which head length approached 2m

(Sereno et al. 2001; Schwimmer 2002). Sarcosuchus is a

neosuchian from the Lower Cretaceous (Aptian-Albian) of

western Africa (Sereno et al. 2001), and Deinosuchus is an

alligatoroid from the Upper Cretaceous (Campanian) of

North America (Schwimmer 2002). Deinosuchus is more

certain than Sarcosuchus to have employed head-slapping

behaviour because Deinosuchus lies within Crocodylia

(Sereno et al. 2001), whereas Sarcosuchus does not (Sereno

et al. 2001). Also, Sarcosuchus is phylogenetically

bracketed by narrow-snouted forms (Sereno et al. 2001),

which increases the likelihood that head-slapping beha-

viour, if present that far back in neosuchian phylogeny, was

lost or weakened in the clade that includes Sarcosuchus.

Members of Alligatoridae (alligators and caimans)

employ both head-slapping and a vocal acoustic advertise-

ment display called bellowing (Garrick 1975; Garrick et al.

1978;Gorzula andSeijas 1989).Maleand femalealligatorids

bellow to advertise presence. Bellowing is contagious and its

sound is sexually dimorphic (Garrick 1975; Garrick et al.

1978). Alligatoridae is unknown before the Cenozoic

(Brochu 2003), but other members of Alligatoroidea, the

larger taxon that includes Alligatoridae but excludes

CrocodylidaeandGavialidae,werepresent inNorthAmerica

as early as the Campanian (Upper Cretaceous) (Brochu

1999). If basal alligatoroids bellowed, then the sound may

have been present in the Upper Cretaceous.

Birds and kin (Archosauria: Ornithodira)

The syrinx of birds (Ornithodira: Aves) is a series of

cartilage rings at the junction of the trachea and primary

bronchi, with membranous folds that protrude into the

lumen and can be vibrated to produce sound (Brackenbury

1989; King 1989). Vocal production by the syrinx depends

on the presence of a clavicular air sac (Brackenbury 1989),

a soft structure that invades and pneumatises the bones of

the avian pectoral girdle and limb, marking its presence

with a characteristic opening on the humerus (McLelland

1989a,b). Such an opening is present in members of the

avian clade Ornithothoraces – which includes modern

birds and the Lower and Upper Cretaceous taxon

Enantiornithes (Chiappe and Walker 2002) – but not in

birds basal to Ornithothoraces (Chiappe et al. 1999; Zhou

and Zhang 2003).

The clavicular air sac does not develop individually

but instead represents a fusion of outgrowths from two pre-

existing air sacs and a pair of outgrowths from the lungs.

The four outgrowths do not meet in the midline, in the

vicinity of the syrinx, until late in embryology (Locy and

Larsell 1916). The status of the clavicular air sac as an

outgrowth of pre-existing structures, two of which are

other air sacs, suggests that it is a later evolutionary

acquisition than the original set of ornithodiran air sacs.

This is consistent with the interpretation that it arrived

relatively late in ornithodiran history. Evidence exists that

non-avian ornithodirans, including basal birds, possessed

other air sacs homologous with those of birds (Britt et al.

1998; O’Connor 2006; Wedel 2006), but not the clavicular

air sac. Outside Ornithothoraces, humeral pneumatisation

is present in Pterosauria (O’Connor 2006) but not in the

many intervening dinosaurian taxa (Britt 1997). Humeral

pneumatisation in pterosaurs is therefore not homologous

with that of birds and so is not evidence for the presence of

a clavicular air sac homologous with that of birds.

Pneumatisation of the furcula is present in the allosauroid

theropod Aerosteon riocoloradensis, suggesting the pre-

sence of a clavicular air sac (Sereno et al. 2008). However,

such a sac is not likely homologous with that of

ornithothoracine birds because its osteological indicator

(furcular pneumatisation) is absent in phylogenetically

intermediate taxa, including other allosauroids (Chure and

Madsen 1996), basal birds (Chiappe et al. 1999; Zhou and

Zhang 2003; Mayr et al. 2007) and non-avian coelur-

osaurian theropods (Norell et al. 1997; Makovicky and

Currie 1998; Clark et al. 1999; Xu and Norell 2004).

