SOUNDS surround us. In fact, humans drown in sounds so much that total deafness in another hundred years is fairly certain. The information sounds convey are an important component for the survival of all animals, including humans. How humans produce sounds and hear them are common knowledge, but such mechanisms in invertebrates, particularly insects, are not so well known.
Many different members of the invertebrate world produce sounds of sorts, but the ability to hear sound exists only among members of Phylum Arthropoda. That insects make sounds is well known. But how do they hear them? Most insects create or pick up only substrate vibrations. The ability to hear airborne sounds, as in humans, is present only among certain groups of insects and crabs. Like vertebrates, insects too have ears to hear. Interestingly, within this small (considering the numbers of insects, it will not be wrong to say minuscule) group of insects, there exists a great variety of ears. Evolution results in diversity, but the forms and functions seen in the ears of insects are testimony to the incredible diversity the evolutionary processes are capable of achieving.
Insects arrived around 480 million years ago in aquatic environments. Around 400 million years ago some of them migrated to land. These were stone deaf. No evidence is available so far to show that insects which arrived on land could hear. Why then did they develop the ability to hear? The answer is both simple and complex. Simple: It is needed for survival in the broadest sense. Faraway sounds can be detected to establish territory, find resources, escape predators; for courtship and reproduction; social communication; protecting the young; and, in some cases, location of hosts for parasitism. Complex because evolutionary history informs us that ears in insects appeared, disappeared and reappeared 20 times over in several avatars for reasons yet to be fully comprehended. Among butterflies and moths alone it has appeared six times. Professor David Yager of the University of Maryland, College Park, United States, who researches the auditory system of insects, is of the opinion that these numbers will grow as more evidence is unearthed.
Form and Function
There are 30 orders of insects known at present. Of these, insects belonging to nine orders possess the ability to hear as per currently available research. Even among them, not all species of a given order have ears and, even if they have, not all can hear. Ear and hearing in insects are like reading fairy tales that boggle the imagination. Ears in humans are two structures sticking out of the sides of the head. Not so for insects, which may have it in any other part of their body, including their mouth. This broad diversity is related to the range of functions they perform. Ears are seen in moths, grasshoppers, tettigonids (katydids and crickets), preying mantids, lacewings, mosquitoes, midges, honeybees, some bugs, beetles, cockroaches and a few species of flies, but they are placed differently in different insects (Figure 1).
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The secret to the diversity of ears lies very much in the same concept that has contributed to the successful diversity of insects. One part many uses, that is, modification of an existing part to serve a new purpose. Ears in insects (with the exception of certain specialised hairs) are modifications of the chordotonal organs (specialised sensory cells that are arranged serially throughout the insect body). Scientifically speaking, these are proprioceptors that help insects in locomotion. (Proprioceptors in organisms, including humans, help to make sense of their position vis-a-vis the space around them. Remember, human ears perform the twin functions of hearing and maintaining balance.) If ears are modifications of a part present all over an insect’s body, it is but natural that insects can have ears in any part of their body.
As insects evolved, they converted the chordotonal organs from a segment of their choice into ears. That is why even within a given group of insects, ears are located at different places. In some cases, it was simpler. The ears were merely a bunch of sensory cells. Among moths, we find a diversity of locations. Hawk moths have ears in their mouth parts, owlet and tiger moths have them at the junction of thorax and abdomen, and the geometer moths have them on either side of the first abdominal segment. What factor caused the choice of location is still under investigation.
Two types of ears are seen among insects, antennal and tympanal ears. Both respond to airborne sounds but in different ways. In order to hear, mechanical vibrations induced by sound are converted into electrical signals for the brain to decipher so that “hearing” can happen. This “conversion” is the function of the ear. Sound has various components. Of these, the antennal ears respond to the particle velocity component of sound, whereas tympanal ears (like in humans) respond to the pressure component.
The antennal ear
The antennal ears are receptors (sensory cells) that detect ‘near-field’ sounds. They are not modifications of chordotonal cells. They are light-weight structures located on the antenna. Being light, they are easily displaced by movement of molecules in air when the antennae vibrate. Antennal ears thus respond to the air-particle movements caused by sounds, a phenomenon that is described as particle velocity component of sound. Although new evidence seems to indicate that antennal ears may hear high frequency sounds that are far away, research shows that antennal ears are generally efficient in hearing low frequency sounds coming from sources closer to the ears. So, which insects have them?
