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<I>Vermicularia Spirata</I>

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<I>Vermicularia Spirata</I> ECOLOGY AND FUNCTIONAL SIGNIFICANCE OF UNCOILING IN VERMICULAR/A SP/RATA: AN ESSAY ON GASTROPOD FORM! STEPHEN JAY GOULD Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138 ABSTRACT In Bermudian waters, the uncoiling marine snail Vermicularia spirata cements itself to a variety of hard substrates, predominantly to the tree coral Oculina. Uncoiling has two major functions: rapid upgrowth to attain earlier access to the rain of detrital food particles, and flexibility in growth required for stable attachment. The branching Oculina is preferred because it provides numerous attachment sites along the course of upward growth. Snails attached to Oculina begin to uncoil earlier than those ce- mented to less advantageous substrates. Comparison of the uncoiled shell with a hypothetical coiled individual of equal shell growth provides an in- dex of uncoiling. Snails attached to Oculina are more highly uncoiled than those attached to massive brain corals; snails attached to vertically oriented colonies of Oculina are more loosely coiled than those cemented to stub- bier, horizontally branched colonies of Oculina; shells fastened to the bases of colonies of Oculina are more uncoiled than those attached near the tops of the same colonies. Although many Vermicularia are very loosely coiled, none approach the theoretical optimum of uncoiling (a straight tube after attachment). Although this is due partly to the necessity for growing around obstacles, the major constraint upon complete uncoiling is the in- herited spiral mode of molluscan growth. Uncoiling is not random; Vermi- cularia always uncoils as a dextral spiral. INTRODUCTION "God," said the Reverend Moseley (1838:354), "hath bestowed upon this humble architect the practical skill of a learned geometrician." Among molluscan architects often cited for the mathematical regularity of their coiling, Turritella occupies a prominent place. Both Moseley and D'Arcy Thompson (1942) singled out its faithful correspondence to the ideal form of a logarithmic spiral. Yet one of its descendents, the worm shell Vermic- ularia (see Morton, 1953), is so markedly erratic in the uncoiling of its later whorls that the pattern has been described as random (Abbott, 1954: 144). Two questions come to mind: What is the adaptive significance of uncoiling in Vermicularia? What is the pattern of uncoiling; is it truly random? I shall, in this work, deal with these questions as they apply to 1 Contribution No. 457 from the Bermuda Biological Station for Research. 1969J Gould: Uncoiling in Vermicularia 433 the common North American worm she]], Vermicularia spirata (Philippi, 1836), in Bermudian waters. Most snails are mobile, benthic browsers, feeding on plant material scraped up by the toothed radula. The choice of actively searching for food as a mode of life requires that the snail's long body be housed in a compact, relatively streamlined shell. In the absence of shell segmentation, regular coiling is the most efficient way to fulfill this requirement. It is not surpris- ing, therefore, that most immobile snails depart from the usual patterns of coiling. The filter-feeding capulid and calyptraeid "limpets" (including the slipper shell Crepidula) have not become irregular in their coiling, but they expand the generating curve so rapidly that very few whorls form before adult sizes are reached. Another departure, uncoiling, has been developed independently by several groups of filter-feeding gastropods, often for dif- ferent reasons. (See Yonge, 1937, on the relationship of filter feeding and sessHity.) Many of the intertidal true vermetids cement to rocky shores in the wave zone and uncoil erratically in order to provide a maximum sur- face for attachment. Several siliquariid species live in sponges; their loose coiling produces the rapid axial translation that may be necessary to keep up with the growth of their host (W. J. Clench, personal communication). I propose that loose coiling in the turritellid Vermicularia spirata also has rapid growth along the axis as its primary adaptive significance. But the impetus for rapid growth is different here; V. spirata cements its shell to a variety of hard substrates and grows upwards. Rapid upgrowth provides a dual advantage: earlier access to the rain of detrital particles that consti- tute the food supply and quick elevation above bottom sediment that might clog the ciliary feeding apparatus. Yet loose coiling is not the only require- ment for success in cementing forms; flexibility is necessary so that ob- stacles in the course of upgrowth can be circumvented and additional points of attachment secured when necessary. A loosely, but extremely regularly, coiled genus such as Laxispira (often incorrectly regarded as a subgenus of Vermicularia, e.g., by Cossmann, 1912) is far too controlled in its direc- tions of growth for success in such an environment. Vermicularia spirata thus combines the