Ultrasound avoidance

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Ultrasound avoidance is an escape or avoidance reflex displayed by certain animal species that are preyed upon by echolocating predators. [1] Ultrasound avoidance is known for several groups of insects that have independently evolved mechanisms for ultrasonic hearing. Insects have evolved a variety of ultrasound-sensitive ears based upon a vibrating tympanic membrane tuned to sense the bat's echolocating calls. The ultrasonic hearing is coupled to a motor response that causes evasion of the bat during flight.

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Although ultrasonic signals are used for echolocation by toothed whales, no known examples of ultrasonic avoidance in their prey have been found to date. [2]

Ultrasonic hearing has evolved multiple times in insects: a total of 19 times. Bats appeared in the Eocene era, (about 50 million years ago); antibat tactics should have evolved then. [3] Antibat tactics are known in four orders of Insecta: moths (Lepidoptera), crickets (Orthoptera), mantises (Dictyoptera), and green lacewings (Neuroptera). There are hypotheses of ultrasound avoidance being present in Diptera (flies) and Coleoptera (beetles). [3]

Ultrasound avoidance in moths

The idea that moths were able to hear the cries of echolocating bats dates back to the late 19th century. F. Buchanan White, in an 1877 letter to Nature [4] made the association between the moth's high-pitched sounds and the high-pitched bat calls and wondered whether the moths would be able to hear it. However, it was not until the early 1960s that Kenneth Roeder et al. made the first electrophysiological recordings of a noctuid moth's auditory nerve and were able to confirm this suspicion. [5]

Later research showed that moths responded to ultrasound with evasive movements. [6] Moths, as do crickets and most insects that display bat avoidance behaviors, have tympanic organs that display phonotactic and directional hearing; they fly away from the source of the sound and will only have the diving behavior considered above when the sound is too loud—or when, in a natural setting, the bat would be presumably too close to simply fly away. [7]

It was found that the moths' responses vary according to ultrasound intensity, diving towards the ground if the pulse was of a high amplitude, or flying directly away from the sound source if the sound amplitude was low (if the sound was softer). Acoustic sensory receptors in noctuid moths are mechanoreceptors located in a chamber formed by the wall of the abdomen and the tympanic membrane, are most sensitive to lower frequencies of ultrasound (between 20 and 30 kHz. [3] ).

The moth's body axis allows it to be more sensitive to sounds coming from particular directions. Their ears, on either side of the metathorax, have two sensory cells within the membranes. Though the tuning curves of these cells are identical, the sensitivity thresholds differ, allowing for sound localization and a wider range of sensitivity to sound. [3] The movement of the wings during flight also plays a role, since sound thresholds change with wing position. The neural mechanisms for triggering the acoustic startle response are partially understood. However, there is little known about the motor control of flight that ultrasound initiates. [7]

Further research has shown that many species of moths are sensitive to ultrasound. Sensitivities for ultrasound change according to the environment the moth thrives in, and the moth can even change its own sensitivity if it is preyed upon by bats with different echolocating calls. Such is the case of the Australian noctuid moth, Speiredonia spectans , which adapts its acoustic sensitivity according to the characteristics of the call of the bat inside the cave with them. [8]

Ultrasound avoidance in crickets

An adult male and a juvenile male of the species Gryllus bimaculatus Hoy crickets.JPG
An adult male and a juvenile male of the species Gryllus bimaculatus

Crickets are preyed on by bats during the night while they fly from one place to another. Avoidance behaviors by crickets were first reported in 1977 by A. V. Popov and V. F. Shuvalov. [9] [10] They also demonstrated that crickets, like moths, fly away from bats once they've heard their echolocating calls, an example of negative phonotaxis. The cricket will steer itself away from the source of the sound within a very short time frame (40–80 ms). The response is evoked by brief ultrasonic pulses in the 20 to 100 kHz range, pulses which fall within the range of bat ultrasonic echolocating calls (20–100 kHz).