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The human irritant, mosquitoes. The buzzing of mosquitoes is not for human ears but for their kith and kin. Their antennae are feathery; described as plumose, the receptors are located in their plumes. Another common insect that sports ears in its antenna is the fast-declining honeybee. Conventional textbooks will record bees as deaf insects since humans are only now beginning to understand the diversity of ears in the animal world. For social insects such as bees, communication is important for survival. Until recently, bee-dance movements were thought to be the signal for communication. Scientists now know that the sound caused by the wingbeats of honeybees can be ‘heard’ by other bees.
In the 1960s, two researchers discovered that dancing bees emitted low frequency sounds, but their announcements fell on ‘deaf’ ears. Experiments conducted by Towne and Kirchner (1989) clearly demonstrated the bee’s ability to hear and respond to low intensity stimuli of 265-350 Hz. We now know that they have ears. Called Johnston’s organ, it is a collection of sensory cells, located in the second segment of the antenna. Skilled beekeepers can distinguish the sounds produced by bees, which vary with circumstances, colonies and subspecies; they recognise sounds made by bees to indicate hunger, agitation, calm and anger. The sounds they produce can range from 190 Hz to 250 Hz, which is well within the hearing range of its antennal ears. Other examples of insects with antennal ears include some of the smallest of insects, namely midges and fruit flies.
The Tympanal ear
Tympanal ears, by contrast, are much more than a group of receptors. Like human ears they have a sound-receiving eardrum—the tympanum—that vibrates in response to the pressure component of sound. Eardrums in insects are believed to have come about through a stepwise thinning of the cuticle. They are backed by air sacs. Because the eardrums are backed by air sacs, impedance-matching middle-ear structures, seen in humans are not required, allowing the auditory organ to pick up the vibrations directly from the eardrum. While this is the basic principle of tympanal ears, there are structural differences seen among insects that have these ears
Mantids are the cheetahs of the insect world. Their forelegs are for no saintly prayers when they hold them together in front of their body; with the liberal scattering of spines on them, these folded forelegs are a hunting posture, ready for attack, to capture the prey and rip it apart for a juicy meal. But this predator king of the insect world has its own nemesis, the bat. Scientists believe that the ear in mantids developed to escape from bats. Did it?
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The tympanal ears of mantids are unique. There is only one ear and so described as auditory cyclops, or cyclopean ear. It is located on the ventral side of the insect’s thorax. More precisely, in the centre of the metathoracic or the third thoracic segment close to the first abdominal segment. The ear is made of two tear-drop shaped tympanum enclosing a groove. The complexities of the ear are beyond the scope of this article. Mantids are the only known terrestrial animal with a single ear. In a few species, a second single ear may be seen on the mesothoracic, or the second thoracic segment, similar in structure to the metathoracic ear. Whereas the metathoracic ear is capable of hearing in ultrasound frequencies, the mesothoracic ear cannot hear high frequency sounds.
The females do not possess ears, and if present, they have reduced hearing power or cannot hear at all. Similarly, ears in males of several mantid species have either disappeared or become non-functional. The loss of hearing is associated with flight. Female mantids rarely fly. Several mantid species cannot fly or have lost their ability for flight. Their escape routes are different. Naturally, all this queerness sparked the curiosity of mantid-mad researchers. What they found was fascinating.
Through studies of well-preserved fossils, they found that mantids that evolved 140 million years ago were at first earless forms. The theory that ears in mantids developed to escape bats went flying out of the window when it was found that mantids were sporting their cyclopean ears long before bats evolved on earth. Bats evolved only 64 million years ago, but a combination of studies using data from anatomical, neurophysiological and behavioural databases confirm that the cyclopean ear evolved in mantids 120 million years ago. Why did they evolve?
Scientists believe that in the beginning the ears evolved for intraspecific communication, that is, to ‘chat’ with one another and for prey detection, in other words to find food. A fine picture they create in the mind, praying mantises chatting about food. Escape from predators was also on the cards but to a lesser extent. In those early years, frogs and birds were the predators to escape from. Birds were already present during the cretaceous period when mantids evolved. As time passed (time in evolutionary scale), the auditory systems were fine-tuned when bats entered the picture, and as more years passed by, the original functions of communication and prey location took a back seat. Studies have revealed that hearing mantids escape capture by flying bats in 76 per cent of attacks, whereas a deafened mantid’s escape rate is only 34 per cent.
