Columellar muscle of neogastropods: muscle attachment and the function of columellar folds.
Malacologists often assume that gastropod shell ornamentation is adaptive, but experiments that demonstrate the function of these presumed adaptations are rare (Morton, 1967; for notable tests of ornamentation function, see Palmer, 1977, 1979; Bertness and Cunningham, 1981; Appleton and Palmer, 1988; Marko and Palmer, 1991; West et al., 1991; Carefoot and Donovan, 1995; Donovan et al., 1999). Columellar folds, plications on the columella, or central column of a gastropod shell (see Fig. 1), are particularly intriguing ornaments because they evolved repeatedly in a number of clades, such as the Caenogatropoda, Opisthobranchia, and Pulmonata (Price, 2001). In the subclade Neogastropoda of the caenogastropods, the columellar folds may be an adaptation that is intimately related to the columellar muscle (Fig. 1). In fact, the muscle does attach the animal to the columella (Signor and Kat, 1984; Fretter and Graham, 1994) and has grooves that fit between each fold. In this paper, I test three hypotheses that purport to explain a functional relationship between the columellar folds and the columellar muscle.
[FIGURE 1 OMITTED]
Columellar folds are readily visible on the inner lip of many shells, and systematists have used the impressive diversity of fold shapes to distinguish species and higher taxa. I consider a fold to be any ridge on the inner lip of the aperture that extends along the columella for a number of whorls, usually extending all the way to the apex. Some folds occur at the bottom edge of the aperture, as in Nassarius vibex, whereas others, such as those in Terebra dislocata, are located in the center of the inner lip. Folds can be wide (Triplofusus giganteus) or narrow (Nassarius vibex), subtle (Busycon contrarium) or prominent (Vasum muricatum).
The columellar muscle conforms exactly to the shape of the folds where it lies over them, and this conformation has inspired the hypotheses that are most commonly cited to explain the function of folds. These hypotheses must be considered in light of the fact that the columellar muscle functions as a muscular hydrostat (Thompson et al., 1998), controlling protraction from, and retraction into, the shell. Like hydrostatic skeletons in general, the volume of a muscular hydrostat remains constant, so a contraction in one direction induces elongation in an opposing direction (Kier and Smith, 1985). The columellar muscle is composed of muscle fibers that are oriented longitudinally, transversely, and obliquely with respect to the long axis of the columellar muscle (Thompson et al., 1998). Thus, the columellar muscle controls its own twisting, shortening, and elongating in addition to protraction and retraction.
Dall (1894; restated by Fretter and Graham, 1994) published the only nonfunctional explanation of folds. His explanation does not pertain to the columellar muscle, relying instead on the nature of the mantle, the tissue that secretes the shell. Dall surmised that folds, and all other internal ornamentation including the parietal ridge, lirae, and teeth on the outer lip, were deposited in the wrinkles that would form when ah overly large mantle retracted into the shell. This idea predicts that ornamentation would be more pronounced at the aperture (Dall, 1894), but ornamentation around the aperture where the mantle is largest is exaggerated only in some species with determinate growth (Paul, 1991; Vermeij and Signor, 1992; Venneij, 2001a); furthermore, contrary to Dall's prediction, not all of these animals have columellar folds. Indeed, the internal morphology of gastropods is highly stereotyped, not random, and it is unlikely that the mantle would always wrinkle uniformly (Signor and Kat, 1984). There are also no obvious differences in mantle size between species with and without internal ornamentation in general, or columellar folds in particular (pers. obs.).
Three interrelated hypotheses have been presented to explain how the folds affect the function of the columellar muscle, thereby explaining both why folds have evolved and why so many neogastropod lineages maintain them:
1. Guidance. Columellar folds guide the columellar muscle as the animal moves in and out of its shell (Signor and Kat, 1984; Ponder, 1972). The analogy here is that the folds act like a railroad track guiding a train; that is, they prevent the animal from slipping in its shell. One manner in which the folds may guide the muscle is by protruding far into the columellar muscle, restricting the muscle movement along the folds. In this event, the area of contact should be greater in species with folds than in those without. I test this prediction.
Signor and Kat (1984) limited their guidance hypothesis to high-spired, narrow (turritelliform) species, implying that the columellar muscle would slip within the shell unless folds guided its movement. Any attempt to extend this hypothesis to low-spired shell shapes must account for the absence of folds in some large neogastropods, such as Syrinx aruanus, whose shell can reach almost a meter in length (Harasewych and Petit, 1989).
2. Maneuverability. Columellar folds enhance a snail's ability to maneuver its shell (Fretter and Graham, 1962; Vermeij, 1978). A number of authors have assumed that the shape of the muscle's physical attachment to the columella is small and circular, like the adductor muscle attachment in bivalves (e.g., Linsley, 1978; Signor and Kat, 1984; Morita, 1993; Thompson et al., 1998). Vermeij (1978) assumed that the attachment occurs immediately over the folds and predicted that animals with folds would consequently have a larger surface area of muscle attachment. An animal with greater attachment area might be better at maneuvering its shell, for example when it swings the shell back and forth to fend off a predator (Thompson et al., 1998), or when it pries open the shells of prey (Taylor et al., 1980). This hypothesis has remained untested because dissections usually begin by removing and discarding the shell, and because the muscle easily detaches from a cracked shell.
3. Predator avoidance. Snails with columellar folds can withdraw more deeply into their shells (Dall, 1894), increasing their ability to escape from predators. Dall (1894) commented that snails with columellar folds retract more deeply, but presented no data in support of this idea. Since then, others have documented that snails that retract more deeply are better at escaping predators: they are harder to reach, and they take so long to handle that the predator eventually abandons the task (Vermeij, 1978, 1987). Although it is not immediately obvious why these behaviors might be associated with columellar folds, the data required to confirm Dall's claim are easy to collect.
I have developed procedures for dissecting gastropods while keeping the columellar muscle intact; employed a novel mathematical algorithm that converts a photograph of a snail into a three-dimensional surface from which I can measure areas; and examined neogastropod species that represent a range of columellar fold morphologies, as well as species with smooth columellae. Contrary to what has been assumed, the muscle attachment to the columella is complex and leaves no scar. None of the three hypotheses outlined above adequately explain the functional relationship between the columellar folds and the columellar muscle.
Materials and Methods
Quantitative data on the columellar muscle were collected from seven species with folds (from live genera and four families) and five species lacking them (from five genera and three families), affording phylogenetic breadth (Table 1). One of the species without folds, Strombus alatus, is not a neogastropod; it is a caenogastropod (a clade that contains the neogastropods) with shell shape similar to other species considered here. At least two and up to five specimens were studied for each species, for a total of 31 specimens for most measurements (36 specimens for attachment depth). These data were supplemented with qualitative observations from an additional nine species. All specimens were stored in 70% ethanol and deposited at the Field Museum of Natural History (FMNH), Chicago, Illinois. Except for Oliva sayana, all species have a functional operculum, eliminating any possible bias introduced by a relationship between folds and an operculum.
The sample includes species with a variety of columellar fold shapes and numbers (Table 2), but all have fairly modest folds. Prominent folds, such as those in the Mitridae, Volutidae, and Cancellariidae could not be included, because they were too difficult to collect or purchase alive. Oliva sayana has plications on the inner lip of the aperture that some authors describe as columellar folds (e.g., Abbott, 1974), but these do not continue inside the shell, and they therefore do not contact the columellar muscle, even when the animal is fully protracted. As such, these apertural plications cannot affect the function of the columellar muscle, so I consider Oliva sayana to be without folds.