Without evidence for a clavicular air sac homologous with

that of birds, we should not presume that basal birds and

non-avian ornithodirans possessed a functioning syrinx.

The lack of evidence of a syrinx in ornithodirans

outside Ornithothoraces will, no doubt, disappoint fans of

roaring movie dinosaurs. However, lack of ability to

vocalise does not necessarily mean that such animals were

silent altogether. Many extant reptiles communicate with

each other and with potential predators by non-vocal

acoustic means such as hissing, clapping jaws together,

grinding mandibles against upper jaws, rubbing scales

together, or use of environmental materials (e.g. splashing

against water) (Campbell and Evans 1972; Gans and

Maderson 1973; Garrick et al. 1978; Thorbjarnarson and

Hernandez 1993). Birds also use non-vocal acoustic means

of communication such as hissing, bill-clapping, stamping

and wing beating (Welty and Baptista 1988; Kear 2005;

Nelson 2005). Non-avian theropods with feathered wings

may have beaten their wings in acoustic displays as extant

P. Senter276


birds often do. Sauropod dinosaurs of the family

Diplodocidae, known from the Upper Jurassic of North

America and Africa (Upchurch et al. 2004), possessed

whiplike tail tips that could have produced loud, whiplike

cracking sounds for intraspecific communication or in

response to predators (Myhrvold and Currie 1997).

The morphology of the nasal passage in Lambeosaur-

inae, a Laurasian clade of Upper Cretaceous ornithischians

(Horner et al. 2004), suggests a role in sonic resonation

(Weishampel 1981). However, resonation need not be for

vocal sounds. Some extant snakes lack vocal cords but

possess resonating chambers that emphasise the low

frequencies of the hiss (Young 1991). The variety of visual

display structures in pterosaurs and dinosaurs (Chapman

et al. 1997; Molnar 2005; Unwin 2006) shows that visual

communication was important to these animals. They may

therefore have relied largely on visual means of

communication. Extant precedent for such reliance is

found among lizards, in which non-chemical communi-

cation is primarily visual (Pough et al. 1998), despite their

excellent hearing (Wever 1978).

Members of a few extant bird orders are known from

before the Cenozoic. Members of Anseriformes (water-

fowl) are known from the latest Cretaceous (Campanian-

Maastrichtian) of Asia, North America and Antarctica

(Hope 2002; Clarke et al. 2005). Several acoustic

behaviours are taxonomically widespread within Anser-

iformes and may be behavioural symplesiomorphies of the

group: near-constant contact calls of low amplitude among

groups, pairs or parents and offspring; a loud duet called a

triumph display by a pair after an agonistic encounter; a

special greeting call; a special post-copulatory call; a

special alarm call; calling during takeoff and throughout

flight; defensive hissing and among juveniles, special

distress calls, begging calls and calls expressing sleepiness

(Kear 2005). Vocal pitch usually differs between the sexes

and is higher in juveniles than adults (Kear 2005).

Members of Galliformes (game birds) are known from

the latest Cretaceous (Campanian-Maastrichtian) of North

America (Hope 2002). Several acoustic behaviours are

taxonomically widespread within Galliformes and may be

behavioural symplesiomorphies of the group: frequent

utterance of contact calls of low pitch and amplitude

among aggregations and pairs; a loud, far-carrying, often

multi-syllable advertisement call by the male that is often

answered by the female to form a vocally dimorphic duet

that may be answered by neighbouring males or pairs; a

special alarm call; and a loud, rapid, multi-syllable call

that differs from the usual alarm call, upon takeoff when

flushed (Jones et al. 1995; Madge and McGowan 2002).

Anseriformes and Galliformes together form the clade

Galloanserae, which is the sister clade to all other extant

birds except ratites and tinamous (van Tuinen et al. 2000).

The frequent occurrence in both Anseriformes and

Galliformes of duetting and near-constant, low-amplitude

contact calls suggests that they may be behavioural

symplesiomorphies for Galloanserae and therefore were

present in the Cretaceous.

Members of Gaviiformes (loons) are known from the

latest Cretaceous (Maastrichtian) of South America (Hope

2002). Loons emit trains of clucking sounds during flight

and a variety of calls in other situations (Oberholser 1974).

