Ormia ochracea

Last updated

Ormia ochracea
Ormia ochracea (gravid female).jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Diptera
Family: Tachinidae
Subfamily: Tachininae
Tribe: Ormiini
Genus: Ormia
Species:
O. ochracea
Binomial name
Ormia ochracea
(Bigot, 1889) [1]
Synonyms

Ormia ochracea is a small yellow nocturnal fly in the family Tachinidae. [2] 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. [3]

Contents

Ormia ochracea is a model organism in sound localization experiments because of its unique "ears", which are complex structures inside the fly's prothorax near the bases of its front legs. The fly is too small for the time difference of sound arriving at the two ears to be calculated in the usual way, yet it can determine the direction of sound sources with exquisite precision. The tympanic membranes of opposite ears are directly connected mechanically, allowing resolution of nanosecond time differences [4] [5] and requiring a new neural coding strategy. Various research groups have designed low-noise differential microphones inspired by O. ochracea’s directionally sensitive hearing system.

Distribution

Ormia ochracea is native to the southeastern United States, including states such as Texas and Florida. [6] O. ochracea is also found throughout North America, South America, and the Caribbean, [7] though its exact range is not known.

Life history

Ormia ochracea has the full life cycle of egg, larvae, pupa, and adult. Once a female fly finds a suitable host, she deposits planidia (first instar larvae) which then quickly burrow into the host. [8] The planidia develop within the body of the field cricket host, embedding initially in muscle before migrating into the abdomen. [9] The larvae molt within the host's abdomen and feed primarily on the host's muscle and fat. O. ochracea larvae typically complete development and emerge after about 7 days, which subsequently kills the host. The larvae pupate and emerge as adult flies approximately 2 weeks after emerging from the host. [8]

field cricket is the common host for O. ochracea Fall Field Cricket (Gryllus pennsylvanicus) - Kitchener, Ontario 2018-06-28.jpg
field cricket is the common host for O. ochracea

Food resources

O. ochracea is a parasitoid known to prey on several species of Gryllus field crickets including Gryllus integer, Gryllus rubens, Gryllus texensis, and Gryllus firmus. [7] Flies have been observed responding to various cricket songs, but seem to be limited to the family Gryllidae. The natural host of the fly may vary by location. Larvae of O. ochracea exhibit highest survival in its natural host and limited survival in other potential host species. [10]

Host-finding

In 1975, William H. Cade experimentally demonstrated that Ormia ochracea uses the mating call of the field cricket as a means to locate its host. Cade placed dead crickets on top of speakers playing cricket songs and various control sounds and recorded the amount of time the fly spent on either the control or test speaker. He found that flies spent more time on the speakers playing cricket songs and observed that the flies would always deposit larvae on and around the speaker which was playing cricket songs. [3]

Learning

O. ochracea have been shown to adjust their preference for host songs after exposure to different songs in the laboratory. In a 2011 study, flies that were previously exposed to the G. lineaticeps song chose the G. lineaticeps song over the G. integer song, and vice versa. [11] This preference was very short term. O. ochracea's flexible learning capabilities may have been critical in expanding its host and geographical range.

Effects of infestation on host behavior

O. ochracea infestation has been shown to affect the behavior and reproduction of host field crickets. [9] [12] Early in the infestation period, non-reproductive behavior is largely unimpaired because the parasitic larvae do not consume the digestive system or central nervous system of the host. [9] After the larvae migrate to the host's abdomen, the host's mating, egg-laying, and fighting ability decline, most likely due to tissue damage caused by the larvae. [9] Additionally, infestation of female crickets alters their mating preferences. Gryllus lineaticeps females normally prefer to respond to male songs with intermediate chirp rates over those with slow chirp rates, but females parasitized by O. ochracea show no preference between chirp rates. [12] Reduced selectivity in infested female G. lineaticeps may be adaptive, as a female may be more likely to reproduce before being killed by the parasitoids if they are less selective.

Host defenses

Some species of cricket which are parasitzed by O. ochracea have evolved methods to avoid infestation. For example, some members of the prey cricket Teleogryllus oceanicus have a mutation called flat wing, in which the sound-producing structures of the male forewings are erased. [13] The flat wing was first observed in 2003 on the Hawaiian island of Kauai, and was also found on neighbouring Oahu two years later. Genetic studies of crickets from each island show that the mutations arose from different genomic variations.