Terminology describing orientation
A description of fold morphology requires terms that orient the reader to the snail shell (Fig. 1). In this paper, all terms refer to a snail shell in a standard orientation, with apex up and aperture visible (and on the right for dextral species). Top and bottom refer to positions along the coiling axis. The bottom of a whorl is farthest from the apex, whereas the top of the whorl is closest to the apex. The width of a feature is measured along a line parallel to the top-bottom axis, following the convention that the short axis of the columellar muscle represents width, whereas the long axis of the columellar muscle represents length (Fig. 1A, E, Fig. 2E). Apical and apertural refer to directions along the spiral of the shell towards the tip or opening respectively: the columellar muscle narrows apically, but is wide aperturally. A junction occurs where the bottom of one whorl meets the top of another. The depth of a feature indicates the number of revolutions between it and the aperture, where one revolution is 360[degrees]; for example, the columellar muscle attachment might begin at a depth of 300[degrees].
[FIGURE 2 OMITTED]
Dissections were performed on live, untreated animals. Surprisingly, any treatment of animals, such as freezing, storing in ethanol, of relaxing in magnesium sulfate (Epsom salts), caused the muscle to detach from the shell, even when tugged only slightly. Fresh material is therefore essential to study columellar muscle attachment.
To expose the soft tissues while keeping them and the columella intact, 1 used a Dremel rotary tool with a 1.6-mm-diameter carborundum abrasive wheel to cut away the exterior. The size of the blade limited the specimens that could be dissected with precision to those with whorls larger than hall a centimeter. Thus, the attachment morphology could be quantified in the largest specimens of Nassarius vibex, but the available specimens of Columbella rusticoides were too small. The largest whorl of Terebra dislocata, a high-spired species, is only a few millimeters tall, so it could not be quantified with these methods. Although the most apertural point of the attachment was documented in Oliva sayana, the morphology of attachment throughout the test of its length was inaccessible, because the delicate columella cannot withstand even slight pressure.
To distinguish between muscle that was physically attached and muscle that was simply pressed against the columella, I used a blunt but flexible 34-gauge copper wire to probe between the tissue and columella. In all cases, only the top of the muscle (that closest to the junction between two whorls; see Figs. 1, 2) was physically attached. Since the bottom of the muscle was free, the attachment was not disturbed when probed.
The measurements required to test the hypotheses (Table 3) were the standardized (see below) total area of muscle physically attached to the columella, the standardized total area of muscle in contact with the columella throughout the attachment, the depth of attachment, and the length of the attachment.
It was especially difficult to measure the total area of muscle physically attached to the columella (ATT in Figs. 1, 2). In these species, the columellar muscle attachment does not scar the shell, so the attachment area had to be observed directly. I tried removing strips of columellar muscle that were not attached to determine how much muscle was left on the columella, but this procedure inevitably destroyed the attachment. However, the attachment was so narrow relative to the total width of the columellar muscle that, when measured from digital photographs, it could be reasonably estimated as a thin but long box, only one pixel wide but many degrees long. The small bias introduced by this approximation should be the same in species with and without folds.
Another challenge was to measure the surface area of contact between the columellar muscle and the columella (CM in Figs. 1, 2G). The apertural end of the muscle grades into the foot (Voltzow, 1990; Thompson et al., 1998), so the only point that could be consistently identified at the apertural end of the columellar muscle was the point at which the muscle attachment began (ATT in Fig. 2E). I measured the total area of muscle in contact with the columella: beginning with the attachment, extending down the width of the muscle to the bottom of the whorl, and extending across the columella to include the most apical part of the muscle (CM in Figs. 1, 2G). Because the muscle always spanned the columella between the attachment and the bottom of the whorl, this measurement could be made in relaxed, contracted, and protracted animals. The position and length of the muscle attachment and the area under the attachment remain the same regardless of the animal's behavior. The exclusion of the area between the foot and the initial attachment was justifiable: it never included muscle that conformed to the morphology of the folds and was therefore not relevant to the present study; there was no reason to assume that it varied differently in species with and without folds.
Both the attachment area and the contact area were standardized to the columellar area (CA in Fig. 1; Table 3) to remove the effect of size. Columellar area is the area of the columella above, below, and including the length of attachment.
I used the depth of attachment as a proxy for depth of retraction, measured as the number of degrees behind the aperture. The two depths are intuitively related, because an animal cannot retract deeper than its attachment. Depth of attachment was much easier to measure, and it is not subject to behavioral variation. This proxy assumes that the amount of space between the columellar muscle attachment of the contracted animal and its operculum varies equally among species with folds and those without.
The length of attachment was defined as the number of degrees between the depth of attachment and the apical edge of the attachment, which occurred in the crease between the columella and the rest of the shell (Fig. 2F, G). Some muscle fibers and connective tissue extended even farther apically beyond this point, but they were small and thus likely to function differently from the rest of the muscle. My methods were too coarse to dissect this tiny strand of tissue accurately.
Because the length of attachment and the depth of attachment were both measured as the number of revolutions behind the aperture (in degrees), they were independent of size and did not need to be standardized.
All measurements were taken from a series of digital photographs that documented each dissection. However, photographs distort three-dimensional data into two dimensions, so the surface areas in the photographs under-represent true areas. I therefore developed a procedure to process the series of photographs for each dissection, as well as a geometric algorithm that calculates the three-dimensional area projected into each photograph. The algorithm is presented in the Appendix.
Photographs were taken with a Nikon CoolPix 950 digital camera. The image plane of each photograph was parallel to the coiling axis, to which the optic axis was perpendicular. Each photograph also included a scale bar, was centered on a landmark, and showed the muscle attachment and the edge of the columella.
The outside of each shell was marked with radial lines running perpendicular to the junctions between whorls (LM in Fig. 1) every quarter of a whorl for small specimens and every eighth of a whorl for larger specimens (generally, those with shells longer than 2 cm). These landmark lines were used to locate the image within the series.
Each series consisted of between 4 and 12 photographs, with at least one photograph per quarter whorl. To create each series, all images were scaled and oriented identically. Only the middle 90[degrees] sector within each photograph was measured (45[degrees] on either side of the landmark line), thus eliminating overlap among the images (Fig. 2C).
The algorithm employed to estimate surface area converted tracings of photographs into three-dimensional surfaces (Fig. 2A-C). I used a mouse of mouse tablet (Wacom Graphire2) to trace the surface areas of the muscle attachment, the muscle in contact with the shell, and the columella within each image. Tracings were transformed according to the procedure described in the Appendix (implemented in MATLAB ver. 6.0; Fig. 2D), and then areas were summed from each image in the series. The procedure used to calculate the number of degrees from the aperture to the apertural and apical ends of the attachment is also described in the Appendix.
The 20 largest specimens were used to determine the precision of each measurement. I had two quarter-whorl series for these specimens, because they were photographed every eighth of a whorl; one series, for example, depicted the attachment centered on landmarks at 135[degrees], 225[degrees], 315[degrees], and 405[degrees], and the other centered on landmarks at 180[degrees], 270[degrees], 360[degrees], and 450[degrees]. I averaged the final measurements from the two series.
The three-dimensional reconstruction technique employed here did not take into account the presence of folds. To account for folds, I employed a scale factor ("modifier") defined as the length of the projected outline of the folds divided by the minimum distance between the two endpoints of the folds (Fig. 1B; Eq. 1):
(1) modifier = [Length.sub.outline]/[Length.sub.minimum]
When there are no folds, the minimum length equals the length of the outline, so the lower limit of the modifier is 1.
I measured the fold modifier in each of the photographs of a series that clearly showed the folds' silhouette. This measurement is highly sensitive to shell orientation and to the endpoints of the fold outline, for which I used inflection points. To compensate for this sensitivity, I always used the maximum fold modifier; this approach favored finding a statistical difference between groups with and without folds. Although there was considerable variability in fold modifier values within a species, the variance for the entire sample of species with folds was low (fold modifier variance, 0.003; range, 1.0 to 1.2; 114 measurements over 17 specimens).