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At present, there are at least five types of auditory systems associated with the metathoracic ear. Yager and his team record that three of these systems can be identified by external anatomy and can be used by taxonomists for identifying mantid genera. Add to this the mesothoracic ear and mantid species have a choice of six auditory systems for adaptation and survival. But the puzzles surrounding ears in mantids are far from over. Extensive studies have provided data on metathoracic ears. But the question of mesothoracic ear remains an enigma. What purpose does this ear, which is sensitive only to low frequency sounds, serve? There are several hypotheses, but the last word is yet to be heard.
Insect musicians: katydids, crickets
Tropical forests buzz with sounds and are a haven for acoustic ecologists. Dominating the scenario are songs of insects such as katydids and crickets. Research by evolutionary scientists has shown that musical notes for communication by katydids was well established during the Jurassic period1 (when dinosaurs roamed the earth) when there were plenty of insect-eating mammals, reptiles and amphibians around. By extension, it proves that ears evolved not for evading bats but as a means of communication.
Globally, around 7,500 species of katydids have been named. As they are not studied much in India, we have no idea of the actual number of species of katydids or crickets to be found here. But for those taxonomists who study them, their call is a defining feature to identify a new species. Katydids and crickets have ears in the tibia of their first pair of legs. Their ears are simple and bear similarities with the human ear. They are also the most studied among insect ears. The ears perform a wide variety of functions. They can hear the ultrasound of bats, know when a mate or a competitor is nearby, and the predaceous ones can also recognise when a meal is available for the taking. When the spotted predatory katydid, Chlorobalius leucoviridis, hears the male cicada, it imitates the mating call of the female cicada. The male responds only to end up as a juicy meal for the katydid.
But crickets and katydids themselves are at risk when they call. The female will choose the male that calls the loudest. When the males call, not only the females but predators too can hear. For the field cricket (Gryllus), there is another insect predator deadlier than the bat, the tachinid fly (Ormia ochraceae). This fly looks mostly like a housefly but for the colours that are light yellow. Ormia’s ears are found in the prothorax, close to where the first pair of legs arise. The female fly on hearing the cricket’s call locates it and deposits the first instar larva, which quickly burrow into its body. The larvae complete their development inside the cricket’s body, killing it as they emerge out to pupate and develop into adults. Some tachinid flies parasitise other cricket species too. Flies from only two families, namely, Tachninidae and Sarcophagidae, have ears.
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An exception to the normal tympanal ears of katydids is the ear in Copiphora gorgonen. Unlike other katydids with tympanal ears, this one possesses endolymph similar to that found in the mammalian ear.1 Research has shown that as in mantids, ears in katydids evolved around 250 million years ago. They evolved for intraspecific communication and functioned under a much lower hearing range; modern day katydid ears, though, are evolved to detect the ultrasonic calls of the bat, too. But if you thought that bats alone have mastered the high-pitched ultrasonic sound, then be prepared for a surprise.
Three species of katydids from Colombia and Eucador hold the record for producing the loudest ultrasonic sound among insects. Aptly called Supersonus aequoreus,2 this katydid calls at a 148 kHz.
Ears in moths and butterflies
Bats are major predators of nocturnal insects, both flying and non-flying ones. They hunt insects even without echolocation, a feature one rarely hears about. Bats can at times glean a stationary insect on vegetation and, fluttering above it, pick it up for their meal, all without echolocation. But it is not just bats that insects have to worry about. There are other vertebrate predators such as reptiles, birds, mammals and amphibians that seek out insects for food. Most of the moths that visit my moth screen at my home fall prey to lizards. At Kalakad Mundanturai Tiger Reserve, a cuckoo came to feed on moths at midnight. Insects such as praying mantids and assassin bugs love to gorge on moths.
Whether day flying or night flying, lepidoptera are a meal for several animals. One of their multipronged strategies to escape predation is the use of their ears. Approximately 55 per cent of lepidopterans have tympanal ears, paired ears that are sensitive to ultrasound.
The location of ears in moths is diverse. The simplest of ears are seen in moths belonging to the Superfamily Noctuoideae. In tiger moths, prominent moths, noctuids and others, the ears are located one on each side, laterally, at the junction of the metathorax and abdomen. A tympanum with associated structures forms the ear.