Far-reaching, drawn-out advertisement calls known as

wails or yodels are produced at dawn and dusk during the

breeding season (Oberholser 1974). In most loons takeoff

involves much noise because a loon has to run along the

water’s surface for a long distance to become airborne, and

landing may involve a powerful splash (Oberholser 1974).

Members of the extant family Phalacrocoracidae

(cormorants, order Pelecaniformes) are known from the

latest Cretaceous (Maastrichtian) of Asia and North

America (Hope 2002). Several acoustic characteristics and

behaviours found in cormorants are widespread in

Pelecaniformes and may be behavioural symplesiomor-

phies for the group. These include general silence away

from the nesting colony except for loud communal fishing

calls; high-pitched begging calls from chicks; sexual

dimorphism in voice; emission of hisses and special

disturbance calls during nest-usurpation attempts; copula-

tory vocalisations and the ability to recognise the voices of

offspring and neighbours (Nelson 2005). Other acoustic

characteristics that are typical of cormorants but not other

pelecaniformes include squeaky complaint calls from

chicks when disturbed; loss of the female voice after five

to six weeks; growling or loud barks by males in nest

defense; and a display by the male when advertising for a

female in which he throws his head back and makes

neighing or gargling sounds and follows this with ‘Goww,

gow, goww,’ if the female approaches (Nelson 2005).

Some fragmentary Upper Cretaceous (Maastrichtian)

bird specimens have been referred to Charadriiformes

(shorebirds) and Psittaciformes (parrots), but these

assignments are doubtful (Hope 2002). We therefore

cannot confidently infer that typical shorebird or parrot

calls were present before the Cenozoic.

Among extant birds, the vocabularies of basal groups –

ratites, tinamous, waterfowl, and galliforms – tend to be

differentiated at least into loud advertisement calls, soft

contact calls, special alarm calls, and (in Ratitae and

Anseriformes) the use of hissing as a threat (Jones et al.

1995; Davies 2002; Madge and McGowan 2002; Kear

2005). Such differentiation also occurs in more derived

groups (e.g. Nelson 2005) and therefore may be

symplesiomorphic for Neornithes, the clade that includes

all birds phylogenetically bracketed by the extant bird

orders. The earliest known neornithean birds are from the

Upper Cretaceous (Campanian) (Hope 2002), at which

time the differentiation was probably present.

Extant bird vocalisations vary in pitch according to body

size, with smaller birds emitting vocalisations of higher



frequency (Welty and Baptista 1988). Avian body size is

also correlated with the range of frequencies detectable by

the inner ear, with smaller birds capable of detecting higher

frequencies (Gleich et al. 2004). There is no reason to expect

that the same was not true of Mesozoic birds.

Whether or not Mesozoic birds sang is at least partly a

semantic issue. According to the technical definition, an

avian advertisement call is considered a ‘song’ if it is

acoustically complex, multi-syllabic, and exhibits shorter

pauses between notes than the pauses between groups of

notes (Welty and Baptista 1988). In practice, however,

avian advertisement vocalisations are called ‘songs’ if they

issue from the mouths of songbirds (Passeriformes), doves

(Columbiformes) or tinamous (Tinamiformes), whether or

not they are complex or multi-syllabic. This is probably

because the advertisement vocalisations of these taxa have a

quality that is musical to human ears. The less pleasant (to

humans) advertisement vocalisations of other bird taxa are

considered ‘calls’ rather than ‘songs,’ despite their similar

function and the fact that in some taxa (e.g. galliforms and

loons) they fit the technical definition of ‘song.’ In any case,

Mesozoic bird sounds probably lacked musical quality

because songbirds, doves and tinamous lack Mesozoic

records (Unwin 1993; Boles 1995), and musical vocalisa-

tions are not the norm in other birds.