Enemies

Because field crickets commonly sing at night, O. ochracea are susceptible to predation by bats. Studies have shown that O. ochracea has evolved an acoustic startle response to bat-like ultrasound, a response very similar to that of female crickets. [14] O. ochracea has also been shown to demonstrate a sharp response boundary between the frequencies of cricket song and bat ultrasound. [14]

Physiology

Directional hearing

In order for an animal to localize sound, it must be able to detect minute differences in intensity and time between the arrival of the sound to the ear closer to the source and the ear further from the source. O. ochracea displays a remarkable ability to localize sound despite the incredibly small distance (450-520μm) between its acoustic sensory organs. [15] Its sound localization ability is facilitated by a cuticular structure which joins its ears, mechanically coupling their motion and magnifying interaural differences by a factor of about 20. [15] Prior to O. ochracea no similar mechanism of auditory localization had been described.

Scientific significance

Several researchers have reported the construction of microphones inspired by the hearing system of O. ochracea. In 2009, R.N. Miles et al. designed and created a low-noise differential microphone inspired by the unique hearing system of O. ochracea, for use in hearing aids. The design of their microphone diaphragm, which measures 1 x 2 mm2, is based on the mechanically coupled ears of O. ochracea. Their microphone was found to have lower noise than commercially available hearing aid microphones while minimizing distance between sensors. [16] In April 2015, a group from the University of Strathclyde and the MRC/CSO Institute for Hearing Research (IHR) announced that it had created a microphone based on O. ochracea's hearing system, and had been awarded a £430,000 grant by the U.K. Engineering and Physical Sciences Research Council to build and test the hearing aid for three years. [17]

Related Research Articles

<span class="mw-page-title-main">Tachinidae</span> Family of insects

The Tachinidae are a large and variable family of true flies within the insect order Diptera, with more than 8,200 known species and many more to be discovered. Over 1,300 species have been described in North America alone. Insects in this family commonly are called tachinid flies or simply tachinids. As far as is known, they all are protelean parasitoids, or occasionally parasites, of arthropods, usually other insects. The family is known from many habitats in all zoogeographical regions and is especially diverse in South America.

<span class="mw-page-title-main">Mole cricket</span> Members of the insect family Gryllotalpidae

Mole crickets are members of the insect family Gryllotalpidae, in the order Orthoptera. Mole crickets are cylindrical-bodied, fossorial insects about 3–5 cm (1.2–2.0 in) long as adults, with small eyes and shovel-like fore limbs highly developed for burrowing. They are present in many parts of the world and where they have arrived in new regions, may become agricultural pests.

Sound localization is a listener's ability to identify the location or origin of a detected sound in direction and distance.

Dr. William H. "Bill" Cade is a biologist and a former president of the University of Lethbridge. He researches the role of acoustic signals in field cricket mating behaviour.

<i>Ormia</i> Genus of flies

Ormia is a small genus of nocturnal flies in the family Tachinidae, that are parasitoids of crickets.

<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

<i>Gryllus veletis</i> Species of cricket

Gryllus veletis, commonly known as the spring field cricket, is abundant throughout eastern North America. G. veletis is a solitary, aggressive, omnivorous, burrow-inhabiting species of cricket. This species is commonly confused with Gryllus pennsylvanicus, as they inhabit the same geographical area. However, the two species are easily distinguished through examination of life history, ovipositor and behavioural differences. Predators of G. veletis include American toads, wild turkeys, red-tailed hawks, wolf spiders and red-backed salamanders.

<span class="mw-page-title-main">Cricket (insect)</span> Small insects of the family Gryllidae

Crickets are orthopteran insects which are related to bush crickets, and, more distantly, to grasshoppers. In older literature, such as Imms, "crickets" were placed at the family level, but contemporary authorities including Otte now place them in the superfamily Grylloidea. The word has been used in combination to describe more distantly related taxa in the suborder Ensifera, such as king crickets and mole crickets.

<i>Senostoma</i> Genus of flies

Senostoma is a genus of parasitoid tachinid flies in the family Tachinidae. Endemic to Australasia, the flies are medium-sized, bristly, and long-legged.

Ultrasound avoidance is an escape or avoidance reflex displayed by certain animal species that are preyed upon by echolocating predators. 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.

