Autotomy – the Self Sacrifice Defence

The ability to cast off a particular section of their anatomy, in order to facilitate escape from a predator, is possessed by a wide range of animals. Although the phenomenon, even in the Mollusca, had been recognized previously the term wasn’t coined until 1883 by Leon Fredericq as “autotomie”. Well known examples include the tail of some lizards, the legs or claws of crabs and the arms of sea stars. This is now referred to as autotomy and the term is generally applied to those instances where the animal deliberately self-severs a non-vital/dispensable extremity, that has been directly aggravated, along predetermined fracture lines (not necessarily visible), assisted by anatomical structures and cellular chemistry to both sever and then seal off the resulting wound. Most usually, there exists the ability to regenerate the lost structure. Understand though that the mere regeneration of sections of an animal directly damaged by trauma however is different to the act of deliberately shedding a portion and then being able to regenerate it. Autotomy does not include the loss of body parts for other reasons such as reproductive methods or development progression. Autotomy could be crudely described as self amputation – a sacrifice made specifically for survival. The predator is distracted or confused or feeds on the sacrificial portion and the intended prey makes its escape. Autotomy however is not an effective response against all predators.

There are a number of sea slugs, across the various orders, that possess the ability to autotomize particular body parts, either as a reaction to a direct assault or from continuous irritation. Certain sea slugs are able to cast off sections of their mantle along specific fracture lines for the purpose and include some members of the Discodorididae family of nudibranchs and the Pleurobranchidae side-gilled slugs.

An entire specimen of Berthella martensi. Note the obvious mantle fracture lines, two longitudinal lateral and one transverse posterior, that delineate the three mantle segments that can be sacrificed. The central mantle portion is never autotomized.

A Berthella martensi specimen that has autotomized all three of its mantle segments thereby exposing the gill and foot. The remaining central portion, containing the shell protecting the internal organs, remains intact.

This specimen of Sebadoris fragilis, in order to make an escape, has cast off large lateral sections of its mantle leaving all the vital organs in the central body portion. Note the very clean fracture lines. A number of Discodorididae species will autotomize portions of their mantle in this manner and intertidal specimens are particularly noted for it. There are even reports in the literature where a complete outer ring of the mantle skirt has been autotomized and the central part of the animal crawled away. (Image by kind courtesy of Ian Hutton, Lord Howe Island.)

Others, such as some of the sacoglossans, have the ability to sacrifice their tail, parapodial lobes or dorsal appendages.

A specimen of Oxynoe viridis with its long tail reduced to a regenerating stump. It is surmised that the tail has been autotomized at some point to enable the animal to effect an escape. Compare with the animal in the image below. (Image by kind courtesy of Scott Johnson, Bali.)

In this image the usual elongate tail of Oxynoe viridis can be seen. A milky defensive secretion (believed to be distasteful and noxious) is often discharged prior to autotomy of the tail.

This Oxynoe viridis is missing its tail completely posterior to the shell. (Image by kind courtesy of Terry Farr, Sunshine Coast, Qld)

Many of the aeolid nudibranchs will autotomize their cerata, at a point of constriction near the notal insertion point, as a defensive method as do also some of the dendronotina, including species of Melibe, Tethys, Doto and Janolus. Some species are known to more readily cast off their cerata, when under threat, than others.

The post-pericardial, dorsal surface of an undescribed aeolid nudibranch exhibiting a dozen detachment points where its cerata have been autotomized.

The commencement of regeneration of the autotomized cerata down the right side of a Flabellina rubrolineata specimen. Several of the new buds, probably about a week into the regeneration process, have been arrowed. The nudibranch has turned its head region and mouth towards the camera lens.

An undescribed species of Melibe that has autotomized all of its large paddle-like cerata except for the two posterior-most, at right in image. It appeared unaffected by the loss and was still moving and feeding by throwing the large oral veil, left in image, over the substrate.

Autotomized cerata in particular are known to wriggle and writhe for quite some time (as much as two days in some reports) creating a more attractive target for the predator as a diversion. In many instances these detached cerata adhere to the substrate or even the attacker by virtue of a sticky secretion. Autotomy in the sea slugs is not executed in isolation. Other defensive methods are implemented in conjunction. Many sea slugs combine the autotomy process with the release of defensive secretions and large amounts of mucus as well, from specialised glands, both from the excised portion and the main body. The copious mucus serves to keep the noxious defensive secretions from being diluted or dissipated from the site. The ability of the cerata to adhere to an attacker reinforces the capability of the defensive secretions to create the greatest and ongoing discomfort.