After measuring the surface area of the columellar folds, and transforming it according to the algorithm in the Appendix, I applied Equation 2:
(2) [Area.sub.final] = [A.sub.T] - [A.sub.fT] + ([A.sub.fT] x modifier)
where [A.sub.T] is the area transformed by the algorithm into an estimate of the area of a three-dimensional surface (cither attachment area or contact mea), and [A.sub.fT] is the similarly transformed area of the folds. In other words, I subtracted the transformed fold area from the attachment area, multiplied it by the fold modifier, added the product back to the attachment area, and then repeated the adjustment for the contact area.
The total surface area of the columella was not adjusted, because that measurement is used to standardize the other metrics. If fold surface area were added to columellar area, the difference between species with and without folds would be erased.
Statistical comparisons between species with folds and those lacking them were performed with a Mann-Whitney U test using StatView 5.0 for Windows.
Morphology of columellar muscle attachment
These dissections demonstrated that the columellar muscle attachment in neogastropods is far more complex than previously assumed (by authors such as Linsley, 1978; Signor and Kat, 1984; Morita, 1993; Thompson et al., 1998). The muscle did not leave a scar, so there was no macroscopic feature on the columella that approximated attachment shape. The shape of the attachment was similar in all species, regardless of the presence of folds (Fig. 2E-G). In most of the species examined, the attachment began about three-quarters of a whorl (~275[degrees]) back from the aperture (Fig. 3C, raw data for the histogram is in Table 4). The depth of attachment might be much deeper in high-spired shells. In Terebra dislocata, attachments began about two whorls back from the aperture (pers. obs.). T. maculata and T. subulata, muscles were previously reported to attach more deeply at about 2.5 and 4.5 whorls back from the aperture, respectively (Signor and Kat, 1984). In general, the attachment was long and sometimes extended for more than one revolution; it was restricted to the upper edge of the muscle (blue line is ATT in Fig. 2E-G).
[FIGURE 3 OMITTED]
The relative position of the attachment changed as it moved from the apertural edge of the muscle across to the apical edge. At its most apertural end, the attachment lay immediately under the junction of the two whorls. Tracing it apically along the rising junction, the attachment shifted in position progressively downward and across the columella toward the bottom of the whorl, with the rate of descent gradually increasing. Shortly before reaching the bottom of the whorl, the angle of the attachment changed dramatically, becoming more oblique to the junction and curving sharply down to the base of the whorl; this is where the attachment crossed the folds when they were present. Here the muscle was remarkably less robust than elsewhere along its length. Farther apically, the muscle was only a thin extension situated in the crease between the columella and the base of the whorl. Within the area where the muscle was attached, the muscle width was maximal at its apertural end and minimal towards the apex.
Contrary to the prediction drawn from the functional hypotheses outlined in the Introduction, no significant differences were found between species with and without folds with respect to the surface area of muscle attachment (P = 0.71), the amount of contact between muscle and columella (P = 0.16), or the length of muscle attachment (P = 0.21) (Fig. 3; Table 4). The depth of attachment in species with folds was significantly closer to the aperture than in species without folds (P = 0.020), which is opposite to what was predicted.
Three specimens (Busycon contrarium FMNH299449, B. contrarium FMNH299459, and Cantharus cancellarius FMNH299487) had fold modifier values close to unity (1.02, 1.00, and 1.04, respectively), meaning that the folds were almost flush with the columella and thus did not protrude enough to increase the topographic relief above that of specimens lacking folds. The data were consequently re-analyzed categorizing these three specimens as lacking folds. Results were identical for the contact area, attachment area, and length of attachment. However, the depth of attachment was no longer significantly different between species with folds and those lacking them (P = 0.19).
Using novel methods to examine the columellar muscle in situ, I have described, for the first time, the surprisingly complex attachment of the columellar muscle in neogastropods. This attachment is remarkable for its delicate structure, lack of discernible muscle scars, and considerable length. The data presented here do not support any of the previously published hypotheses thought to explain the function of columellar folds, although the species included do not exhibit the most exuberantly developed folds. These data cast doubt on the hypothesis that folds act as struts, guiding the columellar muscle as the animal protracts from, and retracts into, its shell. Furthermore, the muscle probably does not need to be guided, because it is a muscular hydrostat. The muscle probably mirrors the morphology of the folds simply because it is physically adjacent to them. I reject the hypotheses that animals with folds maneuver better because their attachment area is larger, and that these animals avoid predators by retracting deeper. While I reject these hypotheses as general explanations for columellar fold function in neogastropods as a whole, future work may demonstrate that some of them adequately explain function within groups of species with similarly shaped folds.
I developed two novel methods in this research: one is a practical dissection technique, and the other is ah analytical approach for measuring distances and areas from photographs of specimens. With the dissection technique, I described the columellar muscle attachment in 20 neogastropods and one caenogastropod (Table 1). The soft tissues of other gastropods can be dissected without damaging the columella, and future applications of this approach will provide a more general understanding of how soft tissues are situated within the shell. With the analytical approach, I determined the relative position of soft tissues and shell features. I quantitatively characterized the columellar muscle in 11 species of neogastropods and one caenogastropod (Tables 1, 3, 4). This algorithm will work for any organism arranged as a stack of circles--echinoderms, cnidarians, foraminifera, diatoms, and mushrooms, for example.
The measurements and their analysis test on three assumptions. First, to measure the area of contact between the columellar muscle and the columella, I assumed that the amount of muscle apertural to the attachment varies equally in species with and without folds. Second, I also assumed that the attachment area was only one pixel wide, which seems justified by the observation that the attachment was quite thin relative to the total width of the muscle. Third, areas were inflated by the algorithm that transformed the two-dimensional data, because the columella was assumed to be perfectly symmetrical (see Appendix). All of these assumptions were justified, especially in this first attempt to quantify differences in the columellar muscle. Furthermore, there is no a priori reason to believe that they would affect species with folds differently than species lacking them.
Note that the measurements are coarse (Table 4), and that subtle differences in contact area, attachment area, depth of attachment, and length of attachment cannot be resolved with these methods.
Columellar muscle attachment
The complexity and extent of the columellar muscle attachment has gone unrecognized because the attachment itself is remarkably delicate. A slight tug in the wrong direction (away from the aperture, toward the apex) tore the muscle from the columella, and the strength of the attachment deteriorated rapidly in preserved or relaxed animals. Its tenuous nature probably reflects the interplay between the physical mechanism of adhesion and the shape of the adhesive surface. Although the muscle was easily detached from the columella, the animal never naturally experiences a force pulling on the attachment from the angle or location I used during dissection; if the shell is opened as I have opened it, the animal is already too exposed to save itself from predators. An adhesive joint that can withstand large shear stresses will frequently fail when peeled (Portelli, 1986). The muscle attachment is analogous to a long piece of tape on a tabletop. When peeled backward, perpendicular to the table, the tape detaches easily, but when pulled along its length, it has great strength.
Surprisingly, none of the species studied here have muscle scars, even though scars are found in all major groups of shelled molluscs throughout their history (e.g., Abbott, 1974; Lindberg, 1985; Pojeta, 1985; Doguzhaeva and Mutvei, 1996; Isaji et al., 2002). In vertebrates, however, muscles frequently do not leave attachment scars (McGowan, 1982; Bryant and Seymour, 1990), especially when they insert directly into bone instead of attaching to a tendon which inserts into bone. In snails, the columellar muscle inserts into an epithelium that in turn inserts into the shell (Tompa and Watabe, 1976). Additional work is required to determine whether neogastropods and vertebrates lack muscle scars for similar reasons.
