ACTAUNIVERSITATISUPSALIENSISUPPSALA2006

Digital Comprehensive Summaries of Uppsala Dissertationsfrom the Faculty of Science and Technology 257

Functional Morphology ofGastropods and Bivalves

JENNY SÄLGEBACK

ISSN 1651-6214ISBN 91-554-6764-4urn:nbn:se:uu:diva-7424

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List of papers

I Savazzi, E. and Sälgeback, J. 2004. A comparison of morphological adaptations in the cardiid bivalves Cardium and Budmania. Paleontological Research 8, 221-239.

II Sälgeback, J. and Savazzi, E. 2006. Constructional morphology of cerithiform gastropods. Paleontological Research 10, 233-259.

III Sälgeback, J. (In progress). Shell strength and breakage patterns in the intertidal snail Nucella lamellosa. Biological Bulletin.

Reproduction of papers I and II was made with permission of the copyright holder.

Paper I © 2004 The Palaeontological Society of Japan Paper II © 2006 The Palaeontological Society of Japan Paper III © by the author

Statement of authorship Paper I: Jenny Sälgeback was deeply involved in the studies of the cardiid material and performed the measurements and analyses for the weight versus volume in vivo comparison. Enrico Savazzi studied the lymnocardiid material. Shared writing. Paper II: Jenny Sälgeback participated in the fieldwork in Japan in 2003 and 2004 and was involved in all experiments performed between 2001-2006. Enrico Savazzi studied the repository material in London, Paris and Italy. Shared writing. Paper III: Michael LaBarbera wrote the methodology section about the tensometer and performed the permutation analyses and part of the ANCOVA analyses.

Contents

Introduction.....................................................................................................9Aims of this study ....................................................................................10

Living with a shell ........................................................................................12Function of the shell .................................................................................12Shell sculpture ..........................................................................................12

Shell strength .......................................................................................13Adaptations to habitat ..........................................................................15

The papers in this study ................................................................................21Paper I ......................................................................................................21Paper II .....................................................................................................22Paper III....................................................................................................23

Svensk sammanfattning ................................................................................24

Acknowledgements.......................................................................................27

References.....................................................................................................29

9

Introduction

The general definition of functional morphology is “The study of the relationship between form and function of organisms and/or their parts”, (Savazzi, 1999). The general definition however, breaks down between palaeontologists and biologists who have differing opinions concerning which methods are valid to use. Biologists often regard direct observation of the organism as the only valid method to evaluate adaptive significance; the function has to be seen in action. This is not possible in the study of fossils where inferential methods have to be used. Confining studies to direct observations excludes some important aspects whereas the fossil record offers a possibility to study a broad range of morphologies through time to observe evolutionary trends. It is in the fossil record that morphological adaptation is especially evident. Inferential methods can also be used with available extant specimens. Direct observations can then be used to verify the results and methods can be refined. Biologists often study the soft parts of molluscs, while palaeontologists are confined to the shell for interpretations.

To make a comprehensive analysis of the causal origins of any organic structure an integration of different types of studies is needed, (see references in Thomas, 1988). Constructional morphology was developed by Seilacher (1970) for this purpose, as a broader attempt to explain morphology than provided by studies restricted to a single species. Constructional morphology is probably the working method followed by most palaeobiologists dealing with questions on form and function. Its aim is to place functional morphology in an evolutionary context, (Savazzi, 1999). The form of an organism is explained as the interplay between three factors/aspects; (1), the phylogenetic or evolutionary heritage, (2), its constructional (developmental and morphogenetic) mechanisms, and (3), its functional morphology, (Fig. 1A). This method provides a conceptual framework for the analysis of form, (Savazzi, 1999). It has been expanded by Seilacher, (1991, 1993), and developed into biomorphodynamics, by adding the aspect of the effective environment involving all effects on morphology, growth and evolution caused by the environment that immediately surrounds the organism, (Fig. 1B).

One of the advantages with constructional morphology is that it can be applied simultaneously to whole lineages. When using functional analysis by itself, it is usually only possible to study adaptive strategies at the species

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level. In constructional morphology, however, it is often unsatisfactory to study a single species, and the best results are accomplished by analyzing several species simultaneously, as this facilitates the understanding of their phylogenetic heritage and Bauplan (“The basic set of characters and adaptations that constitute the common background of a group, but that need not be expressed in all its members.” Savazzi, 1999).