As opposed to moths, the cricket ear, located in the foreleg, is complex - having 70 receptors that are arranged in a tonotopic fashion. This is understandable since crickets don't only need to listen to bats, but also to each other. [7] Crickets have broad frequency sensitivity to different types of echolocating calls. One specific auditory interneuron, the AN2 interneuron, exhibits remarkably rapid responses to echolocating call stimuli. [11]

All these receptors synapse on a far lower number of interneurons that relay the receptors' information to the cricket's central nervous system. In the Teleogryllus cricket, two ascending interneurons carry information to the brain - one carries information about cricket song (around 5 kHz) while the other gets excited at ultrasound and other high frequencies (15–100 kHz). [7] The ultrasound-sensitive interneuron - labeled INT-1 - has been demonstrated as both necessary and sufficient for negative phonotaxis by Nolen and Hoy in 1984: [12]

Stimulating int-1 by current injection is sufficient to initiate negative phonotaxis, while hyperpolarizing int-1 effectively cancels the turning response to ultrasound. Due to this, int-1 has been proposed to be a command neuron of sorts; in the cricket, int-1 is a bat detector when the cricket is in flight and the interneuron's activity reaches a specific threshold. If these conditions are met, the magnitude of the sound is linearly proportional to the magnitude of the avoidance response. [12] This research also demonstrated that the brain is necessary for the response, since decapitated crickets will fly, but show no avoidance response behaviors.

Bats may have found ways to get around this system. In the Teleogryllus oceanicus cricket, its broad sensitivity can be circumvented by the use of frequency-mismatched calls[ citation needed ] by part of bats like the gleaning bat, Nyctophilus geoffroyi . [11] Furthermore, it has been found that the ultrasound avoidance response is restricted to when the crickets are in flight: that is, the response is extinguished when the crickets are on the ground. [13]

It has also been shown that short-winged crickets are less sensitive to ultrasound, but not to low frequencies, than their long-winged counterparts in a wing-dimorphic cricket, Grillus texensis. [14] A hormone, named juvenile hormone (JH), is believed to play a role in whether the individual develops shorter or longer wings: if the individual has a higher level of JH, its wings will be shorter.

Ultrasound avoidance in other insects

In praying mantises, ultrasound avoidance behaviors are non-directional turns or power dives that are very effective in preventing capture by bats. [15] [16] The mantis ear, located in the midline between the metathoracic (third) legs, comprises two tympana within an auditory chamber that enhances sensitivity. [17] A bilaterally symmetrical pair of auditory interneurons, 501-T3, accurately track the ultrasonic calls during the early stages of a bat attack. Because 501-T3 stops firing just before the evasive response starts, it may be involved in triggering the behavior. [18] [19] The praying mantis ear first appeared c. 120 million years ago, predating the appearance of echolocating bats by c. 50 million years, so its original function must be different from its current one. [20]

Arctiid moths use a very different, but highly effective defense against bats. [21] They produce loud ultrasonic clicks in response to ultrasound. Depending on the species of moth and its ecology, the clicks may work by startling the bat, by jamming its echolocation system, or by warning of distastefulness (aposematism).

Green lacewings (Chrysopidae) have sensitive ears on their wings. Ultrasound causes flying lacewings to fold their wings and drop, an effective maneuver for evading capture by bats. [22] Some tettigoniids use a similar strategy, [23] although other species respond much like crickets. [24]

Several other insects have sensitive ultrasonic hearing that probably is used in bat evasion, but direct evidence is not yet available. These include scarab beetles, [25] tiger beetles [26] and a parasitoid fly ( Ormia sp.) [27]

Related Research Articles

<span class="mw-page-title-main">Ultrasound</span> Sound waves with frequencies above the human hearing range

Ultrasound is sound with frequencies greater than 20 kilohertz. This frequency is the approximate upper audible limit of human hearing in healthy young adults. The physical principles of acoustic waves apply to any frequency range, including ultrasound. Ultrasonic devices operate with frequencies from 20 kHz up to several gigahertz.

<span class="mw-page-title-main">Animal echolocation</span> Method used by several animal species to determine location using sound

Echolocation, also called bio sonar, is a biological active sonar used by several animal groups, both in the air and underwater. Echolocating animals emit calls and listen to the echoes of those calls that return from various objects near them. They use these echoes to locate and identify the objects. Echolocation is used for navigation, foraging, and hunting prey.

<span class="mw-page-title-main">Microbat</span> Suborder of mammals

Microbats constitute the suborder Microchiroptera within the order Chiroptera (bats). Bats have long been differentiated into Megachiroptera (megabats) and Microchiroptera, based on their size, the use of echolocation by the Microchiroptera and other features; molecular evidence suggests a somewhat different subdivision, as the microbats have been shown to be a paraphyletic group.