Mammals and kin (Amniota: Synapsida)

The amniote clade Synapsida includes mammals (Mam-

malia) and their extinct relatives. Basal synapsids

(‘pelycosaurs’) lacked tympanic ears (Carroll 1986). The

bones that support the tympanum in mammals and connect

it with the stapes are homologous to the posterior bones of

the mandible and jaw joint in other synapsids (Allin 1986;

Luo and Crompton 1994). In the synapsids most closely

related to mammals these bones became smaller and less

solidly attached to the anterior mandible (Allin 1986;

Crompton and Hylander 1986). In basal mammals – and

possibly inHadrocodium, the genus most closely related to

mammals (Luo et al. 2001) – these bones detached from

the mandible and became incorporated into the middle ear

(Wang et al. 2001). This specialisation was present by the

Middle Jurassic at the latest (Kielan-Jaworowska et al.

2004), and by the Lower Jurassic if it was present in

Hadrocodium (Luo et al. 2001). It indicates definitive

evidence for tympanic hearing, hence the possibility of

acoustic communication, in the earliest mammals. The

earliest mammals and their predecessors were probably

nocturnal (Crompton et al. 1978), so their evolution of

airborne hearing may have been functionally related to

their occupation of a visually compromised niche.

The possibility of tympanic hearing in synapsids

intermediate between ‘pelycosaurs’ and mammals has

received attention. There are strong osteological indicators

that these animals lacked a tympanum posterior to the

quadrate such as diapsids possess (Luo and Crompton

1994). Some researchers have suggested that a mandibular

tympanum was present in derived Permian and Triassic

synapsids with a posterior mandibular cleft bordered by

bones homologous to those that contact the mammalian

tympanum (e.g. Allin 1986). However, three lines of

evidence support the absence of a tympanum outside a

derived synapsid clade that appeared in the Upper Triassic.

That clade, hereafter called the DS (derived synapsid) clade

for concision, includesmammals and their extinct outgroups

Morganucodontidae and Tritylodontidae (Figure 4). First,

the synapsid homologue of the cochlea retained its

plesiomorphic, globular shape in other synapsids (Allin

1986) but became elongated, indicating increased auditory

acuity, in the DS clade (Vater et al. 2004). Second,

osteological evidence suggests that the posterior mandibular

bones were muscle attachment sites in other synapsids but

not in the DS clade, and the attachment of muscles would

have impeded transmission of vibrations from a tympanum

(Kemp 2005). Third, the attachment of the posterior

mandibular bones was solid, impeding transmission of

vibrations from a tympanum, in other synapsids but was

loose, facilitating transmission of vibrations, in the DS clade

(Crompton and Hylander 1986).

The same three lines of evidence also suggest an

increase in auditory acuity at the base of the DS clade.

However, they do not demonstrate the presence of

tympana. New osteological evidence from a particularly

well-preserved skull of Chiniquodon, a non-mammalian

member of the DS clade, shows that the posterior

mandibular bones were acoustically isolated from the

anterior mandible and were free to vibrate as a unit about

their collective longitudinal axis in response to low-

frequency airborne sound (Kemp 2007). However, the

arrangement of the rest of the skull bones precludes the

presence of an air-filled tympanic cavity, without which a

tympanum is pointless (Kemp 2007). Basal members of

the DS clade could therefore hear airborne sounds but only

at low frequencies (Kemp 2007).

Extant mammals of all three clades – Monotremata

(egg-laying mammals: echidna and platypus), Metatheria

(marsupials) and Eutheria (placental mammals) – vocalise

using vocal cords in the larynx. Their common ancestor,

which appeared in the Middle Jurassic (Kielan-Jawor-

owska et al. 2004), therefore presumably also could

vocalise with laryngeal vocal cords. It is uncertain how

much, if any, further back in synapsid phylogeny vocal

cords were present. Venomous hindlimb spurs are

plesiomorphic for the clade that includes Mammalia and

its close outgroup Docodonta (Hurum et al. 2006), which

phylogenetically bracket Lower Jurassic taxa (Kielan-

Jaworowska et al. 2004). If proto-mammals employed

acoustic ‘honest warnings’ to predators, as do many

insects and amphibians (Masters 1979; Duellman and

Trueb 1994), vocal cords may have been present as far

P. Senter278


back as the common ancestor of Docodonta and

Mammalia in the Lower Jurassic.

