Predators & defenses
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  Larval defenses
  Topics relating to predators & defenses include larval defenses, considered here, and PHYSICAL, CHEMICAL, and BEHAVIOURAL defenses, considered in other sections.
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Research study 1
 

drawing of post-torsional veliger larva of an abaloneAll marine gastropods undergo torsion during larval development.  This is a 180o rotation of the shell and viscera relative to the head and foot of the veliger.  It usually occurs in 2 stages, the first being a quick twist effected by unequal contraction of retractor muscles; the second being a slow growth of body parts to complete the rotation. Shown here is a post-torsional veliger of an abalone Haliotis. Drawing from Crofts 1929 HALIOTIS Publ XXIX Liverpool Mar Biol Comm Memoirs, Univ Press Liverpool, 174 pp.

NOTE sometime referred to as ontogenetic torsion; in other words, occurring during the development of the snail – but, as this is the only time it does occur, it seems to be unnecessary jargon

NOTE the role of the retractor muscles in torsion is considered in abalones Haliotis kamtschatkana in Research study 3 below. For review see Page 1997 Acta Zoologica 78: 227

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Research study 2
 

drawings of hypothetical pre-torsional adult snail and a contemporary post-torsional adult snailThere has been much conjecture about the function of torsion, and opinion is divided as to whether it benefits primarily the larva or the adult.  The major consequence to the veliger larva is that it can now retract its head and foot into the shell and seal it with the operculum (the operculum is produced at the same time as torsion). Since this ability (see figure on Right) carries over into the adult and provides protection for the adult against predators, drying, UV irradiation, and so on, there is no quarrel as to its post-metamorphic importance.  The intitial hypothesis for its function, proposed in the 1920s, is that it primarily benefits the larva (rather than the adult) by enabling it to protect its sensitive soft parts (head and velum) from being nipped off by planktonic predators.  But is this realistic?  Wouldn’t most predators either swallow veligers whole or crush their weak shells and then swallow the parts?  The idea for a larval function for torsion has lasted many decades and has many contemporary adherents.  Garstang 1929 Report Brit Assn Adv Sci 96: 77; drawings from Ghiselin 1966 Evolution 20: 337.

 

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Research study 3

 

photo series of normal torsion in a snail Calliostoma ligatumShown on the Left is normal torsion in a veliger larva of the trochid snail Calliostoma ligatum (the larva is about 300um in shell diameter). The retractor muscles attach the larval body to the shell and allow the body to be pulled in (usually only partly, before torsion).  In the Pre-Torsion photo, the foot is facing to the Right. At Mid-Torsion the foot has rotated 90o, while at Final Torsion the foot has rotated almost 180o and an operculum has formed. The larva is now able to pull into its shell and close off the opening. The scientist who originated the larval-defense theory, Walter Garstang, thought that a sudden mutation imposed an asymmetry on these muscles in an otherwise symmetrical ancestral larva, thus torquing the larval body and producing torsion.  The condition, with its presumed benefits, produced a new evolutionary line leading to present-day gastropods.  photo series showing abnormal torsion in a snail Calliostoma lilgatum caused by exposure to antibioticsHowever, several scientists have questioned the role of the retractor muscles in torsion. 

In the study considered here, antibiotics employed to control bacterial infection during embryonic culture of keyhole limpets Diodora aspera and trochid snails Calliostoma ligatum are found to interfere with the attachment of the retractor muscles to the inner wall of the larval shell, yet torsion still occurs. Such observations, and others, place into question the fundamental tenents of Garstang’s theory regarding the larval function of torsion.  Page 2002 Evol & Develop 4: 212; for information on torsion in other gastropods, including the caenogastropods Amphissa columbiana and Euspira lewisii see Bondar & Page 2003 Invert Biol 122: 28

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Research study 4
 

photograph of snail Pupillaria pupillus

In adddition to the retractor-muscle issue, other studies cast doubt on Garstang’s hypothesis.  For example, torsion in the west-coast species Pupillaria (Margarites) pupillus could not be caused by contraction of the retractor muscles because the larval shell is not fully calcified at this time and could not hold up to the stress. Hickman & Hadfield 2001 Biol Bull 200: 257. 