<i>Gryllus rubens</i> Species of cricket

Gryllus rubens, commonly known as the southeastern field cricket, is one of many cricket species known as a field cricket. It occurs throughout most of the Southeastern United States. Its northern range spans from southern Delaware to the extreme southeastern corner of Kansas, with a southern range stretching from Florida to eastern Texas.

<span class="mw-page-title-main">Marlene Zuk</span> American evolutionary biologist

Marlene Zuk is an American evolutionary biologist and behavioral ecologist. She worked as professor of biology at the University of California, Riverside (UCR) until she transferred to the University of Minnesota in 2012. Her studies involve sexual selection and parasites.

Stimulus filtering occurs when an animal's nervous system fails to respond to stimuli that would otherwise cause a reaction to occur. The nervous system has developed the capability to perceive and distinguish between minute differences in stimuli, which allows the animal to only react to significant impetus. This enables the animal to conserve energy as it is not responding to unimportant signals.

<i>Anastrepha suspensa</i> Species of fly

Anastrepha suspensa, known as the Caribbean fruit fly, the Greater Antillean fruit fly, guava fruit fly, or the Caribfly, is a species of tephritid fruit fly. As the names suggest, these flies feed on and develop in a variety of fruits, primarily in the Caribbean. They mainly infest mature to overripe fruits. While thought to have originated in Cuba, the Caribbean fruit fly can now also be found in Florida, Hispaniola, and Puerto Rico.

An illegitimate receiver is an organism that intercepts another organism's signal, despite not being the signaler's intended target. In animal communication, a signal is any transfer of information from one organism to another, including visual, olfactory, and auditory signals. If the illegitimate receiver's interception of the signal is a means of finding prey, the interception is typically a fitness detriment to either the signaler or the organism meant to legitimately receive the signal, but it is a fitness advantage to the illegitimate receiver because it provides energy in the form of food. Illegitimate receivers can have important effects on the evolution of communication behaviors.

Gryllus integer, commonly known as the western trilling cricket, is one of many species of field cricket in the genus Gryllus. It is called the "triller" field cricket because its song is nearly continuous rather than broken into discrete chirps. G. integer can be found in parts of the Western United States, having been recorded from Oregon, California, Arizona and New Mexico.

Ormia depleta, sometimes called the Brazilian red-eyed fly, is a species of fly in the family Tachinidae. It is a parasitoid of mole crickets in the genus Scapteriscus. It is native to South America but has been imported into the United States and elsewhere as a biological pest control agent.

Sturmiopsis inferens is a species of fly in the family Tachinidae. It is native to Asia and is a parasitoid of various moth species whose larvae feed inside the stems of sugarcane, rice and other large grasses, including the Gurdaspur borer and the sugarcane shoot borer.

Liriomyza trifolii, known generally as the American serpentine leafminer or celery leafminer, is a species of leaf miner fly in the family Agromyzidae.

Exorista mella is a tachinid fly of the genus Ezorista within the family Tachinidae of the order Diptera. They are typically found in the United States and Canada. Within the U.S in the state of Arizona they have been found in both mountainous and agricultural regions. E. mella is a parasitoid fly, a polyphagous generalist which parasitizes a variety of hosts.