<span class="mw-page-title-main">Arctiinae</span> Subfamily of moths

The Arctiinae are a large and diverse subfamily of moths with around 11,000 species found all over the world, including 6,000 neotropical species. This subfamily includes the groups commonly known as tiger moths, which usually have bright colours, footmen, which are usually much drabber, lichen moths, and wasp moths. Many species have "hairy" caterpillars that are popularly known as woolly bears or woolly worms. The scientific name Arctiinae refers to this hairiness. Some species within the Arctiinae have the word "tussock"' in their common names because they have been misidentified as members of the Lymantriinae subfamily based on the characteristics of the larvae.

<span class="mw-page-title-main">Range fractionation</span>

Range fractionation is a term used in biology to describe the way by which a group of sensory neurons are able to encode varying magnitudes of a stimulus. Sense organs are usually composed of many sensory receptors measuring the same property. These sensory receptors show a limited degree of precision due to an upper limit in firing rate. If the receptors are endowed with distinct transfer functions in such a way that the points of highest sensitivity are scattered along the axis of the quality being measured, the precision of the sense organ as a whole can be increased.

<span class="mw-page-title-main">Anti-predator adaptation</span> Defensive feature of prey for selective advantage

Anti-predator adaptations are mechanisms developed through evolution that assist prey organisms in their constant struggle against predators. Throughout the animal kingdom, adaptations have evolved for every stage of this struggle, namely by avoiding detection, warding off attack, fighting back, or escaping when caught.

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<i>Ormia ochracea</i> Species of fly

Ormia ochracea is a small yellow nocturnal fly in the family Tachinidae. It is notable for its parasitism of crickets and its exceptionally acute directional hearing. The female is attracted to the song of the male cricket and deposits larvae on or around him, as was discovered in 1975 by the zoologist William H. Cade.

<span class="mw-page-title-main">Crypsis</span> Aspect of animal behaviour and morphology

In ecology, crypsis is the ability of an animal or a plant to avoid observation or detection by other animals. It may be a predation strategy or an antipredator adaptation. Methods include camouflage, nocturnality, subterranean lifestyle and mimicry. Crypsis can involve visual, olfactory or auditory concealment. When it is visual, the term cryptic coloration, effectively a synonym for animal camouflage, is sometimes used, but many different methods of camouflage are employed by animals or plants.

<span class="mw-page-title-main">Campaniform sensilla</span> Class of mechanoreceptors found in insects

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<span class="mw-page-title-main">Motion camouflage</span> Camouflage by choosing path to avoid seeming to move against background

Motion camouflage is camouflage which provides a degree of concealment for a moving object, given that motion makes objects easy to detect however well their coloration matches their background or breaks up their outlines.

<span class="mw-page-title-main">Tympanal organ</span> Hearing organ in insects

A tympanal organ is a hearing organ in insects, consisting of a membrane (tympanum) stretched across a frame backed by an air sac and associated sensory neurons. Sounds vibrate the membrane, and the vibrations are sensed by a chordotonal organ. Hymenoptera do not have a tympanal organ, but they do have a Johnston's organ.

<i>Cycnia tenera</i> Species of moth

Cycnia tenera, the dogbane tiger moth or delicate cycnia, is a moth in the family Erebidae. It occurs throughout North America, from southern British Columbia to Nova Scotia southwards to Arizona and Florida. The species is distasteful and there is evidence that it emits aposematic ultrasound signals; these may also jam bat echolocation, as the functions are not mutually exclusive.

<i>Teleogryllus oceanicus</i> Species of cricket

Teleogryllus oceanicus, commonly known as the Australian, Pacific or oceanic field cricket, is a cricket found across Oceania and in coastal Australia from Carnarvon in Western Australia and Rockhampton in north-east Queensland

James A. Simmons is a pioneer in the field of biosonar. His research includes behavioral and neurophysiological studies of sound processing in the echolocating bat. From the time he began graduate research in the late 1960s to the present, he has been in the forefront of bat echolocation research. Simmons was honored as a fellow of the Acoustical Society of America (ASA) in 1996 and of the American Association for the Advancement of Science in 2000. He was awarded the ASA's second Silver Medal in Animal Bioacoustics in 2005. His current position is Professor in the Department of Neuroscience, Brown University.

<span class="mw-page-title-main">Bat</span> Order of flying mammals

Bats are flying mammals of the order Chiroptera. With their forelimbs adapted as wings, they are the only mammals capable of true and sustained flight. Bats are more agile in flight than most birds, flying with their very long spread-out digits covered with a thin membrane or patagium. The smallest bat, and arguably the smallest extant mammal, is Kitti's hog-nosed bat, which is 29–34 millimetres in length, 150 mm (6 in) across the wings and 2–2.6 g in mass. The largest bats are the flying foxes, with the giant golden-crowned flying fox reaching a weight of 1.6 kg and having a wingspan of 1.7 m.