The fact that the muscle attachment is so much longer than previously thought (by authors such as Linsley, 1978; Morita, 1993; Thompson et al., 1998) has interesting implications for how the columellar muscle functions. Thompson et al. (1998) calculated, on theoretical considerations, the force required to buckle the columellar muscle and the amount of torsion the muscle could exert. The muscle, which has a crescentic cross section, buckled more easily and could not exert as much torsional force as a cylindrical muscle with a circular cross section. However, these authors assumed that the muscle was attached at only one end rather than throughout its length. The true, side-long attachment should help the muscle resist compressive forces (J. T. Thompson, St. Joseph's University, pers. comm.), so that the mechanical disadvantage due to buckling may not be so severe. Similarly, the net torsion exerted must be reconsidered in light of the new attachment data.
I hypothesized that folds guide the columellar muscle during protraction and retraction by protruding far into the columellar muscle, compelling the muscle to move along the folds. I reasoned further that, if folds act as struts, then they should protrude far enough into the muscle to significantly increase the amount of contact between the muscle and columella. For the species analyzed here, however, there was no significant difference in the contact area or length of attachment between species with folds and those lacking them. Therefore, the folds-as-struts hypothesis, as explained here, was not supported.
From another perspective, the methods were relatively coarse, and the data were poorly resolved. If these methods are applied to species with a subtle fold topology, then no significant increase in the contact area may be detectable. In species with folds, I compared the unadjusted contact area to the contact area after it had been adjusted with the fold modifier. The two metrics differed by more than 2% in only one specimen, and the average difference was only 0.2% (n = 17). This difference is less than the precision of the measurement of contact area, which is only to one decimal place. Therefore, although the topography of folds does not increase the contact area in the specimens considered here, the contact area may be greater in species with more prominent folds, such as those in the Volutidae, Mitridae, and Cancellariidae. Thus, additional work with these species and with methods providing higher resolution may lend support to the guidance hypothesis and its corollary that folds act as struts.
A consideration of the association between the area of contact and the presence of folds suggests other functional relationships. For example, if the advantage offered by strut-like folds were offset by the benefit of a large contact area, species with folds should have a significantly smaller area of contact than those without. Similarly, species with folds could have the same area of contact as species without folds, provided that the increase in contact due to the protruding folds was offset by a shorter attachment length. However, no such significant differences were observed.
The guidance hypothesis assumes that, without the resistance offered by folds, the muscle would slip along the columella during both retraction and protraction, presumably causing the animal to expend more energy. However, the arrangement of fibers within the muscle, including some fibers that are wound obliquely around the robust, apertural end of the muscle, suggests that the fibers, and not the columellar folds, control the path of the muscle when it contracts (Thompson et al., 1998). Because the muscle is attached along its top edge (Fig. 2), it will shift across the columella when the oblique fibers contract. In light of this newer evidence about the columellar muscle in particular and the muscular hydrostats of molluscs in general (Kier and Smith, 1985, 1990; Hodgson and Trueman, 1987; Kier, 1988; Marshall et al., 1989), the muscle seems to function in the way that was previously thought inefficient (Signor and Kat, 1984).
Signor and Kat (1984) formulated the guidance hypothesis in part because Signor (1982) correlated burrowing behavior in high-spired gastropods with columellar folds: 55 of 59 burrowing species had folds, but only I in 46 non-burrowing species did. He concluded that columellar folds guide the columellar muscle in burrowing animals (Signor and Kat, 1984). However, 40 of his 59 burrowers were in the Terebridae, and only 4 of his 11 families included non-burrowing species. Thus, his results may be explained by phylogenetic bias and should be reanalyzed with comparative methods based on phylogenetic contrasts (as in Harvey and Pagel, 1991) once the appropriate estimates of relationship are available. The advantage of folds to burrowing animals is not obvious, especially if the guidance hypothesis is not true. Furthermore, many species with folds do not burrow (G. J. Vermeij, University of California, Davis, pers. comm.). The species considered here cannot be used to explore the relationship between folds and burrowing behavior, because species were not sampled randomly across burrowing and non-burrowing habitats.
In conclusion, since the inner surface of the columellar muscle is an exact impression of the columellar folds, it is only reasonable to assume that the muscle moves along the folds. This assumption does not require, however, that the folds dictate the muscle's motion. I suspect that the similarity in the shape of the muscle and folds is due simply to their proximity, and that the direction the muscle moves is governed instead by attachment morphology and muscle fiber orientation.
As with contact area, the folds added insignificantly to the attachment area. The attachment was so long, and so much of it was distant from the folds, that the folds would need to protrude into the muscle six times more than they do (i.e., multiply the fold modifier by 6) to significantly increase attachment area in species with folds at the [alpha] < 0.05 level. If animals with folds are better able to maneuver their shells, it is not because they have a greater surface area of muscle attachment.
Signor and Kat (1984) suggested that the columellar muscle is divided by the folds into functionally discrete units joined only by connective tissue. However, judging by the observations presented here, the divisions they describe are probably part of a gradation between the robust, most apertural, part of the muscle and the weak, more apical pan (left and right sides of Fig. 2E-G). Since Signor and Kat (1984) did not mention the frequency or placement of their histological sections, nor illustrate their results, it is difficult to reevaluate their conclusions in the light of the newly recognized attachment morphology. The muscle histology of high-spired species with and without folds should be compared to determine whether the muscle is subdivided, and if so, whether those subdivisions are constrained by, of at least correspond to, columellar folds.
Maneuverability in a number of terrestrial pulmonates does appear to be enhanced by physically distinct subdivisions of the columellar muscle (Suvorov, 1993, 1999a, b, c). In these taxa, the columellar muscle originates from the most apical point (this is the only part of the muscle that is attached) and is divided into left and right pedal retractors, and left and right buccal mass retractors. These four branches continue to subdivide closer to the aperture. The four functional groups of the muscle are separated by a septum of connective tissue, but apertural teeth and columellar folds may playa secondary role in keeping subsets of branches separated. Thus, columellar ornamentation in pulmonates apparently evolved for a different reason than it did in neogastropods.
I was unable to substantiate Dall's (1894) claim that animals with folds retract deeper into their shells. Instead, animals lacking folds retract more deeply, because they have a significantly deeper attachment site. A larger sample of species is required to confirm this conclusion. Because all of the specimens from which quantitative data were obtained were collected in spring, seasonal variability in growth rate and attachment site were not considered. Variability in growth rate may be especially important to consider in genera such as Busycon, which exhibit highly episodic growth.
The depth of attachment was surprisingly constant among most species considered here (median depth = 295[degrees]; n = 36). Interestingly, the distribution of attachment depth was bimodal, with medians at 280[degrees] (n = 31) and 630[degrees] (n = 5) (Fig. 3), although, admittedly, there were few specimens in the higher mode. One species, Stramonita haemastoma, had specimens in both modes. This bimodality may reflect episodicity in growth.
Despite these overall similarities, the shallower attachment depth of species with folds implies that columellar folds do not help gastropods to escape from their predators by retracting into their shell. Moreover, my qualitative laboratory and field observations suggest that neogastropods are not subject to particularly intense predation. For example, a number of species (Leucozonia nassa, Stramonita haemastoma, S. rustica, Pisania tincta, and Melongena corona) neither retract quickly nor re-orient themselves quickly when their shells are overturned (pers. obs.). I have found wild specimens of Latirus mediamericanus (fasciolariid, with folds) lying on coral, each with the aperture pointed upward and the loot hanging outside the aperture.
Do folds have a single function?