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Research study 5
 

Additionally, veligers of some species (e.g., littorines and sea hares Aplysia) withdraw not into the mantle cavity, but into the shell cavity, because the mantle fold is not firmly attached in the post-torsional larvae.  Note in the drawings that on withdrawal into the shell, the mantle fold "slips" down, making drawings of sea-hare Aplysia veligers showing loose fastening of mantle tissue in the veliger larvaeroom for the velum and foot. The implication of this is that this space would be available for the larva to withdraw its “fragile” head/velum into regardless of whether torsion happened or not; thus, the position and volume of the mantle cavity is irrelevant. Further, on microscopic examination the head and velum appear no more “fragile” than the foot; thus, there is no need to invoke the “special” protective strategy conferred by torsion.  The observations in these and other Research studies question several basic tenents of Garstang’s theory.  None of these criticisms by themself is enough to discount Garstang’s theory, but together they cast a sense of “reasonable doubt”. Thompson 1967 Malacologia 5: 423. 

NOTE Garstang's idea of a sudden macromutation leading to torsion and a new evolutionary line is also criticised (for a consideration of this idea and a review of older literature see Ghiselin 1966 Evolution 20: 337). At least one author agrees that torsion could have originated as a single mutation or “macromutation” leading to a major evolutionary advance, namely, Goodhart 1987 J Moll Stud 53: 33)

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Research study 6
 

histograms showing consumption of pre-tort and torted veliger lavae of abalone by several different planktonic predatorsWhat about a test of the hypothesis?  The first and possibly only test1 of Garstang’s larval-benefit hypothesis, at Friday Harbor Laboratories, Washington, assesses rates of predation by 7 planktonic predators from 4 phyla on pre-torted and torted veliger larvae of abalone Haliotis kamtschatkana.  The torted larvae at this time are only 90o twisted, but can fully retract2 and seal the shell aperture with the operculum, and are similar in size and swimming ability to the pre-torted larvae.  The null hypothesis in the experiment is that there will be no difference in numbers of pre-torted and torted veligers eaten by the predators.  The predators include megalops larvae (decapod crustacean), copepods, hydromedusae3, ctenophorans, and juvenile pink salmon.  Results show that all but one predator (a ctenophore species) eat significant numbers of Haliotis larvae.  Only two predator species, however, eat significantly more of one veliger type or another.  Megalopae eat more torted larvae and one species of medusa eats significantly more pre-torted larvae. The authors conclude that torsion in Haliotis does not function defensively4 and that other selective pressures have maintained the trait.  Pennington & Chia 1985 Biol Bull 169: 391.

NOTE1  tests are run in 1-liter jars with 50 veligers and one predator except for: megalopae (5 individuals), copepods (5 individuals), and salmon (2 individuals) over a 15-h period.  Each combination is replicated 5 times.  “Number eaten” is corrected for veliger losses in control jars (without predators).  Two runs are done, one with pre-torted veligers and one with torted veligers.  The authors culture the larvae of H. kamstschatkana to a 48h stage (pre-torted) and 120h stage (torted).  Although not specifically mentioned in the study, it is presumed that predators are not re-used, thus avoiding possible learning (dietary conditioning) effects

NOTE2  many (or most) species cannot fully withdraw into the larval shell until torsion is completed

NOTE3  the authors test 2 species of medusae but, as one species ate so few of either type of larvae, the data are not included here

NOTE4  not all researchers support the authors’ conclusion.  At least one scientist criticises the choice of abalone larvae in the experiments, based on the fact that Haliotis is one of only a few gastropods with a free-living pre-torsional larva (most undergo torsion before hatching).   Also criticised are the generally “inconclusive” results obtained in the experiments (only 2 predators are recorded as eating significantly more of one type or another of the larvae...see red asterisks in the histograms)

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Research study 7
 

As noted above, there are other objections to the larval-benefit theory and other ideas regarding torsion, but only the single experimental test.  The authors of the Haliotis study acknowledge the possibility that torsion may protect veligers from adverse physical conditions, but do not explain.  One such example may relate to the behaviour of swimming veligers that have undergone torsion.  When the larvae bump into something, they immediately withdraw into their shells and sink down.  Even the boundary layer of freshwater overlying seawater in a test-tube causes this response – either acting as a physical or chemical obstruction, or both.  So, even though torsion may not protect veligers from predators, it may protect them from surface haloclines or similarly averse chemicals. 

NOTE  in fact, this behaviour forms the basis for Garstang’s theory, and is eloquently described in the first verse of his delightful poem, The ballad of Veliger, or how the gastropod got its twist:

         Veliger’s a lively tar, the liveliest afloat,
         A whirling wheel on either side propels his little boat;
         But when the danger signal warns his bustling submarine,
         He stops the engine, shuts the port, and drops below unseen.