<span class="mw-page-title-main">Mantis</span> Order of insects

Mantises are an order (Mantodea) of insects that contains over 2,400 species in about 460 genera in 33 families. The largest family is the Mantidae ("mantids"). Mantises are distributed worldwide in temperate and tropical habitats. They have triangular heads with bulging eyes supported on flexible necks. Their elongated bodies may or may not have wings, but all Mantodea have forelegs that are greatly enlarged and adapted for catching and gripping prey; their upright posture, while remaining stationary with forearms folded, has led to the common name praying mantis.

<span class="mw-page-title-main">Deimatic behaviour</span> Bluffing display of an animal used to startle or scare a predator

Deimatic behaviour or startle display means any pattern of bluffing behaviour in an animal that lacks strong defences, such as suddenly displaying conspicuous eyespots, to scare off or momentarily distract a predator, thus giving the prey animal an opportunity to escape. The term deimatic or dymantic originates from the Greek δειματόω (deimatóo), meaning "to frighten".

Echolocation systems of animals, like human radar systems, are susceptible to interference known as echolocation jamming or sonar jamming. Jamming occurs when non-target sounds interfere with target echoes. Jamming can be purposeful or inadvertent, and can be caused by the echolocation system itself, other echolocating animals, prey, or humans. Echolocating animals have evolved to minimize jamming, however; echolocation avoidance behaviors are not always successful.

Rohini Balakrishnan is an Indian bioacoustics expert. She is a senior Professor and Chair of the Centre for Ecological Sciences at the Indian Institute of Science (IISc), Bengaluru. Her research focuses on animal behavior through the lens of animal communication and bioacoustics.

References

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  2. ↑ Wilson, M.; Hanlon, R. T.; Tyack, P. L. & Madsen, P. T. (2007). "Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii". Biology Letters. 3 (3): 225–227. doi:10.1098/rsbl.2007.0005. PMC   2464686 . PMID   17412672.
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  4. ↑ White's reference can be found in the following link: . His question is close to the ending of the letter.
  5. ↑ Payne, R. S.; Roeder, K. D. & Wallman, J. (1966). "Directional Sensitivity of the Ears of Noctuid Moths". The Journal of Experimental Biology. 44 (1): 17–31. doi:10.1242/jeb.44.1.17. PMID   5922736.
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  17. ↑ Yager, D. D. & Hoy, R. R. (1987). "The midline metathoracic ear of the praying mantis, Mantis religiosa". Cell and Tissue Research. 250 (3): 531–541. doi:10.1007/bf00218944. PMID   3690633. S2CID   37360392.
  18. ↑ Triblehorn, J. D. & Yager, D. D. (2002). "Implanted electrode recordings from a praying mantis auditory interneuron during flying bat attacks". The Journal of Experimental Biology. 205 (Pt 3): 307–320. doi:10.1242/jeb.205.3.307. PMID   11854368.
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  23. ↑ Libersat, F. & Hoy, R. R. (1991). "Ultrasonic startle behavior in bushcrickets Orthoptera; Tettigoniidae". Journal of Comparative Physiology A. 169: 507-514.
  24. ↑ Schulze, W. & Schul, J. (2001). "Ultrasound avoidance behavior in the bush cricket Tettigonia viridissima". The Journal of Experimental Biology. 204: 733–740. doi:10.1242/jeb.204.4.733. PMID   11171355.
  25. ↑ Forrest, T. G.; Farris, H. E. & Hoy, R. R. (1995). "Ultrasound acoustic startle responses in scarab beetles". The Journal of Experimental Biology. 198 (Pt 12): 2593–2598. doi: 10.1242/jeb.198.12.2593 . PMID   8576685.
  26. ↑ Yager, D. D. & Spangler, H. G. (1997). "Behavioral response to ultrasound in the tiger beetle, Cicindela marutha Dow combines aerodynamic changes and sound production". The Journal of Experimental Biology. 200 (Pt 3): 649–659. doi: 10.1242/jeb.200.3.649 . PMID   9057313.
  27. ↑ Robert, D. & Hoy, R. R. (1998). "The evolutionary innovation of tympanal hearing in Diptera". In: Hoy, R. R.; Popper, A. N. & Fay, R. R., editors. Comparative Hearing: Insects. Heidelberg and New York: Springer-Verlag. p 197-227
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