Although the function of columellar folds remains unidentified, there are potentially fruitful paths for future research. As discussed above, the correlation between the presence of folds and burrowing habit in high-spired gastropods (Signor, 1982) must be studied in more detail. Also, columellar folds might strengthen the shell, thereby protecting the animal from predators. External features of the shell, such as thickness and the presence of spines, have been shown to increase resistance to predators, making it more difficult for a durophagous predator to break a snail's shell (reviewed in Vermeij, 1993; Kohn, 1999). In fact, some species have a corrugated shell, which presumably increases strength while minimizing the costs associated with building and moving a heavy shell (Vermeij, 1993). Perhaps, in a similar manner, columellar folds protect against predators by increasing the strength of the inner lip while minimizing the cost of thickening the entire columella. Supporting this idea, Hughes and Elner (1979) report that crabs open Nucella lapillus shells that have thin columellae by snapping the inner lip, breaking the shell in half. In contrast, N. lapillus individuals with thickened columellae are attacked at the apex of the shell. Both N. lapillus phenotypes lack folds, but these observations imply that strengthening the inner lip makes the columella harder to break more apically. However, predators of gastropods rarely break the inner lip. Most predators either crush the shell at its apex or peel back the shell al the outer lip (Vermeij, 1982; Johannesson, 1986); folds are simply ill-placed to affect either of these actions directly. There may be no evidence of damage on columella, as there are with failed attempts at predation in other parts of the shell, because when these attacks succeed, the shell fails catastrophically (G. J. Vermeij, pers. comm.).
Vermeij (1978) has observed that, within at least the families Vasidae and Mitridae, columellar folds are more common in tropical species, suggesting that the presence of folds might be correlated with latitude and increased predation intensity. This observation should certainly be tested quantitatively, although it is difficult to interpret the meaning of latitudinal diversity trends (Roy et al., 1998).
Columellar folds may not have a function. Still, convergence is considered to be some of the best evidence for adaptation (Raup and Gould, 1974; Harvey and Pagel, 1991; Larson and Losos, 1996), and columellar folds have evolved at least six times within different families of neogastropods (Price, 2001). Direct observations on how fold shape has evolved over time may reveal patterns of evolution that are consistent with adaptation. This approach would require a phylogenetic context (Harvey and Pagel, 1991; Larson and Losos, 1996), although there are currently no well-resolved phylogenies that include a sufficiently large number of species with and without folds to give power to such ah analysis. With the phylogenetic comparative method, it would be possible to determine whether folds evolved by "hitchhiking" along with demonstrably adaptive characters (Maynard Smith and Haigh, 1974).
On the other hand, folds may have evolved as a common solution to a number of problems, especially because the function of folds in pulmonates obviously differs from that in neogastropods. Functional experiments on species from a number of smaller clades that contain closely related species with and without folds should be conducted to identify functions unique to those smaller clades. If columellar folds serve different functions in different clades, then they might be an easy-to-evolve, flexible solution to a number of problems.
Columellar folds probably do not guide the columellar muscle. Rather, the motion of the muscle is likely determined by muscle fiber orientation and by the attachment to the shell, which is along the upper edge of the muscle. The geometry of the attachment is probably responsible for its adhesive strength, and the weak physical connection between muscle and shell is not. The methods employed here show no association between the presence of folds and the length of columellar muscle attachment, surface area of attachment, or depth of attachment. The widely observed similarity in morphology between the folds and the columellar muscle may be due simply to their physical juxtaposition rather than to any functional relationship, with folds having some other and presently unknown functions. Because folds have evolved multiple times, the most plausible explanation for their existence might be that they are an easy-to-evolve solution to a number of functional demands.
Measuring True Surface Area and Location on a Shell from a Series of Photographs
Measuring surface area
A photograph defines an XY-plane that contains an object (Appendix Fig. 1A), and the pixels within the object are "on," whereas those outside the object are "off." That object is a projection of a surface, Z, onto the XY-plane. The projected surface area, S[A.sub.z], is defined as
(A1) S[A.sub.z] = [[integral.sub.x] [[integral.sub.y] (1 + [([differential]z/[differential]x).sup.2] + [([differential]z/[differential]y).sup.2]) dxdy
(equation 6a in Thomas and Finney, 1984).
Because a digital photograph is pixelated, I approximated S[A.sub.z] by calculating the surface area of each pixel, i, then summing those values over all n pixels:
(A2) [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII],
where [A.sub.i] is the area of the pixel. Since the area of a pixel is 1, Equation A2 reduces to
(A3) [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII].
I found the partial derivative of Z with respect to x and the partial derivative of Z with respect to y by assuming that the object was a series of circles stacked on top of each other. Each row in the object corresponded to one circle, and all circles were centered about the Y-axis, which is also the coiling axis. Anyone familiar with the shape of neogastropods will recognize that the columella is somewhat asymmetrical. Imposing symmetry on the columella inflated true surface area, but this deviation was uniform across randomly sampled specimens with and without folds (28% inflation, st. dev. = 15%, n = 10).
Consider one row of pixels, i, of the photograph. The number of "on" pixels in that row equals the diameter of the circle, because the circle was projected straight onto that row. Thus, the circle's radius and origin were both known, the surface function, [z.sub.i], for a given row was
(A4) [x.sup.2.sub.i] + [z.sup.2.sub.i] = [r.sup.2.sub.i]
(Appendix Fig. 1B), and the partial derivative was
(A5) [differential][z.sub.p]/[differential][x.sub.p] = -[x.sub.p]/[square root of ([r.sup.2.sub.i] + [x.sup.2.sub.p)]
where p was any pixel in row i of the object.
The partial derivative of Z in the x-direction represented the distortion of the projection due to the curvature of the circle about the coiling axis. Therefore, a pixel located immediately on or above the coiling axis did not have any horizontal distortion, and the two pixels 90[degrees] from the coiling axis were the most severely distorted.
To calculate the partial derivative of Z with respect to y, I expressed the edge of the image as f(y) = r. Rewriting Equation A4 gives:
(A6) [x.sup.2.sub.i] + [y.sup.2.sub.i] = f[([y.sub.i]).sup.2]
where f(y) was found empirically by fitting a second-degree polynomial to the edge. The partial derivative [differentialz/[differential]y was evaluated from this polynomial.
The resulting area was measured in pixels.
Identifying a target region
A curved surface projects a 180[degrees] sector onto a row, so when a series contains photographs taken every 90[degrees] about a coiling axis, the photographs overlap. I eliminated overlap by using only the middle of each image (dashed lines in Appendix Fig. 1). This approach has the added benefit of using the region of the photograph with the best focus and least distortion.
One row of "on" pixels represented a circle projected onto its diameter. The coiling axis marked the midpoint of the diameter, and the end points of the row were 45[degrees] and -45[degrees] from the coiling axis. If we draw the circle, we can see that its radius is the hypotenuse of ah isosceles right triangle (Appendix Fig. 1B). The sides of this triangle equal the x-coordinate for the boundary of the target region.
Measuring degrees from aperture
I used the same circle to locate point [P.sub.i] relative to the aperture (Appendix Fig. 1), to calculate the edges of the attachment. In this case, I determined the X-coordinate of the point from the photograph, which is simply the distance between the coiling axis and [P.sub.i]. Here, the X-coordinate was known, but the triangle was not necessarily isosceles, so the angle, [theta] was not known. The angle that defined the are between the coiling axis and [P.sub.i] was calculated:
(A7) [theta] = asin(x/r)
If [P.sub.i] was apertural to the nearest landmark, I subtracted [theta] from the landmark's depth. Suppose, for example, that [P.sub.i] was depth of attachment, the curve f(y) in Appendix Figure I was coincident with the landmark at 270[degrees], and [theta] equals 20[degrees]. The value of attachment depth would be 290[degrees]. If [P.sub.i] were apical to the nearest landmark, then I would have added [theta] to the landmark's depth.