In monotremes and the extinct basal mammalian clade

Multituberculata, the cochlea is more elongated than in

more basal synapsids, indicating that a wider range of

frequencies can be heard; even so, monotreme auditory

acuity is poor, with a peak at 5 kHz and low ability to hear

low-amplitude sounds (Vater et al. 2004). Therefore, in

Mesozoic mammals of this grade, any vocalisations used in

intraspecific communication likely exhibited low pitch.

In contrast, the cochleae of therian (marsupial and placental)

mammals are extremely elongated and coiled, allowing

hearing through wide frequency ranges even at low

amplitudes (Vater et al. 2004). The frequencies of peak

sensitivity for therian ears vary inversely according to body

size, with the largest therian ears sensitive to infrasound and

the smallest sensitive to ultrasound (Long 1994) (Figure 1).

Therefore, in Mesozoic therians, vocalisations used in

intraspecific communication likely were of highest pitch in

small species and of lower pitch in larger species.

The monotreme and marsupial vocal apparatus is poor,

due to fusion of the thyroid cartilage (a mammalian

apomorphy) of the larynx with the cricoid cartilage and the

possession of primitive laryngeal musculature (Negus 1949;

Kelemen 1963). Perhaps because of this, monotreme and

marsupial vocal sounds are generally simpler than those of

placental mammals, and their vocabularies are smaller.

Cooing, purring and snuffing sounds of unclear significance

are known in echidnas (Tachyglossidae) (Hutchins 2004).

Platypuses (Ornithorhynchus) growl when disturbed, and

the female emits pre-copulatory squeaks that are answered

by the male; juveniles make squeaking contact calls to each

other during play and are also known to hiss (Tembrock

1963; Griffiths 1978). Marsupial vocabularies often include

courtship vocalisations, aggressive vocalisations, and

hissing as a defensive sound, although in some taxa

defensive sounds are vocal (Nowak 2005). More extensive

vocabularies exist in the marsupial genus Macropus (true

kangaroos), but this is probably related to eusociality, a trait

characteristic of Macropus and uncharacteristic of marsu-

pials in general (Menkhorst and Knight 2004). It is therefore

doubtful that complex vocabularies existed among Meso-

zoic marsupials.

Stem-group marsupials are known from as early as the

Lower Cretaceous (Aptian-Albian) (Kielan-Jaworowska

et al. 2004), but no member of the marsupial crown group

is known from before the Cenozoic (Rougier et al. 1998).

None of the vocalisations characteristic of extant

marsupial families can therefore be inferred to have

existed before the Cenozoic. However, the fact that

vocabularies are differentiated into different vocalisations

for different situations in both platypuses and marsupials

suggests that such differentiation is an ancient trait. Vocal

differentiation may therefore have been present in the

common mammalian ancestor in the Middle Jurassic.

Also, the possibility of behavioural homology of defensive

hissing in marsupials and reptiles suggests that hissing was

a typical defensive behaviour through the synapsid

ancestry of mammals.

In placental mammals the thyroid cartilage has detached

from the cricoid cartilage (Figure 1) and the laryngeal

musculature is elaborated, so the eutherian larynx facilitates

more elaborate vocalisation than is possible in monotremes

and marsupials (Kelemen 1963). Perhaps because of this the

vocabularies of placental mammals tend to be larger than

those of monotremes and marsupials and can convey

information about a wider variety of situations and

emotional states (Estes 1991). The earliest known placental

mammals are from the Lower Cretaceous (Barremian)

(Ji et al. 2002), and complex vocabularies may have existed

among placentals that early.

One extant placental order, Soricomorpha (shrews,

tenrecs, hedgehogs and kin), is known from the Mesozoic

(Kielan-Jaworowska et al. 2004). Echolocation, clicking

sounds, defensive hissing and aggressive squeaking are

common and taxonomically widespread in extant sorico-

morphs (Nowak and Paradiso 1983). If these are ancestral

acoustic behaviours for Soricomorpha, they were present

before the Cenozoic. Soricomorphs are known from as

early as the Coniacian (Upper Cretaceous) of Asia and the

Campanian (Upper Cretaceous) of North America

(Kielan-Jaworowska et al. 2004).