Figure 1. The working methods of constructional morphology (A) and biomorphodynamics (B). Each corner represents one aspect that affects the form of an organism. (After Savazzi, 1999 and Seilacher, 1991)

Aims of this study In this project the principles of constructional morphology (sensu Seilacher 1970) have been used to study morphological adaptations of the shell in some post-Paleozoic gastropods and bivalves. Special attention has been given to relationships between morphology and mode of life.

The adaptive features of gastropods have not been widely studied even though they are among the most common shell-bearing invertebrates in shallow-water environments. Bivalves have been much more thoroughly studied in functional terms. However, bivalves do not exhibit the behavioral complexity observed in gastropods. Shell geometry, sculptures and pigmentation are much more varied in gastropods, and as a consequence, are more difficult to interpret in adaptive terms (Signor, 1982b). Life habits in marine bivalves appear to be consistently predictable from shell form, (Stanley, 1970, 1972, 1975, 1977).

For this study field observations on recent organisms were performed when possible, allowing the possibility to see how different shell characteristics are used in the animal’s natural habitat, thus facilitating the

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interpretation of similar characters in fossil forms. Further it includes studies of fossil and recent material in museum collections and some laboratory experimentation.

Evaluation of the taxonomic position of gastropods and bivalves studied herein has not been part of this project. All discussions are based on existing taxonomy.

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Living with a shell

Function of the shell In both gastropods and bivalves, the shell provides protection for the vulnerable soft parts. Kohn (1999) stated that “A snail’s shell is its castle” and with this in mind it is easy to understand that the shell is of major importance to the survival of a gastropod. The primary function, and reason for the evolution of the gastropod shell, is thought to be protection from predators (Vermeij, 1977a, 1993; Bengtsson, 1994). Most gastropods are helically coiled and consist of several whorls. In the large majority of species, each whorl is cemented onto and partly overlaps the preceding whorl, (e.g. Savazzi and Sasaki, 2004).

The bivalve shell is the simplest possible lever skeleton, consisting of two valves, rigid enough to provide skeletal support and protection, which are free to rotate about a hinge axis. Valves are closed by adductor muscles and opened by a spring-like elastic ligament (Thomas, 1988). Both bivalves and gastropods grow by marginal accretion.

The shells of gastropods and bivalves provide additional functions, e.g., mechanical support of soft parts, protection against hostile environmental conditions, a variety of functions in connection with locomotion or other behaviour and a gill-chamber for filter feeding. In bivalves, the shell provides carbonate as a pH-buffer to neutralize acidic by-products of anaerobic metabolism when the shell needs to remain sealed (Thomas, 1988). The above functions are not mutually exclusive. Most often, morphologic characters of the shell can be related to concurrent functions, although sometimes a primary function can be identified due to a high degree of morphologic specialization.

Shell sculpture Apart from the basic functions of shell-morphology mentioned above, there is also a range of functional features occurring within the shell. These features are often adaptive in relation to habitat, locomotion, feeding and defence from predators (e.g. Vermeij 1977b, 1993; Signor 1982a, 1982b; Palmer 1985; Savazzi 1989, 1991a, 1994; Kohn 1999). Two main aspects of the gastropod/bivalve shell will be discussed below. However, a specific

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character can function in several different ways and it is difficult to make a strict division. There is reason for caution when making interpretations of morphological features, as the presence or absence of a character might be misleading. The whole organism should be regarded as a complete adaptive unit.

Shell strength Gastropods and bivalves usually invest a lot of energy in specializing and strengthening the shell. It is necessary to have a strong and sturdy shell to meet the demands imposed on the organism by the surrounding environment. For instance, gastropods or bivalves living in a high-energy environment may be subject to tumbling by waves and water currents. Predation is another factor controlling shell strength (e.g. Vermeij, 1977b). A range of shell-crushing, peeling and boring predators (e.g. crustaceans, fish, and gastropods) lives in most environments. Carrying a large and thick shell is in most cases a good defence against predators. The size-relationship between predator and prey can be crucial for the outcome of their encounter, i.e. whether the attack is successful or not, (Zipser and Vermeij, 1978). In the case of an unsuccessful attack gastropods are often able to repair the shell. This will result in a scar telling the story of the encounter (Fig. 2A-D). Bivalves have comparable repair capabilities (Savazzi, pers. comm.).