Table 1 Species examined Collection Species site * Family Busycon contrarium (Conrad, 1840) FS Melongenidae Busycon spiratum (Lamarck, 1816) FS Melongenidae Fasciolaria hunteria (Perry, 1811) FS, WFS, SM Fasciolariidae Fasciolaria tulipa (Linnaeus, 1758) HT Fasciolariidae Nassarius vibex (Say, 1822) FS, WFS Nassariidae Triplofusus giganteus (Kiener, 1840) HT Fasciolariidae Cantharus cancellarius (Conrad, 1846) ([dagger]) DIR Muricidae Chicoreus florifer distans (Adams, 1855) WFS Muricidae Melongena corona (Gmelin, 1791) FS, WFS Melongenidae Stramonita haemastoma (Linnaeus, 1767) WFS Muricidae Strombus alatus (Gmelin, 1791) P Strombidae Urosalpinx perrugata (Conrad, 1846) WFS, SM, ST Muricidae Columbella rusticoides (Heilprin, 1886) DIR Columbellidae Leucozonia nassa (Gmelin, 1791) S Fasciolariidae Opeatostoma pseudodon (Burrow, 1815) IV Fasciolariidae Pleuroploca salmo (Wood, 1928) B Fasciolariidae Terebra dislocata (Say, 1822) HT Terebridae Vasum muricatum (von Born, 1778) G Vasidae Cypraea cervus (Linnaeus, 1771) G Cypraeidae Oliva sayana (Ravenel, 1834) SM, HT Olividae Polystira nobilis (Hinds, 1843) GC Turridae Species Folds Museum ID Busycon contrarium (Conrad, 1840) Yes 299449, 299459 Busycon spiratum (Lamarck, 1816) Yes 299444, 299463, 299468, 299472 Fasciolaria hunteria (Perry, 1811) Yes 299450, 299492, 299493 Fasciolaria tulipa (Linnaeus, 1758) Yes 299448, 299456 Nassarius vibex (Say, 1822) Yes 299475, 299477 Triplofusus giganteus (Kiener, 1840) Yes 299441, 299442 Cantharus cancellarius (Conrad, 1846) ([dagger]) Yes 299486, 299487 Chicoreus florifer distans (Adams, 1855) No 299451, 299458 Melongena corona (Gmelin, 1791) No 299453, 299457 Stramonita haemastoma (Linnaeus, 1767) No 299452, 299454, 301941 Strombus alatus (Gmelin, 1791) No 301942, 301943 Urosalpinx perrugata (Conrad, 1846) No 299481, 299482, 299483, 299484, 299485 Columbella rusticoides (Heilprin, 1886) Yes 299473 299474 Leucozonia nassa (Gmelin, 1791) Yes 299506, 299520, 299521, 299522, 299526, 299527, 299530, 299531 Opeatostoma pseudodon (Burrow, 1815) Yes 299496 Pleuroploca salmo (Wood, 1928) Yes 299494 Terebra dislocata (Say, 1822) Yes 299488, 299489, 299490, 299491 Vasum muricatum (von Born, 1778) Yes 299500 Cypraea cervus (Linnaeus, 1771) No 299495 Oliva sayana (Ravenel, 1834) No 299460, 299461, 299466, 299469 Polystira nobilis (Hinds, 1843) No 299497, 299499 Species Data type Busycon contrarium (Conrad, 1840) Quantitaive Busycon spiratum (Lamarck, 1816) Quantitaive Fasciolaria hunteria (Perry, 1811) Quantitaive Fasciolaria tulipa (Linnaeus, 1758) Quantitaive Nassarius vibex (Say, 1822) Quantitaive Triplofusus giganteus (Kiener, 1840) Quantitaive Cantharus cancellarius (Conrad, 1846) ([dagger]) Quantitaive Chicoreus florifer distans (Adams, 1855) Quantitaive Melongena corona (Gmelin, 1791) Quantitaive Stramonita haemastoma (Linnaeus, 1767) Quantitaive Strombus alatus (Gmelin, 1791) Quantitaive Urosalpinx perrugata (Conrad, 1846) Quantitaive Columbella rusticoides (Heilprin, 1886) Qualitative Leucozonia nassa (Gmelin, 1791) Qualitative Opeatostoma pseudodon (Burrow, 1815) Qualitative Pleuroploca salmo (Wood, 1928) Qualitative Terebra dislocata (Say, 1822) Qualitative Vasum muricatum (von Born, 1778) Qualitative Cypraea cervus (Linnaeus, 1771) Qualitative Oliva sayana (Ravenel, 1834) Qualitative ([double dagger]) Polystira nobilis (Hinds, 1843) Qualitative * Collection sites: B, Bique, Panama (Pacific Ocean); DIR, Dog Island Reef, Florida (Gulf of Mexico); FS. Florida State University Marine Lab, Turkey Bayou, Florida (Gulf of Mexico); G, Galeta, Panama (Caribbean Sea); GC, Golfo de Chiriqui. Panama (Pacific Ocean); HT, Hammock Trail, near St. Joseph Bay, Gulf County, Florida (Gulf of Mexico); IV, Isla Venado near Playa Veracruz, Panama (Pacific Ocean); P, Purchased from Gulf Specimen Aquarium and Marine Biological Supply, Panacea, Florida; S, Sebastian, Florida (Indian River County); SM, St. Mark's Wildlife Refuge, Florida (Gulf of Mexico); ST, Beach at St. Teresa, Florida (Gulf of Mexico); WFS, West side of Florida State University Marine Lab on oyster bar. ([dagger]) Tentatively placed in Soleneistra by Vermeij (2001b). ([double dagger]) Only the attachment depth was measured. Table 2 Fold morphology in species examined Species Fold morphology Busycon contrarium 1 subtle fold at the bottom of the whorl, distinguished by a groove and angled obliquely; difficult to observe at aperture, but more prominent in older whorls Busycon spiratum As in B. contrarium, but slightly more defined Cantharus cancellarius 1 fold at the bottom of the whorl, angled obliquely; broader than in other species Columbella rustticoides 1 fold immediately at the bottom of the whorl Fasciolaria hunteria 2 folds al the bottom of the whorl, angled obliquely; the lower edge of the bottom fold coincides with the edge of the columella Fasciolaria tulipa As in F. hunteria, but with 3 folds Leucozonia nassa 3 folds, angled obliquely and closely spaced Nassarius vibex 1 well-defined fold at the bottom of the whorl, angled obliquely; square, rather than rounded, profile Opeatostoma As in L. nasssa pseudodon Pleuroploca salmo Terebra dislocata 2 large, broad folds spread throughout whorl; the bottom fold is more prominent than the top one Triplofusus giganteus As in F. tulipa, but top fold is more subtle than the others Vasum muricatum 5 folds in "1 prominent--1 weak--1 prominent--weak--1 prominent" pattern; folds angled more perpendicular to coiling axis than in any of the other species and spread throughout the bottom two-thirds of the whorl Table 3 Summary of measurements required to test hypotheses Use modifier to adjust for fold Measurement Hypothesis topography? Standardized total area of muscle Maneuverability Yes physically attached to the columella (ATT/CA in Fig. 1) Standardized surface area of Guidance Yes contact between columella and columellar muscle throughout attachment when animal is relaxed (CM/CA in Fig. 1) Depth of attachment, in degrees Retraction depth No Length of attachment, in degrees Maneuverability No Table 4 Measurements for all specimens Standardized attachment area (x Species Museum ID Folds [10.sup.