An autotomized ceras (singular: ceras; plural: cerata) attached to a hydroid by its sticky tip. Appearance would suggest it to be from the aeolid Phyllodesmium magnum. Phyllodesmium species do not have functional cnidosacs in the ceras tip to store undischarged nematocysts that many aeolids obtain from their hydroid or anemone prey to recycle in defence. It is thought that the nematocysts of the soft corals they eat are ineffective for this use. Instead the ceratal tips contain glands that exude a sticky substance that cause them, once cast off, to adhere to the predator or to the substrate (here that sticky apical tip is attached to a hydroid). This prevents them being swept away in currents and surge thus remaining in the immediate vicinity. They wriggle for considerable time acting as a decoy, distracting the predator and hopefully enabling escape by the nudibranch.

The fracture lines, the autotomy planes, are set up with a particular type of granular cell structure plus musculature, nerve and vascular arrangements to enable the process to be carried out promptly and with minimal collateral damage. Studies have been carried out on some species, Melibe leonina in particular. The following is a very simplified explanation taken from the detailed description of research into the autotomy of cerata by Melibe leonina in a paper by Bickell-Page 1989. The cerata of Melibe leonina have a pair of sub-epidermal sphincter muscles on both sides of the autotomy plane with a second deeper pair surrounding the digestive gland that runs up the core of each ceras. Externally this area is visible as a basal restriction. Longitudinal muscle bands run through the autotomy plane. The various attachment points of these longitudinal muscles is important for subsequent fracture. Contraction of the longitudinal muscles and the circular sphincter muscles combined with the loss of tensile strength in the connective tissue attachments and surrounding tissue by degranulation of the granular cells causes a fracture and dislocation of the ceras. Closure of the resulting wounds on both sides of the fracture is effected by the sphincter musculature.

As previously mentioned autotomy is not an effective defence against all sea slug predators. The process and hopeful escape against a large active predator is too slow.

An aeolid nudibranch, Flabellina rubrolineata, being attacked and eaten by a species of Gymnodoris. Note an autotomized ceras bottom right. This defensive technique is not effective against the gymnodorids. Most of my observations of small gymnodorids attacking aeolids show the gymnodorid attacking beneath the ceratal line, into the side of the body wall.

Another Gymnodoris strike, this time on a Unidentia aeolid. Autotomized cerata are littering the foreground, to no avail.

Although survival in the short term may have been achieved there is a cost to the self sacrifice of course. The animal is now more susceptible to another attack having expended the sacrificial portions. Further energy and resources need to be applied to regenerate those lost portions. Studies on some aeolids have revealed that while signs of regeneration appear quite soon after autotomy, normal morphology is achieved at about 24 days, whilst complete regeneration of the cerata to full maturity and size takes about 40 days.

Give it up to hopefully get away.

References:

Fredericq, L. (1883). Sur l’autotomie ou mutilation par voie réflexe comme moyen de défense chez les animaux. Archives de Zoologie Expérimentale et Générale, Paris, Series 2, Vol. 1, pp. 413-426.

Stasek, C.R. (1967). Autotomy in the Mollusca. Occasional Papers of the California Academy of Sciences 61, 1-44.

Lewin, R.A. (1970). Toxin secretion and tail autotomy by irritated Oxynoe panamensis (Opisthobranchiata: Sacoglossa). Pacific Science 24: 356-358.

Willan, R.C. (1984) The Pleurobranchidae (Opisthobranchia: Notaspidea) of the Marshall Islands, Central-West Pacific Ocean. The Veliger, 27(1): 37-53.

Bickell-Page, L.R. (1989). Autotomy of cerata by the nudibranch Melibe leonina (Mollusca): ultrastructure of the autotomy plane and neural correlate of the behaviour. Phil. Trans. Roy. Soc. Lond. B324: 149-172.

Tsubokawa, R. & Bolland, R.F. (1991). Berthella martensi (Pilsbry, 1896), new to the Japanese Notaspidea Fauna. Venus, Japanese Journal of Malacology, 50(3): 184-195.

Piel, W.H. (1991). Pycnogonid Predation on Nudibranchs and Ceratal Autotomy. The Veliger 34(4):366-367.

Rudman, W.B. (1998, October 14). Autotomy. [In] Sea Slug Forum – http://www.seaslugforum.net. Australian Museum, Sydney.

Miller, J.A. & Byrne, M. (2000). Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators. Invertebrate Biology 119(2): 167-176

David A. Mullins – March 2020