Figure 2. Examples of gastropod shells with scars after unsuccessful predatory attacks supposedly by crabs. A. Rhinoclavis vertagus (Recent, Iriomote island, Japan). B. Diastoma costellatum (Middle Eocene, Grignon, Paris Basin, France). C-D. Nucella lamellosa (Recent, San Juan Island, USA). Scale bars represent 10mm.

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Above a given predator-size ratio, with increasing shell-size of the prey, the success-rate of attack decreases and handling time prior to shell breakage increases, (Kohn, 1999; Vermeij, 1987). A way for the organism to increase its size is to add projecting sculptures, e.g. spines or knobs. Shell thickness together with large size are common defensive features in shell-bearing gastropods (Preston et al., 1996; Vermeij, 1987). The thicker the shell, the more difficult it is to crush or bore.

Addition of sculpture to the external shell surface is a common way of increasing shell strength in both gastropods and bivalves (e.g. Vermeij, 1993). Spines, knobs, ribs and keels of different shapes and sizes are commonly found in both groups (Fig. 3A-D, 4A-G). Spines are often used as protection against predators (e.g. Palmer, 1979). They can be placed in different areas of the shell. Spines around the siphonal gape in shallowly buried bivalves protect the delicate siphons against fish nibbling on them (Vlas, 1979) (Fig. 3A-B). Spines can also be functional in preventing scour by keeping sediment from being transported away and leaving the shell exposed, (Savazzi, 1985).

Figure 3. Shell sculpture in cardiid bivalves. A-B. Cardium hians (Recent, Algeria) possess radial ribs and posterial spines. The latter protect the siphons, reduce scour and add strength. C. C. costatum (Recent, Mbour, Senegal) has keels on top of the radial ribs. D. The Lymnocardiine Budmania semseyi (Miocene, Köningsgnad, Rumania) possess prominent keels, probably used for anchoring the shell in the sediment. Scale bars represent 10mm in A-C and 20mm in D.

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Knobs or corrugations on the external surface of either bivalves or gastropods increase the strength of the shell by making it stiffer and thereby more resistant to different kinds of deformation, especially compression (Vermeij, 1993), (Fig. 4A-B). Ribs and keels provide a comparable increase in rigidity of the shell (Fig. 3A-C). Radial ribs are a very common sculptural trait in bivalves, (Savazzi, 1985). The construction of these structures follow basic engineering principles, where increased stiffness of a plate is achieved by adding rib-like structures perpendicular to the plate, folding the plate into an undulating, corrugated structure or by placing a folded plate sandwiched between two surfaces (as in corrugated cardboard). All of the above increases the distance between the inner and outer surfaces.

Sculptural elements in gastropods may sometimes be synchronized (Savazzi and Sasaki, 2004) (Fig. 4E). Supposedly they play a dual role in providing mechanical stiffening and adding stability to the shell by preventing it from being overturned. Varices, swellings of the shell, are present in some gastropod species. The presence of a varix increases the strength of the shell at this location by making the shell thicker and effectively larger (Vermeij, 1982). A predator might be able to peel the shell up until this point but possibly not further (Vermeij, 1982).

Strengthening of vulnerable areas of the shell can be achieved by non-uniform shell-thickening (Kohn, 1999). In gastropods thickening of the outer lip is common (Fig. 4A-B, 5B, D, F), (e.g. Paul, 1991; Kohn, 1999). A thick outer lip acts as a first line of defence against predators trying to gain access to the soft parts, (Vermeij, 1987). Adding an apertural barrier, often in the shape of teeth, further reinforces the outer lip, (Fig. 5B), (Kohn, 1999). In addition to adding strength, apertural barriers also make the entrance narrower and less accessible for predators. They serve primarily to resist peeling as they hinder the positioning of a peeling organ, (Stanley, 1988). Other internal sculptural elements in gastropods include barriers, which increase shell strength at various locations of the shell interior, (Fig. 5E), and spiral ridges on the columella, called columellar folds (Fig. 5E). Several authors have hypothesised about the function of columellar folds (e.g. Signor and Kat, 1984) but as yet there is no general agreement on their function (see review in Price, 2003).