Other extant placental orders are unknown before the

Cenozoic, but members of some extant placental supraor-

dinal taxa are present. Basal members of Archonta, which

includes the orders Dermoptera (colugos), Chiroptera (bats)

and Primates (primates), are known from the latest

Cretaceous (Maastrichtian) of India (Kielan-Jaworowska

et al. 2004). Basal members of the supraordinal taxon

Ungulatomorpha (hoofed mammals) are known from as

early as the Upper Cretaceous (Turonian) of Asia and the

latest Cretaceous (Campanian-Maastrichtian) of Europe and

South America (Kielan-Jaworowska et al. 2004). Sounds

made by extant archontans and ungulatomorphs are too

varied across taxa (Hill and Smith 1984; Estes 1991) to infer

ancestral acoustic behaviour for either group. Basal

members of Ferae, which includes the order Carnivora

and a few extinct orders, are known from the latest

Cretaceous (Campanian-Maastrichtian) of North America

(Kielan-Jaworowska et al. 2004). Sounds made by extant

carnivorans vary, but three types of sounds are common to

so many members of so many carnivoran families that they

may be plesiomorphic for Carnivora or perhaps even Ferae:

low-pitched growling to communicate threat, high-pitched

vocalisations in response to physical pain, and high-pitched

distress and contact calls from juveniles (Estes 1991).

Drumming with the hind feet on the substrate is a

common method to communicate alarm or the presence of

danger among mammals with hindlimbs that are specialised

for saltatory locomotion (hopping). This method has



appeared convergently in Macropodidae (kangaroos and

their saltatory relatives), Macroscelididae (elephant

shrews), Leporidae (rabbits), Dipodidae (jerboas) and

Dipodomys (kangaroo rats) (Nowak and Paradiso 1983;

Menkhorst and Knight 2004). It is probably no coincidence

that this form of communication is prevalent among

mammals of this morphotype and that in all cases it

transmits the same type of information. Theoretically, a

novel reflexive behaviour in response to a given stimulus

could most easily evolve by modification of a preexisting

reflexive behaviour involving the same set of muscles in

response to the same stimulus. An oscillatory hindlimb

motor reflex (drumming) in response to danger might

therefore most easily evolve inmammals that already have a

preexisting oscillatory hindlimb motor reflex (hopping) in

response to danger. Because of its prevalence among

saltatory mammals, it is possible that this method of

acoustic communication of alarm/danger was present in

Zalambdalestes, a saltatory placental mammal from the

Upper Cretaceous (Campanian) of Mongolia (Kielan-

Jaworowska 1978).


Rigorous analysis is needed to determine whether the

potential acoustic behavioural homologies proposed here

within Aves and Mammalia meet tests of homology. It

would also be informative to compare aspects of

vocalisation across anuran, avian and mammalian

phylogeny to determine whether or not it is possible to

infer ancestral characteristics of vocal sounds in each

group. It would also be informative to study inner ear

endocasts of more fossil archosaurian and synapsid taxa to

determine hearing ranges, as has been done for a few taxa

(Gleich et al. 2004; Vater et al. 2004). In addition, it would

be interesting to study sound-producing structures across

the phylogeny of ray-finned fishes to determine whether

homologies in acoustic anatomy can be assessed.

The big picture

The evidence and inferences presented above suggest that

the questions posed in this paper’s opening paragraph can

be answered. Triceratops and indeed even the earliest

dinosaurs heard crickets chirping in the evening.

The Mesozoic treetops did not resound with frogsong,

although Upper Jurassic and Cretaceous bodies of water

did. Cretaceous treetops were filled with the sounds of

honking, cackling and wailing birds in what must have

been an awful cacophony that would not become sweet

and musical until the advent of songbirds, doves and

tinamous in the Cenozoic. The immense corpses of

sauropods were surrounded with the buzzing of legions of

bottle flies, but not until the Upper Cretaceous.