-3]) Busycon contrarium 299449 Yes 3.0 Busycon contrarium 299459 Yes 2.7 Busycon spiratum 299444 Yes 2.2 Busycon spiratum 299463 Yes 1.8 Busycon spiratum 299468 Yes 2.3 Busycon spiratum 299472 Yes 2.4 Cantharus cancellarius 299486 Yes 3.6 Cantharus cancellarius 299487 Yes 3.4 Fasciolaria hunteria 299450 Yes 2.5 Fasciolaria hunteria 299492 Yes 2.4 Fasciolaria hunteria 299493 Yes 2.4 Fasciolaria tulipa 299448 Yes 2.5 Fasciolaria tulipa 299456 Yes 2.7 Nassarius vibex 299475 Yes 1.9 Nassarius vibex 299477 Yes 4.6 Triplofusus giganteus 299441 Yes 3.9 Triplofusus giganteus 299442 Yes 4.7 Chicoreus florifer distans 299451 No 3.1 Chicoreus florifer distans 299458 No 3.1 Melongena corona 299453 No 2.7 Melongena corona 299457 No 2.3 Oliva sayana 299460 No ND Oliva sayana 299461 No ND Oliva sayana 299465 No ND Oliva sayana 299466 No ND Oliva sayana 299469 No ND Stramonita haemastoma 299452 No 2.3 Stramonita haemastoma 299454 No 2.2 Stramonita haemastoma 301941 No 3.0 Strombus alatus 301942 No 2.4 Strombus alatus 301943 No 2.6 Urosalpinx perrugata 299481 No 1.2 Urosalpinx perrugata 299482 No 4.7 Urosalpinx perrugata 299483 No 3.4 Urosalpinx perrugata 299484 No 3.5 Urosalpinx perrugata 299485 No 5.0 Depth of Length of Standardized attachment attachment Species contact area (degrees) (degrees) Busycon contrarium 0.5 210 330 Busycon contrarium 0.5 240 330 Busycon spiratum 0.4 280 230 Busycon spiratum 0.3 270 290 Busycon spiratum 0.4 270 450 Busycon spiratum 0.4 250 270 Cantharus cancellarius 0.5 350 330 Cantharus cancellarius 0.3 360 230 Fasciolaria hunteria 0.5 310 290 Fasciolaria hunteria 0.5 280 370 Fasciolaria hunteria 0.5 260 390 Fasciolaria tulipa 0.6 260 390 Fasciolaria tulipa 0.5 230 420 Nassarius vibex 0.5 630 250 Nassarius vibex 0.4 570 240 Triplofusus giganteus 0.7 290 360 Triplofusus giganteus 0.8 280 370 Chicoreus florifer distans 0.4 270 190 Chicoreus florifer distans 0.4 330 260 Melongena corona 0.6 270 460 Melongena corona 0.5 320 400 Oliva sayana ND 280 ND Oliva sayana ND 260 ND Oliva sayana ND 370 ND Oliva sayana ND 300 ND Oliva sayana ND 290 ND Stramonita haemastoma 0.4 320 370 Stramonita haemastoma 0.4 280 350 Stramonita haemastoma 0.4 660 90 Strombus alatus 0.2 590 210 Strombus alatus 0.2 650 170 Urosalpinx perrugata 0.4 310 300 Urosalpinx perrugata 0.5 330 330 Urosalpinx perrugata 0.3 360 320 Urosalpinx perrugata 0.6 420 170 Urosalpinx perrugata 0.5 360 310 ND--not determined. Measurements could not be taken because the columella is too delicate to survive dissection.
I thank Dan Reuman, Moon Duchin, and Chris Degni for generously devoting their time to help develop the algorithm to reconstruct the 3-D surface of the shell. Jason Goodman and Gidon Eshel helped debug the programs that implemented the algorithm. Deirdre Gonsalves-Jackson, Greg Farley, Cheryl Swanson, Jessica Cande, the Smithsonian Marine Station, and the Florida State University Marine Lab helped with field collections. Jochen Gerber, Janeen Jones, and Martin Pryzdia at the Field Museum of Natural History helped deposit specimens. Additional thanks to Michael LaBarbera, David Jablonski, Rudiger Bieler, Susan Kidwell, Peter Wagner, and colleagues at the University of Chicago for support throughout this research and helpful comments on the manuscript. Geerat J. Vermeij, two anonymous reviewers, and especially Michael J. Green berg provided helpful suggestions that greatly improved this paper. This material is based upon work supported by the National Science Foundation under Grant No. 0073248. NSF grant 9903030 to David Jablonski, the Conchologists of America, the Link Foundation and Smithsonian Marine Station, and the University of Chicago Hinds and Gurley Funds provided additional support.
Abbott, R. T. 1974. American Seashells, 2nd ed. Van Nostrand Reinhold, New York.
Appleton, R. D., and A. R. Palmer. 1988. Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proc. Natl. Acad. Sci. USA 85: 4387-4391.
Bertness, M. D., and C. Cunningham. 1981. Crab shell-crushing predation and gastropod architectural defense. J. Exp. Mar. Biol. Ecol. 50: 213-230.
Bryant, H. N., and K. L. Seymour. 1990. Observations and comments on the reliability of muscle reconstruction in fossil vertebrates. J. Morphol. 206: 109-117.
Carefoot, T. H., and D. A. Donovan. 1995. Functional significance of varices in the muricid gastropod Ceratostoma foliatum. Biol. Bull. 189: 59-68.
Dall, W. H. 1894. The mechanical cause of folds in the aperture of the shell of Gastropoda. Am. Nat. 28: 909-914.
Doguzhaeva, L., and H. Mutvei. 1996. Attachment of the body to the shell in ammonoids. Pp. 43-63 in Ammonoid Paleobiology, N. H. Landman, K. Tanabe, and R. A. Davis, eds. Plenum Press, New York.
Donovan, D. A., J. P. Danko, and T. H. Carefoot. 1999. Functional significance of shell sculpture in gastropod molluscs: test of a predator-deterrent hypothesis in Ceratostoma foliatum (Gmelin). J. Exp. Mar. Biol. Ecol. 236: 235-251.
Fretter, V., and A. Graham. 1962. British Prosobranch Molluscs: Their Functional Anatomy and Ecology, 1st ed. Ray Society, London.
Fretter, V., and A, Graham. 1994. British Prosobranch Molluscs: Their Functional Anatomy and Ecology, 2nd ed. Ray Society, London.
Harasewych, M. G., and R. E. Petit. 1989. The nomenclatural status and phylogenetic affinities of Syrinx aruanus Linn, 1758 (Prosobranchia: Turbinellidae). Nautilus 103: 83-84.
Harvey, P. H., and M. D. Pagel. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, New York.
Hodgson, A. N., and E. R. Trueman. 1987. The siphons of Scrobicularia plana (Bivalvia; Tellinacea). Observations on movement and extension. 3. Zool. 194: 445-459.
Hughes, R. N., and R. W. Elner. 1979. Tactics of a predator, Carcinus maenas, and morphological responses of the prey, Nucella lapillus. J. Anim. Ecol. 48: 65-78.
Isaji, S., T. Kase, K. Tanabe, and K. Uchiyama. 2002. Ultrastructure of muscle-shell attachment in Nautilus pompilius Linnaeus (Mollusca: Cephalopoda). Veliger 45: 316-330.
Johannesson, B. 1986. Shell morphology of Littorina saxatilis Olivi: the relative importance of physical factors and predation. J. Exp. Mar. Biol. Ecol. 102: 183-196.
Kier, W. M. 1988. The arrangement and function of molluscan muscle. Pp. 211-252 in Form and Function. E. R. Trueman and M. R. Clarke, eds. Academic Press, New York.