Adaptations to habitat Adaptations specific to the habitat of the gastropod or bivalve are often reflected in the shell. Factors like predation pressure, substrate, grain size, turbidity, behaviour, etc. have an effect on the morphology of the shell.

As described above, a thick shell is usually a good defence against predators, but this is not always feasible because of the demands imposed by the inhabited environment. An animal living in soft sediments with a low density, (specific gravity), may sink if its own bulk density exceeds that of

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Figure 4. Examples of shell sculptures in cerithiform gastropods. Arrows indicate stabilizing varices. A, C. Cerithium nodulosum (Recent, Indo-Pacific). Strong knobs and stabilizing ventrolateral varix. B, D. Rhinoclavis sinensis (Recent, Iriomote island, Japan). Beaded appearance and stabilizing ventrolateral varix. E. Pyrazus pentagonatus (Middle Eocene, Roncá, Italy) with synchronized sculpture. F. Ventrolateral and dorsal varices in Clypeomorous bifasciata (Recent, Iriomote island, Japan). G. Ventrolateral and dorsolateral varices in C. petrosa (Recent, Iriomote island, Japan). Scale bars represent 10mm.

the sediment, i.e., it cannot apply more stress than the sediment is able to bear if it wants to stay afloat (Thayer, 1975). Since sinking below the sediment surface is detrimental to suspension-feeding animals (i.e. most bivalves), it is important for the organism to use the appropriate adaptations. In these conditions, having a large and heavy shell is no longer an advantage. Instead, the secretion of a thin shell, resulting in a lower specific gravity of the organism close, or equal to, that of the sediment is preferable since this allows the animal to float within the topmost layer of the sediment (Thayer, 1975). Another adaptation to life on or near the surface of a weak substrate, is to increase the surface area carrying the weight of the organism, (the so called “footprint”), relative to the mass or volume of the organism. This is best described as a “snow-shoe effect” (Thayer, 1975).

To increase the “footprint” of the shell some gastropods have a large flaring lip, (e.g. strombids and cerithiforms, Savazzi, 1991b; Salgeback and Savazzi, 2006), or long projecting spines, (e.g. strombids, Savazzi, 1991b). A flared lip shelters the extended soft parts against predators when the gastropod is epifaunal. Spines increase the “footprint” without adding too much material that would make the shell unnecessarily heavy. The broad “footprint” provided by a flared lip or spines also makes accidental overturning of the shell less likely (Savazzi, 1991b).

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Figure 5. A-B. Nucella lamellosa (Recent, San Juan Island, USA). Subadult (A) before thickening of the outer lip. Adult (B) with thickened outer lip and apertural teeth. C-D. Terebralia palustris (Recent, Iriomote island, Japan). Subadult (C) without thickened outer lip. Adult (D) with flared thickened outer lip as a result of determinate growth. Short arrow points to ventrolateral varix. E. Tangential section through adult T. palustris showing internal barriers and the columellar fold. F-G. T. sulcata (Recent, Tayud, Cebu island, the Philippines) with clamping, tangential aperure. Short arrow points to ventrolateral varix. Scale bars represent 10mm.

Shelled organisms living in fluid sediments typically possess an inconspicuous sculpture, reducing the bulk density of the organism (a smooth shell weigh less than a ribbed one of the same size). The elimination of sculpture is possible in quiet, soft-bottom environments, where it is not needed to strengthen the shell (Thayer, 1975). However, if the organism lives in a high-energy environment, “snow-shoes” consisting of prominent sculptures (e.g. spines or keels) make it possible to increase shell-strength while retaining a relatively low density (Thayer, 1975). In bivalves, these are sometimes referred to as anchoring sculptures because of their function to prevent dislodgment from the sediment (Fig. 3C-D). The optimal solution is hollow sculptures, as they increase the surface area for minimal weight gain. A good example is the hollow keels of the cardiid bivalves Cardiumcostatum (Linnaeus) and Budmania spp., (Fig. 3C-D), (see paper I for details).