In addition to such tidbits, a larger paleobioacoustical

scenario emerges from the pooled information presented

here (Figure 6). Incidental animal sounds were probably

present in the oceans by the beginning of the Paleozoic

Era, but those sounds were not heard (except perhaps by

cephalopods) until much later. The first terrestrial

arthropod communities arose in the Silurian Period, and

defensive stridulation in terrestrial arthropods may have

appeared soon thereafter. In the Silurian Period cartilagi-

nous and bony fishes appeared, and each independently

acquired the ability to hear low-frequency water-borne

sounds. Parallel evolution of defensive, aggressive and

courtship sounds is rampant among ray-finned fishes and

may have begun in the Silurian or Devonian. Malacos-

tracan crustaceans also appeared in the Devonian, and

several lineages evolved defensive stridulation in parallel,

possibly in response to predation by fishes with underwater

hearing. Bony fishes and early tetrapods of the Silurian and

Devonian Periods engaged in noisy air-breathing without

fear of being overheard by predators, because no

vertebrate had yet acquired tympanic ears.

Tetrapods exploded in diversity in the Carboniferous

Period. Amniotes appeared in the Pennsylvanian and

employeddefensivedisplays that incorporatedbody inflation

as a visual signal. The resulting hissing sound was first heard

by seymouriamorph predators in the Lower Permian and by

archosauriform predators in the Upper Permian. Arthropod

defensive stridulation was heard by diapsid predators for the

first time in the Upper Permian, although the mechanical

vibrations produced by stridulation may have deterred other

tetrapod predators as early as the Mississippian.

An explosion of terrestrial sound appeared in the

Triassic Period. Low-frequency twilight choruses may

already have existed among ray-finned fishes, but the

earliest terrestrial twilight choruses appeared in the Triassic

with the advent of crickets and their mesoedischiid and

titanopteran relatives. The drumming of stoneflies appeared

in theMiddle Triassic. The hemipteran taxon Prosorrhyncha

appeared in the Upper Triassic and radiated into several

lineages that evolved defensive and courtship stridulation in

parallel. Turtles first appeared in the Upper Triassic; their

courtship sounds may have appeared soon thereafter, or

those sounds may be evolutionary continuations of court-

ship sounds that were present in parareptiles from perhaps as

early as the Permian.

Water boatmen joined the twilight chorus in the Lower

Jurassic, and anurans joined it in the Upper Jurassic.

Venomous mammals began making defensive vocalisa-

tions in the Lower Jurassic. Tympanic ears appeared in

mammals by the Middle Jurassic and may have been used

to locate (chorusing?) insect prey. The tapping of booklice,

the buzzing of aculeate wasps, and tail-cracking sounds by

diplodocid sauropods appeared in the Upper Jurassic.

In the Lower Cretaceous, geckoes and birds joined the

twilight chorus. The tapping of death-watch beetles and

P. Senter280


termite soldiers, and the buzzing of horseflies, bottle flies

and mosquitoes appeared. Mammalian vocalisations

increased in pitch as therians gained the ability to hear

high-frequency sounds. In the Upper Cretaceous, cicadas

and head-slapping crocodilians joined the twilight chorus,

along with birds from a few extant orders. The buzzing of

bottle flies and the echolocating chirps of soricomorph

mammals also appeared, possibly along with the growling

of angry basal members of Ferae. High-frequency fish

sounds appeared with the advent of hearing-specialist

fishes.

This scenario is unlikely to be the last word on

Paleozoic andMesozoic animal sounds. Future discoveries

will augment, hone and perhaps even falsify hypotheses

put forth here. It is my hope that this synthesis will

stimulate more research on the voices of the past.

Acknowledgements

Of those who provided help with this project, M. Holmandeserves a particularly huge amount of thanks. She was in chargeof inter-library loan at Lamar State College-Orange in Orange,Texas while I worked there on the first phase of this project, andshe was run ragged during the massive literature search requiredfor this study. B. Karpinecz helped with the typing of thebibliography. Several ichthyologists provided help with findingreferences on acoustic behaviour in fishes: A. Popper,R. Rountree, C. Johnston, A. Bass, K. Huebert and J. McManus.R. Fortey and P. Selden helped me track down references onstridulatory structures in Paleozoic arthropods. Conversationswith R. Senter and M. McClure sparked useful ideas. Of thespecimens in Figure 1, M. McClure of Lamar State College-Orange provided access to the crab, toad and pig; L. Wilmore ofLamar State College-Orange provided access to the snake skull;and T. Rowe and C. Jass of the Texas Memorial Museumprovided access to the turtle skull. M. Laurin provided usefulinput that improved this paper.

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