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Autotomy

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Not to be confused with Autonomy.
A white-headed dwarf gecko with tail lost due to autotomy.

Autotomy (from the Greek auto = "self-" and tomy = "severing") or self amputation is the behaviour whereby an animal sheds or discards one or more of its own appendages,[1] usually as a self-defense mechanism to elude a predator's grasp or to distract the predator and thereby allow escape. The lost body part may be regenerated later.

Vertebrates

Reptiles and amphibians

Lizard tail autotomy
Discarded salamander tails exhibiting continued movement

Some geckos,[2][3] skinks,[4][5][6] lizards[7][8][9] and salamanders[10][11][12] that are captured by the tail will shed part of the tail structure and thus be able to flee. The detached tail will continue to wriggle, creating a deceptive sense of continued struggle and distracting the predator's attention from the fleeing prey animal. The animal can partially regenerate its tail, typically over a period of weeks. The new section will contain cartilage rather than regenerating vertebrae of bone, and the skin of the regenerated organ generally differs distinctly in colour and texture from its original appearance. The technical term for this ability to drop the tail is caudal autotomy. In most lizards that sacrifice the tail in this manner, breakage occurs only when the tail is grasped with sufficient force, but some animals, such as some species of geckos, can perform true autotomy, throwing off the tail when sufficiently stressed, such as when attacked by ants.[13] Some such lizards, in which the tail is a major storage organ for accumulating reserves, will return to a dropped tail after the threat has passed, and will eat it to recover part of the sacrificed supplies.[14] Conversely, some species have been observed to attack rivals and grab their tails, which they ate as their opponents fled.[15]

Caudal autotomy in lizards takes two forms. In the first form, called intervertebral autotomy, the tail breaks between the vertebrae. The second form of caudal autotomy is intravertebral autotomy, in which there are zones of weakness, fracture planes across each vertebra in the mid-part of the tail. In this second second type of autotomy the lizard contracts a muscle to fracture a vertebra, rather than break the tail between two vertebrae.[16] Sphincter muscles in the tail then contract around the caudal artery to minimize bleeding.

Mammals

At least two species of African Spiny mice, Acomys kempi and Acomys percivali, are capable of autotomic release of skin, e.g. upon being captured by a predator. They are the first mammals known to do so. [17] They can completely regenerate the autotomically released or otherwise damaged skin tissue - regrowing hair follicles, skin, sweat glands, fur and cartilage with little or no scarring. It is believed that the corresponding regeneration genes could also function in humans.[18]

Invertebrates

Over 200 species of invertebrates are capable of using autotomy as an avoidance or protective behaviour[19][20] including -

These animals can voluntarily shed appendages when necessary for survival. Autotomy can occur in response to chemical, thermal and electrical stimulation, but is perhaps most frequently a response to mechanical stimulation during capture by a predator. Autotomy serves either to improve the chances of escape or to reduce further damage occurring to the remainder of the animal such as the spread of a chemical toxin after being stung.

Molluscs

Autotomy occurs in some species of octopus for survival and for reproduction: the specialized reproductive arm (the hectocotylus) detaches from the male during mating and remains within the female's mantle cavity.

Species of (land) slugs in the genus Prophysaon can self-amputate a portion of their tail.[26] There is known autotomy of the tail of sea snail Oxynoe panamensis under persistent mechanical irritation.[27]

Evisceration, the ejection of the internal organs of sea cucumbers when stressed, is also a form of autotomy, and they regenerate the organ(s) lost.[28]

Some sea slugs exhibit autotomy. Both Discodoris lilacina and Berthella martensi will often drop their entire mantle skirt when handled, leading to Discodoris lilacina also being called Discodoris fragilis. The members of Phyllodesmium will drop a large number of their cerata each, on the tip having a large sticky gland that secretes a sticky substance.[29]

Crustaceans

Autotomic stone crabs are used as a self-replenishing source of food by humans, particularly in Florida. Harvesting is accomplished by removing one or both claws from the live animal and returning it to the ocean where it can regrow the lost limb(s).[30] However, under experimental conditions, but using commercially accepted techniques, 47% of stone crabs that had both claws removed died after declawing, and 28% of single claw amputees died; 76% of the casualties died within 24 hours of declawing.[31] The occurrence of regenerated claws in the fishery harvest is low; one study indicates less than 10%,[31] and a more recent study indicates only 13% have regenerated claws.[32] (See Declawing of crabs)

Post-harvest leg autotomy can be problematic in some crab and lobster fisheries, and often occurs if these crustaceans are exposed to freshwater or hypersaline water in the form of dried salt on sorting trays.[33] The autotomy reflex in crustaceans has been proposed as an example of natural behaviour that raises questions concerning assertions on whether crustaceans can "feel pain", which may be based on definitions of "pain" that are flawed for lack of any falsifiable test, either to establish or deny the meaningfulness of the concept in this context.[34]