The functional role of varices in strengthening the shell was discussed in the previous section. However, an important function of varices is to add stability to the shell when resting on the substrate. They are preferentially placed on the last whorl opposite the outer lip thereby increasing the “footprint” of the shell (Fig. 4A-D, F-G), but varices can also be placed at various other locations of the shell (Fig. 4F-G). In some gastropods a dorsal varix or one or more projecting dorsal tubercles facilitate righting by

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preventing the aperture of an overturned shell from facing directly upward (Fig. 4C, F-G) (Savazzi, 1991b). Dorsal knobs are usually part of a sculpture pattern. Dorsal righting projections are typically found on the last whorl in epifaunal forms and on the penultimate whorl in infaunal forms (Savazzi, 1991b; Salgeback and Savazzi, 2006).

Gastropods living on hard substrates often have a specialized clamping aperture tangential to the shell surface, (Fig. 5F-G), that allow the shell to seal itself closely against the substrate, (Linsley, 1977). A flared lip provides the foot with a broad surface for clamping and increase stability, (Stanley, 1988). Close contact between the aperture and the substrate prevents desiccation, makes it difficult for predators to gain access to the aperture, and hinders dislodgement by wave action etc. A specialized clamping aperture is often the result of determinate, or periodic, growth and often cannot be formed by continuous growth (Savazzi, 1991b; Savazzi and Sasaki, 2004).

Gastropods and bivalves that burrow through loose sediment do so by repeating a sequence of push-pull movements, (Savazzi, 1991a). The actively burrowing part of the organism, the foot in most bivalves and gastropods, digs into the sediment while the shell acts as an anchor to prevent back-slippage. The burrowing part subsequently becomes anchored within the sediment and pulls the rest of the body forward, (Savazzi, 1989, 1991a). The external shell surfaces involved in burrowing alternately push in opposite directions against the sediment. Because burrowing requires a lot of energy, and any back-slippage wastes energy, it is desirable to make the progress through the sediment as effective as possible (Savazzi, 1991a, 1994). To do so many shell-bearing invertebrates posses burrowing sculptures, (Signor, 1982a; Savazzi, 1991a; Savazzi and Pan, 1994), (Fig. 6).

Burrowing sculptures are adaptive, offering differential friction when moving in opposite directions against the sediment. The requirements for burrowing sculptures to have maximum effect were summarized by Seilacher (1973; see also Signor, 1982a) as, (1), showing frictional asymmetry (i.e. asymmetrical in cross-section, with their steep side facing away from the burrowing direction), (2), being cross-orientated (i.e. perpendicular to the burrowing direction), (3), displaying perimeter-smoothening (i.e. being subdued or absent in regions of the shell that provide the highest cross-sectional area in a plane perpendicular to burrowing direction), and (4), being proportional to the sediment grain size, thus implying that sculpture growth should be allometrical to maintain a constant absolute height and spacing throughout the growth of the organism (Fig. 7A).

There are, however, many burrowing gastropods and bivalves that do not possess all the above characteristics of the optimal burrowing sculpture, (Savazzi, 1985). Differences between the optimal structure and the observed morphology may be due to constructional and phylogenetic limitations on

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Figure 6. Burrowing sculptures. A. Rhinoclavis aspera (Recent, Iriomote island, Japan). B. R. fasciata (Recent, the Philippines).

A BFigure 7. Theoretical and natural positioning of sculpture pattern in burrowing gastropods. A. Optimal ratchet sculpture according to Signor (1982a). Here all sculptural elements are equidistant, and the sculpture is discordant to growth lines and spiral elements. This pattern does not exist in nature. B. Spiral sculpture pattern. The number of sculptural element on each whorl is constant and distance between elements increases with growth. This is common in nature.