References

  1. 1 2 Bigot, J. M. F. (1889). "Dipteres nouveaux ou peu connus. 34e partie, XLII: Diagnoses de nouvelles especes". Annales de la Société Entomologique de France. 8 (6): 253–270.
  2. O’Hara, James E.; Shannon, J. Henderson; D. Monty, Wood (5 March 2020). "World Checklist of the Tachinidae" (PDF). Tachinidae Resources. Retrieved 28 February 2022.
  3. 1 2 Cade, W. (1975-12-26). "Acoustically Orienting Parasitoids: Fly Phonotaxis to Cricket Song". Science. American Association for the Advancement of Science (AAAS). 190 (4221): 1312–1313. doi:10.1126/science.190.4221.1312. ISSN   0036-8075. S2CID   85233362.
  4. Miles, R. N.; Robert, D.; Hoy, R. R. (1995). "Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea". The Journal of the Acoustical Society of America. Acoustical Society of America (ASA). 98 (6): 3059–3070. doi:10.1121/1.413830. ISSN   0001-4966. PMID   8550933.
  5. Robert, D.; Miles, R.N.; Hoy, R.R. (1996). "Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea". Journal of Comparative Physiology A. Springer Science and Business Media LLC. 179 (1): 29–44. doi:10.1007/bf00193432. ISSN   0340-7594. PMID   8965258. S2CID   21452506.
  6. Sabrosky, C.W. (1953). "Taxonomy and host relations of the tribe Ormiini in the Western Hemisphere (Diptera, Larvaevoridae)". Proceedings of the Entomological Society of Washington. 55: 167–183.
  7. 1 2 Lehmann, Gerlind U.C. (January 2003). "Review of Biogeography, Host Range and Evolution of Acoustic Hunting in Ormiini (Insecta, Diptera, Tachinidae), Parasitoids of Night-calling Bushcrickets and Crickets (Insecta, Orthoptera, Ensifera)". Zoologischer Anzeiger - A Journal of Comparative Zoology. 242 (2): 107–120. doi:10.1078/0044-5231-00091. ISSN   0044-5231. S2CID   85839051.
  8. 1 2 Wineriter, S. A.; Walker, T. J. (December 1990). "Rearing phonotactic parasitoid flies [Diptera: Tachinidae, ormiini, ormia spp.]". Entomophaga. 35 (4): 621–632. doi:10.1007/bf02375096. ISSN   0013-8959. S2CID   27347119.
  9. 1 2 3 4 Adamo, S.A.; Robert, D.; Hoy, R.R. (March 1995). "Effects of a tachinid parasitoid, Ormia ochracea, on the behaviour and reproduction of its male and female field cricket hosts (Gryllus spp)". Journal of Insect Physiology. 41 (3): 269–277. doi: 10.1016/0022-1910(94)00095-x . ISSN   0022-1910.
  10. Thomson, Ian R.; Vincent, Crystal M.; Bertram, Susan M. (March 2012). "Success of the Parasitoid FlyOrmia ochracea(Diptera: Tachinidae) on Natural and Unnatural Cricket Hosts". Florida Entomologist. 95 (1): 43–48. doi: 10.1653/024.095.0108 . ISSN   0015-4040.
  11. Paur, Jennifer; Gray, David A. (October 2011). "Individual consistency, learning and memory in a parasitoid fly, Ormia ochracea". Animal Behaviour. 82 (4): 825–830. doi:10.1016/j.anbehav.2011.07.017. ISSN   0003-3472. S2CID   18427803.
  12. 1 2 Beckers, Oliver M.; Wagner, William E. (April 2013). "Parasitoid infestation changes female mating preferences". Animal Behaviour. 85 (4): 791–796. doi:10.1016/j.anbehav.2013.01.025. ISSN   0003-3472. PMC   3857093 . PMID   24347669.
  13. Pascoal, Sonia; Cezard, Timothee; Eik-Nes, Aasta; Gharbi, Karim; Majewska, Jagoda; et al. (2014). "Rapid Convergent Evolution in Wild Crickets". Current Biology. Elsevier BV. 24 (12): 1369–1374. doi: 10.1016/j.cub.2014.04.053 . ISSN   0960-9822. PMID   24881880.
  14. 1 2 Rosen, M. J.; Levin, E. C.; Hoy, R. R. (2009-11-27). "The cost of assuming the life history of a host: acoustic startle in the parasitoid fly Ormia ochracea". Journal of Experimental Biology. 212 (24): 4056–4064. doi:10.1242/jeb.033183. ISSN   0022-0949. PMC   2784737 . PMID   19946084.
  15. 1 2 Miles, R. N.; Robert, D.; Hoy, R. R. (December 1995). "Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea". The Journal of the Acoustical Society of America. 98 (6): 3059–3070. doi:10.1121/1.413830. ISSN   0001-4966. PMID   8550933.
  16. Miles, R.N. Su, Q. Cui, W. Shetye, M. Degertekin, F.L. Bicen, B. Garcia, C. Jones, S. Hall, N. (April 2009). A low-noise differential microphone inspired by the ears of the parasitoid fly Ormia ochracea. Acoustical Society of America. OCLC   678236270.{{cite book}}: CS1 maint: multiple names: authors list (link)
  17. Clark, Liat (2015-04-21). "Parasitic flies inspire potential revolution in hearing aids". WIRED UK. Retrieved 2021-11-11.