Garstang 1962 p. 36 In, Larval Forms with other zoological verses Basil Blackwell, Oxford
(see Research Study 9 below for more on Garstang and his poetry)

NOTE  this is easily set up by gently pouring freshwater into a test-tube containing swimming veligers of any kind in seawater, and observing the behaviour of the veligers under a stereomicroscope.  For greater contrast the freshwater can be coloured with a vital dye such as methylene blue

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Research study 8
 
photograph of turbinid snail Pomaulax gibberosa with symbiotic worm

A feature that seems to be ignored in this veliger/torsion research, or at least not given the attention that it deserves, is the operculum.  It appears in post-torsional larvae and, while perhaps not so important (it seems) for survival of the veliger stage, is of critical importance for survival of juvenile and adult stages.  The shell and operculum are arguably the two most important morphological features enabling colonisation of intertidal and land habitats by gastropod molluscs.

 

The large west-coast turbinid snail Pomaulax (Astraea) gibberosa
has a thick, pearly operculum, the beauty of which is not done
justice in this photograph. The snail is partly out of water and
its commensal polynoid worm has come out to investigate 0.6X

 
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Research study 9
 

photograph of Walter Garstangphotograph of book of poetry "Larval forms and other zoological verses" by Walter GarstangIn addition to being knowledgeable about marine-invertebrate larvae and fervently interested in the role of larvae in evolution of invertebrates, Walter Garstang had a delightful knack of presenting his ideas, and some quite serious ones at that, in the form of light-hearted verse.  These are collected in a book of poetry, published in 1962.  In addition to the perennial favourite “The ballad of Veliger...”, are the equally enjoyable and evolutionarily provocative The amphiblastula and the origin of sponges, The invaginate gastrula and the planula, Mülleria and the ctenophore, Tornaria’s water-works,and many others.  Because the book is several decades out of print and may not be readily available to many students, the poem most germane to this section of the ODYSSEY is presented in full, with identical spelling to the original:

The ballad of Veliger, or how the gastropod got its twist:

Veliger's a lively tar, the liveliest afloat,
A whirling wheel on either side propels his little boat;
But when the danger signal warns his bustling submarine,
He stops the engine, shuts the port, and drops below unseen.

He's witnessed several changes in pelagic motor-craft;
The first he sailed was just a tub, with a tiny cabin aft.
An Archi-mollusk fashioned it, according to his kind,
He'd always stowed his gills and things in a mantle-sac behind.

Young Archi-mollusks went to sea with nothing but a velum -
A sort of autocycling hoop, instead of pram - to wheel 'em;
And, spinning round, they one by one acquired parental features,
A shell above, a foot below - the queerest little creatures.

But when by chance they brushed against their neighbours in the briny,
Coelenterates with stinging threads and Arthropods so spiny,
By one weak spot betrayed, alas, they fell an easy prey -
Their soft preoral lobes in front could not be tucked away!

Their feet, you see, amidships, next the cuddy-hole abaft,
Drew in at once, and left their heads exposed to every shaft.
So Archi-mollusks dwindled, and the race was sinking fast,
When by the merest accident salvation came at last.

A fleet of fry turned out one day, eventful in the sequel,
Whose left and right retractors on the two sides were unequal:
Their starboard halliards fixed astern alone supplied the head,
While those set aport were spreadabeam and served the back instead.

Predaceous foes, still drifting by in numbers unabated,
Were baffled now by tactics which their dining plans frustrated.
Their prey upon alarm collapsed, but promptly turned about,
With the tender morsal safe within and the horny foot without!

This manoeuvre (vide Lamarck) speeded up with repetition,
Until the parts affected gained a rhythmical condition,
And torsion, needing now no more a stimulating stab,
Will take its predetermined course in a watchglass in the lab.

In this way, then, Veliger, triumphantly askew,
Acquired his cabin for'ard, holding all his sailing crew -
A Trochosphere in armour cased, with a foot to work the hatch,
And double screws to drive ahead with smartness and despatch.

But when the first new Veligers came home again to shore,
And settled down as Gastropods with mantle-sac afore,
The Archi-mollusk sought a cleft his shame and grief to hide,
Crunched horribly his horny teeth, gave up the ghost, and died.
                                                  - Walter Garstang 1928

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Although torsion may seem esoteric and more suited as a topic for philosophical discussions in turn-of-the-century drawing rooms, it is actually one of the more dynamic and interesting controversies in marine-invertebrate study. A dialogue of opinion and argument has been on-going for 80 years! Students interested in such things (and in torsion) should additionally read the references cited in Pennington & Chia 1985 Biol Bull 169: 391 and Page 2002 Evol & Develop 4: 212.

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