Spiders

A fishing spider with two limbs missing

Under natural conditions, orb-weaving spiders (Argiope spp.) undergo autotomy if they are stung in a leg by wasps or bees. Under experimental conditions, when spiders are injected in the leg with bee or wasp venom, they shed this appendage. But, if they are injected with only saline, they rarely autotomize the leg, indicating it is not the physical injection or the ingress of fluid per se that causes autotomy. In addition, spiders injected with venom components which cause injected humans to report pain (serotonin, histamine, phospholipase A2 and melittin) autotomize the leg, but if the injections contain venom components which do not cause pain to humans, autotomy does not occur.[35]

Bees

Sometimes when honey bees (genus Apis) sting a victim, the barbed stinger remains embedded. As the bee tears itself loose, the stinger takes with it the entire distal segment of the bee's abdomen, along with a nerve ganglion, various muscles, a venom sac, and the end of the bees digestive tract, i.e. autotomy.[36][37] This massive abdominal rupture kills the bee.[38] Although it is widely believed that a worker honey bee can sting only once, this is a partial misconception: although the stinger is barbed so that it lodges in the victim's skin, tearing loose from the bee's abdomen and leading to its death, this only happens if the skin of the victim is sufficiently thick, such as a mammal's.[39] The sting of a queen honey bee has no barbs, however, and does not autotomize.[40] All species of true honey bees have this form of stinger autotomy. No other stinging insect, including the yellowjacket wasp and the Mexican honey wasp, have the sting apparatus modified this way, though they may have barbed stings.

The endophallus and cornua portions of the male genitalia of male honey bees (drones) also autotomize during copulation, and form a mating plug, which must be removed by the genitalia of subsequent drones if they are also to mate with the same queen.[41] The drones die within minutes of mating.