Kier, W. M., and A. M. Smith. 1990. The morphology and mechanics of octopus suckers. Biol. Bull. 178: 126-136.
Kier, W. M., and K. K. Smith. 1985. Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats. J. Linn. Soc. Lond. Zool. 83: 307-324.
Kohn, A. J. 1999. Anti-predatory defences of shelled gastropods. Pp. 169 181 in Functional Morphology of the Invertebrate Skeleton, E. Savazzi, ed. Wiley and Sons, New York.
Larson, A., and J. B. Losos. 1996. Phylogenetic systematics of adaptation. Pp. 187-220 in Adaptation, M. R. Rose and G. V. Lauder, eds. Academic Press, New York.
Lindberg, D. R. 1985. Aplacophorans, monoplacophorans, polyplacophorans, scaphopods: the lesser classes. Pp. 230-247 in Mollusks: Notes for a Short Course, D. J. Bottjer, C. S. Hickman, and P. D. Ward, eds. The University of Tennessee, Knoxville.
Linsley, R. M. 1978. Shell form and the evolution of gastropods. Am. Nat. 66: 432-441.
Marko, P. B., and A. IL Palmer. 1991. Responses of a rocky shore gastropod to the effluents of predatory and non-predatory crabs: avoidance and attraction. Biol. Bull. 181: 363-370.
Marshall, D. J., A. N. Hodgson, and E. R. Trueman. 1989. The muscular hydrostat of a limpet tentacle. J. Molluscan Stud. 55: 421-422.
Maynard Smith, J., and J. Haigh. 1974. The hitch-hiking effect of a favourable gene. Genet. Res. 23: 23-35.
McGowan, C. 1982. The wing musculature of the brown kiwi Apteryx australis Mantelli and its bearing on ratite affinities. J. Zool. 197: 173-219.
Morita, R. 1993. Development mechanics of retractor muscles and the "Dead Spiral Model" in gastropod shell morphogenesis. Neues. Jahrb. Geol. Palaeontol. Abh. 190: 191-217.
Morton, J. E. 1967. Molluscs. Hutchinson University Library, London.
Palmer, A. R. 1977. Function of shell sculpture in marine gastropods: hydrodynamic destabilization in Ceratostoma foliatum. Science 197: 1293-1295.
Palmer, A. R. 1979. Fish predation and the evolution of gastropod shell sculpture--experimental and geographic evidence. Evolution 33: 697-719.
Paul, C. R. C. 1991. The functional morphology of gastropod apertures. Pp. 127-140 in Constructional Morphology and Evolution, N. Schmidt-Kittler and K. Vogel, eds. Springer-Verlag, Berlin.
Pojeta, J., Jr. 1985. Early evolutionary history of diasome mollusks. Pp. 102-121 in Mollusks: Notes for a Short Course, D. J. Bottjer, C. S. Hickman, and P. D. Ward, eds. The University of Tennessee, Knoxville.
Ponder, W. F. 1972. The morphology of some mitriform gastropods with special reference to their alimentary and reproductive systems (Neogastropoda). Malacologia 11: 295-342.
Portelli, G. B. 1986. Testing, analysis, and design of structural adhesive joints. Pp. 447-449 in Structural Adhesives: Chemistry and Technology, S. R. Hartshorn, ed. Plenum Press, New York.
Price, R. M. 2001. Using constructional data to detect convergence: an underutilized approach to studying adaptation in the fossil record. Paleobios 21: 105-106.
Raup, D. M, and S. J. Gould. 1974. Stochastic simulation and evolution of morphology--towards a nomothetic paleontology. Syst. Zool. 23: 305-322.
Roy, K., D. Jablonski, J. W. Valentine, and G. Rosenberg. 1998. Marine latitudinal diversity gradients: tests of causal hypotheses. Proc. Natl. Acad Sci. USA 95: 3699-3702.
Signor, P. W., III. 1982. Resolution of life habits using multiple morphologic criteria: shell form and life-mode in turritelliform gastropods. Paleobiology 8: 378-388.
Signor, P. W., III, and P. W. Kat. 1984. Functional significance of columellar folds in turritelliform gastropods. J. Paleontol. 58: 210-216.
Suvorov, A. N. 1993. Some aspects of functional morphology of the aperture in the Pupillina suborder (Gastropoda Pulmonata). Ruthenica 3: 141-152.
Suvorov, A. N. 1999a. The conflict between operative and conservative subsystems of organism in the evolution of terrestrial snails (Sylommatophora, Pulmonata). Russ. J. Zool. 3: 401-409.
Suvorov, A. N. 1999b. Functional interrelations between aperture structures and soft organs in lower Geophila: 1. Pupillina, Oleacinina. Russ. J. Zool. 3: 5-15.
Suvorov, A. N. 1999e. Some mechanisms of adaptation to the wet microhabitats in higher Geophila (Mollusca, Pulmonata). J. Gen. Biol. (Moscow) 60: 177-188.
Taylor, J. D., N. J. Morris, and C. N. Taylor. 1980. Food specialization and the evolution of predatory prosobranch gastropods. Palaeontology 23: 375-409.
Thomas, G. B., Jr., and R. L. Finney. 1984. Calculus and Analytical Geometry, 6th ed. Addison-Wesley, Reading, MA.
Thompson, J. T., A. D. Lowe, and W. M. Kier. 1998. The columellar muscle of prosobranch gastropods: morphological zonation and its functional implications, Invertebr. Biol. 117: 45-56.
Tompa, A. S., and N. Watabe. 1976. Ultrastructural investigation of the mechanism of muscle attachment to the gastropod shell. J. Morphol. 149: 339-352.
Vermeij, G. J. 1978. Biogeography and Adaptation: Patterns of Marine Life. Harvard University Press, Cambridge, MA.
Vermeij, G. J. 1982. Gastropod shell form, breakage, and repair in relation to predation by the crab Calappa. Malacologia 23: 1-12.
Vermeij, G. J. 1987. Evolution and Escalation: ah Ecological History of Life. Princeton University Press, Princeton, NJ.
Vermeij, G. J. 1993. A Natural History of Shells. Princeton University Press, Princeton, NJ.
Vermeij, G. J. 2001a. Innovation and evolution at the edge: origins and fates of gastropods with a labral tooth. Biol. J. Linn. Soc. 72: 461-508.
Vermeij, G. J. 2001b. Taxonomy, distribution, and characters of Pre Oligocene members of the Cantharus group of Pisaniinae (Neogastropoda: Buccinoidea). J. Paleontol. 75: 295-309.
Vermeij, G. J., and P. W. Signor. 1992. The geographic, taxonomic, and temporal distribution of determinate growth in marine gastropods. Biol. J. Linn. Soc. 47: 233-247.
Voltzow, J. 1990. The functional morphology of the pedal musculature of the marine gastropods Busycon contrarium and Haliotis kamtschatkana. Veliger 33: 1-19.
West, K., A. Cohen, and M. Baron. 1991. Morphology and behavior of crabs and gastropods from Lake Tanganyika, Africa--implications for lacustrine predator-prey coevolution. Evolution 45: 589-607.
REBECCA M. PRICE
Department of Geophysical Sciences, University of Chicago, 5734 S. Ellis Ave., Chicago, Illinois 60637
Received 22 October 2002; accepted 29 August 2003.
|Printer friendly Cite/link Email Feedback|
|Author:||Price, Rebecca M.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2003|
|Previous Article:||Localization of a symbiosis-related protein, sym32, in the Anthopleura elegantissima--Symbiodinium muscatinei association.|
|Next Article:||Response in nematocyst uptake by the nudibranch Flabellina verrucosa to the presence of various predators in the Southern Gulf of Maine.|