A number of moths belonging to the Crambidae, Geometridae and Uraniidae families communicate through ultrasound clicks to find mates, but keep their sounds low to avoid eavesdropping by predators, competitors or parasites. Several of them have evolved a new strategy. They communicate via hyper-frequency ultrasonic signal which their predators do not detect since they do not use those frequencies.
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Among the geometer moths, the ears are present on the ventral surface of the first abdominal segment. While all geometer moths have ears, they are reduced or lost in flightless females. Uraniid moths, closely related to the geometer, also have ears in their abdomen at the junction of second and third abdominal segments.
In the pyrlaids grass moths and snout moths, among others, the ears are located in the abdomen. They exist in two forms, which is a predominant feature for classifying these moths into the Family Crambidae or Pyralidae. Some of the moths of these families have entered into an evolutionary competition with their arch enemies, bats. Since these moths can hear bats’ calls, bats evolved to call at a higher pitch that the moths cannot hear. Not to be outdone and become a tasty meal for them, the moths evolved ears that could hear these higher pitches. The greater wax moth, Galleria mellonella, which gorges on bees, was found to hear at sounds up to 300 kHz. Some moths belonging to Family Thyrididae have ears at the base of the forewing near the subcostal vein, whereas those belonging to Drepanidae have a unique structure located in the abdomen
Butterflies, too, have ears. Their predators are many, ranging from reptiles, birds to mammals. Their ears, referred to as alars, are adapted to hear a wide variety of sounds, such as the rustling of a leaf, the wingbeat of a bird and movements of animals among plants. Butterflies belonging to Papilionidae (swallow tails) and Nymphalidae (brush-footed) have these structures at the base of their hindwings.
Non-tympanic ear among hawk moths
Probably the weirdest form of ears one can imagine is ears on the tongue. Two groups of hawk moths (distantly related) have ears on their labial palps or the proboscis, whose primary function is to sip nectar from flowers. It is a complex arrangement that is beyond the scope of this story. Suffice it to say that even within the two groups that sport the ears in their tongue there are differences in structures.
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The elephant hawk moth, Deilephila elpenor, as well as moths belonging to the genus Hippotion belong to the tribe Choerocampini in which the ears are located on each side of the proboscis. Around 150 species of moths from this tribe are auditory species. Two parts the labral pilfer and the labial palp together help in hearing. A somewhat different structure is seen among moths of the tribe Acherontini (13-14 auditory species). The death’s head hawk moth has a tuft of scales in its proboscis that vibrates in response to sound and helps in hearing. Despite the structural differences, both groups of moths can hear only ultrasound in the range of 20 kHz or sometimes 50 kHz to 70 kHz. Despite the ears on the proboscis, the structural differences led scientists to believe that these ears must have evolved independently.
There are several more insect species that have ears. The green lacewing has ears on the radial vein of its forewing. Among the beetles, only the scarabs of a few families and the tiger beetle have ears. Among tiger beetles, only those belonging to the genus Cicindela have ears located in the upper side of the first abdominal segment. The scarabs have their ears in their neck membrane, present on either side dorsally. Grasshoppers have them in their abdominal segments, and the aquatic bug, commonly called water boatman, has ears in the mesothorax, just above the second pair of legs.
No story on ears would be complete without mentioning the South African grasshopper, Bullacris membracioides.3 Its acoustic communication is quite unique. They are multi-eared. There are serially arranged, six homologous pairs of auditory organs in their abdomen. The males call so loudly that the females can hear them from a distance of two kilometres and start an acoustic duet with the male. According to Yager, the female’s hearing is considered to be the most sensitive among all insects.
Nádatmatam Jagat says the Vishnu Puranam, meaning the universe, is the embodiment of sound. Our ears can hear only a small part of the sounds of Nature. But a select group of insects learned long ago the significance of sound energy for survival and found ways to take advantage of it. Bioacoustics is increasingly being accepted as a reliable tool for studying, understanding and monitoring the health of ecosystems such as forests and oceans. Whereas due to inefficient ears, humans had to wait for technology to provide the hearing tools, for insects it was a matter of fine-tuning a part of their body organ to hear.
Geetha Iyer is the author of the book The Weavers: The Curious World of Insects. An education consultant, she has edited and written textbooks for middle and high school students.