rapid directional growth of siliquariids with the flexibility for continual attachment of vermetids. Such requirements may seem con- tradictory, for horizontal growth to secure attachment should operate in opposition to vertical upgrowth. The potential conflict can, however, be resolved by a suitable choice of substrate, one which provides numerous sites of attachment along the course of upward growth (see Fig. 1). NATURAL-HISTORY OF V. spirata During the summers of 1964-1967, I studied the morphology and mode of life of Vermicularia spirata in Bermudian waters. This common species 434 Bulletin of Marine Science [19(2) FIGURE 1. A specimen of Vermicularia spirata attached to a vertically oriented colony of Oculina (initial turritellid stage at A, adult aperture at B). Note the availability of numerous attachment sites along the course of upward growth, allowing stability to be maintained with rapid upgrowth. 1969] Gould: Uncoiling in Vermicu/aria 435 lives both in protected bays and lagoons (Walsingham Pond, Harrington Sound) and in subtidal open-sea habitats. Its range of depth is large. In Harrington Sound, for example, V. spirata inhabits all depths from inches below extreme low tide to the maximum of 82 feet (Neumann, 1965). Its temperature tolerance must also be great, for it is common throughout the West Indies and has been reported as far north as Buzzards Bay, Massa- chusetts (Stimpson, 1851). The protoconch of Vermicularia spirata is reduced in comparison with that of Turritella species having a free-swimming veliger; Morton (1953: 84) thus supposed the veliger stage to be suppressed in Vermicularia. The foot, functionless and reduced in the attached adult, is small but functional in the regularly coiled turritellid juvenile stage. The maximum length of the extended juvenile foot is never more than Y:{ the length of the shell. Movement is most inefficient compared with that of most browsing snails. In poorly oxygenated tanks, juveniles of V. spirata will climb up the side walls of the aquarium. The juvenile moves in a series of small steps rather than in a continuous progression. The foot is extended and the animal moves forward out of its shell; the shell is then pulled up to the new level, but it falls slightly backwards before the sequence is completed. I timed sixty such sequences for an individual whose shell was 15.4 mm long and whose extended foot had a maximum length of 4.5 mm. The average for- ward motion was 1.65 mm per sequence (36 per cent of the foot's length) and a sequence averaged 21.4 seconds. When placed in a sandy-bottomed aquarium tank far from a potential uncoiling site (the coral Ocu/ina), individual juveniles either form a Tur- ritella-like feeding burrow in the sand or crawl to the coral and lodge them- selves in a stable spot thereon. I have seen them resting immobile on the coral, though presumably capable of movement, for up to two weeks be- fore physically cementing to begin uncoiling. Either in the sand burrow or on the coral, they filter feed, as does the adult, by passing water currents in and out between the operculum and the shel1 margin. The operculum is held at, or just slightly in front of, the shell margin at all times unless the animal is disturbed, at which time the operculum is sharply retracted far into the shell. The diameter of the operculum is slightly smaller than that of the aperture, but the difference is not enough to account for the deep retraction of the animal. This is permitted by the extremely flexible oper- cular edge which lacks the supporting bristles of Turritella. THE COILED JUVENILE SHELL The most outstanding aspect of Vermicularia's distribution in Bermudian waters is its preference for the tree-coral Oculina as a substrate for cemen- tation and subsequent uncoiling. I have never seen a large accumulation 436 Bulletin of Marine Science [19(2) of colonies of Oculina without attached Vermicularia; often every coral colony is host to many uncoiled snails. Where Oculina is not found, Ver- micularia is rare or absent (with the single exception of Walsingham Pond [see Gould, 1968], where large numbers have no sites for attachment). If the hypothesis of the introductory section is accepted, then this striking cor- relation can be explained. If rapid upgrowth with secure attachment is advantageous, then Oculina is unique among potential substrates in pos- sessing a vertically oriented, branching structure which provides numerous attachment sites along a potential course of upward growth. Indeed, the only other possibility would be the loosely spiralled shells of other individ- uals of Vermicularia. I have seen museum specimens, purportedly from Bermuda, of colonies of Vermicularia in which 50 to 100 shells, their aper- tures all pointing upwards, form an intertwining network of highly uncoiled tubes. Data on variation in length of the juvenile coiled shell confirms the pref- erence for Oculina as an attachment site, for mean length of the turritellid stage is shortest in Oculina-based local populations.
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