See also

References

  1. ^ (2000). The American Heritage Dictionary of the English Language: Fourth Edition.
  2. ^ Congdon, J.D., Vitt, L.J. and King. W.W., (1974). Geckos: adaptive significance and energetics of tail autotomy. Science, 184: 1379–1380
  3. ^ Kelehear, C. and Webb. J.K., (2006). Effects of tail autotomy on anti-predator behavior and locomotor performance in a nocturnal gecko. Copeia, 2006: 803–809
  4. ^ Wilson, R.S., and Booth. D.Y., (1998). Effect of tail loss on reproductive output and its ecological significance in the skink Eulamprus quoyii. Journal of Herpetology 32: 128–131
  5. ^ Chapple, D.G., McCoull, C.J. and Swain, R., (2002). Changes in reproductive investment following caudal autotomy in viviparous skinks (Niveoscincus metallicus): lipid depletion or energetic diversion? Journal of Herpetology, 36: 480–486
  6. ^ Lin, Z., Qu, Y. and Ji, X., (2006). Energetic and locomotor costs of tail loss in the Chinese Skink, Eumeces chinensis. Comparative Biochemistry and Physiology, 143A: 508–513
  7. ^ Bellairs, A.D., and Bryant, S.V., (1985). Autotomy and regeneration in reptiles. In: Biology of the Reptilia. Vol. 15. C. Gans and F. Billet (eds.). John Wiley and Sons, New York. pp. 301–410
  8. ^ Cooper, W.E., (2003). Shifted balance of risk and cost after autotomy affects use of cover, escape, activity, and foraging in the Keeled Earless Lizard (Holbrookia propinqua). Behavioral Ecology and Sociobiology, 54: 179–187
  9. ^ Dial, B.E. and Fitzpatrick, L.C., (1981). The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae). Oecologia, 51: 310–317
  10. ^ Maiorana, V.C. (1977). Tail autotomy, functional conflicts and their resolution by a salamander. Nature, 265: 533–535
  11. ^ Ducey, P.K., Brodie, E.D. and Baness, E.A., (1993). Salamander tail autotomy and snake predation: role of antipredator behavior and toxicity for three neotropical Bolitoglossa (Caudata: Plethodontidae). Biotropica, 25: 344–349.
  12. ^ Marvin, A.G., (2010). Effect of caudal autotomy on aquatic and terrestrial locomotor performance in two Desmognathine salamander species. Copeia, 3: 468–474 [1]
  13. ^ Rose, Walter; The Reptiles and Amphibians of Southern Africa; Pub: Maskew Miller, 1950
  14. ^ Clark DR (1971) Strategy of Tail-Autotomy in Ground Skink, Lygosoma laterale. Journal of Experimental Zoology 176: 295–&
  15. ^ Durrell, Gerald. My Family and Other Animals. Penguin Books 1987. ISBN 978-0140103113
  16. ^ Bateman, P.W. and Fleming P.A., (2009). To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years. Journal of Zoology, 277: 1-14. doi:10.1111/j.1469-7998.2008.00484.x [2]
  17. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi:10.1038/nature11499, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi=10.1038/nature11499 instead.
  18. ^ Cormier, Zoe (2012-09-26). "African spiny mice can regrow lost skin". Nature. Retrieved 2012-09-27.
  19. ^ Bely, A.E. and Nyberg, K.G., (2009). Evolution of animal regeneration: re-emergence of a field. Trends in Ecology & Evolution, 25: 161-170
  20. ^ a b c Fleming, P.A., Muller, D. and Bateman, P.W., (2007). Leave it all behind: a taxonomic perspective of autotomy in invertebrates. Biological Reviews, 82: 481-510 doi:10.1111/j.1469-185X.2007.00020.x
  21. ^ McDonnel, R.J., Paine, T.D. and Gormally, M.J., (2009). Slugs: A Guide to the Invasive and Native Fauna of California. 21 pp., ISBN 978-1-60107-564-2, page 9.
  22. ^ Lewin R.A., (1970). Toxin secretion and tail autotomy by irritated Oxynoe panamensis (Opisthobranchiata: Sacoglossa). Pacific Science, 24: 356-358
  23. ^ Wilson, A.D.M., Whattam, E.M., Bennett, R., et al., (2010). Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European housecricket, Acheta domesticus. Behavioural Ecology and Sociobiology, 64: 703–715 DOI 10.1007/s00265-009-0888-1
  24. ^ Stankowich, T., (2009). When predators become prey: flight decisions in jumping spiders. Behavioural Ecology, 20: 318-327
  25. ^ Booksmythe, I., Milner, R.N.C., Jennions, M.D., et al., (2010). How do weaponless male fiddler crabs avoid aggression? Behavioural Ecology and Sociobiology, 64: 485-491
  26. ^ Mc Donnel R. J., Paine T. D. & Gormally M. J. (2009). Slugs: A Guide to the Invasive and Native Fauna of California. 21 pp., ISBN 978-1-60107-564-2, page 9.
  27. ^ Lewin R. A. (1970). "Toxin secretion and tail autotomy by irritated Oxynoe panamensis (Opisthobranchiata: Sacoglossa)". Pacific Science 24: 356-358. PDF
  28. ^ Patrick Flammang, Jerome Ribesse, Michel Jangoux (2002-12-01). "Biomechanics of adhesion in sea cucumber cuvierian tubules (echinodermata, holothuroidea)". Integrative and Comparative Biology. Archived from the original on 26 December 2008. Retrieved 2008-12-22.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  29. ^ Rudman, W.B. (October 14, 1998). "Autotomy". The Sea Slug Forum.
  30. ^ Gulf and Florida Stone Crabs
  31. ^ a b Gary E. Davis, Douglas S. Baughman, James D. Chapman, Donald MacArthur & Alan C. Pierce (1978). Mortality associated with declawing stone crabs, Menippe mercenaria (PDF). US National Park Service. Report T-522.{{cite book}}: CS1 maint: multiple names: authors list (link)
  32. ^ "The 2006 Stock Assessment Update for the Stone Crab, Menippe spp., Fishery in Florida". Florida Fish and Wildlife Conservation Commission. Retrieved 23 September 2012.
  33. ^ Davidson, G.W. and Hosking, W.W. (2004)Development of a Method for Alleviating Leg Loss During Post-harvest Handling of Rock Lobsters. 104 pp.
  34. ^ Rose JD, Arlinghaus R, Cooke SJ, Diggles BK, Sawynok W, Stevens ED, Wynne CDL (2012). Can fish really feel pain? Fish and Fisheries DOI: 10.1111/faf.12010
  35. ^ Eisner, T. and Camazine, S., (1983). Spider leg autotomy induced by prey venom injection: an adaptive response to 'pain'? Proceedings of the National Academy of Sciences, USA, 80:3382-3385
  36. ^ Snodgrass, R.E. (1956). The Anatomy Of The Honey Bee. Ithaca, New York: Cornell University Press.
  37. ^ Visscher, P.K. Vetter, R.S. and Camazine, S. "Removing bee stings". Retrieved April 23, 2013.{{cite web}}: CS1 maint: multiple names: authors list (link)
  38. ^ "Why do honeybees die after they sting you?". Retrieved April 23, 2013.
  39. ^ How Bees Work – howstuffworks.com. Retrieved 23 April 2013.
  40. ^ Steinau, R. (2011). "Bee stings". Retrieved April 23, 2013.
  41. ^ Collins, A.M., Caperna, T.J., Williams, V., Garrett, W.M. and Evans, J.D., (2006). Proteomic analyses of male contributions to honey bee sperm storage and mating. Insect Molecular Biology 15(5): 541–549

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