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evolution, (Signor, 1982a) (Fig. 7B). Some have no sculpture at all, but are still very efficient burrowers, (see e.g. Trueman 1968; Signor 1982a). Therefore it is important to be cautious when making inferences about the life habits of both gastropods and bivalves. There may be other mechanisms involved in the burrowing process that are not directly reflected in morphology and may instead be due to behavioural factors (Savazzi, 1985). This is the case with cardiid bivalves, which lack burrowing sculptures and use a combined mechanical-hydraulic burrowing process in place of utilizing an asymmetrical profile, or a constant size of the sculpture, (Savazzi, 1982, 1985).

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The papers in this study

Paper I In this paper we compare and analyse the morphological adaptations in the cardiid bivalves Cardium (Subfamily Cardiinae) and Budmania (Subfamily Lymnocardiine). Previous studies (Savazzi, 1985) have shown that species of the genus Cardium (Neogene-Recent), especially Cardium costatum,display extreme specializations in shell morphology unknown in other cardiids. Budmania (Late Miocene) was a fresh, or brackish water lymnocardiine endemic to the Pannonian lake of Eastern Europe. It is unique among the Lymnocardiinae in possessing exceptionally prominent external sculpture. Both the Cardiinae and the Lymnocardiinae otherwise display rather conservative morphologies and are not very closely related to each other. The two taxa are similar in overall shell geometry, in having a relatively low shell thickness and the presence of conspicuous, internally hollow keels.

In C. costatum and C. hians there is evidence of secondary resorption of shell material from the internal surfaces of the intercostae (the area between radial ribs), reducing shell weight. To compensate for the reduced shell thickness in this area there is a secondary deposit of material on the outside of the shell. This crusty deposit is also interpreted as deterring predators. There is no resorption or crusty deposit present in Budmania, which instead displays an overall lightweight shell.

The prominent keels of C. costatum are interpreted as optimized for performing a dual function of mechanical strengthening and as anchors within the sediment, but only for the latter in Budmania. The keels of C.costatum are straight and resistant to buckling, while the keels of Budmaniaoften are deformed. Deformed keels do not have a stiffening function. The difference is explained by different environments. Cardium lives in medium-energy marine environments (Sabelli, 1980; Gofas et al., 1989) while Budmania occupied low- to very low-energy limnic environments (Brusina, 1897, 1902; Marinescu, 1973). Hollow keels reduce shell weight in comparison with an equivalent massive structure. In very soft sediment anchoring sculpture combined with low shell weight could effectively prevent sinking within the substrate. It also prevents dislodgement. The

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higher keels in Budmania may reflect an environment in which burrowing took place infrequently and also the necessity for very effective anchors. This seems to be so since Budmania lacks several of the specializations to reduce shell weight that are observed in Cardium. C. hians do not possess keeled ribs.

This is an example of parallel evolution that allows the constructional principles, adaptive significance and possible evolutionary pathways of these features to be compared in the two lineages. The remarkable morphological similarity of keeled ribs in Cardium costatum and Budmania can be attributed to a combination of two factors: (1) parallel evolution favored by the function of keels as anchors in soft sediment, and (2) the availability of a common cardiid Bauplan.

Paper II Cerithiform gastropods are characterized by a high-spired shell, a small aperture, the presence of an anterior canal or sinus and usually a sculptural pattern consisting of one or more spiral rows of tubercules, spines or nodes. The term cerithiform, as used in this paper, is strictly morphological and has no taxonomic connotation. While it is mainly applied to representatives of the superfamily Cerithioidea it can also be used to describe taxa that were included in this superfamily in the past but are now placed in separate superfamilies. The shells of cerithiform gastropods are characterized by a determinate growth pattern, (Vermeij and Signor, 1992; Savazzi et al. in prep.), as shown by their usually specialized adult apertures. They also display a count-down pattern, (Seilacher and Gunji, 1993), where the adult aperture is preceded by other specializations of the shell.

Different shell characters were compared between different groups, which showed several examples of convergent evolution. The morphological characters of cerithiform shells are adaptive within five broad functional areas: (1), defence from shell-peeling predators, (external sculptures, pre-adult internal barriers, pre-adult varices, adult aperture), (2), burrowing and infaunal life, (burrowing sculptures, bent and elongated inhalant adult siphon, plow-like outer lip and flattened dorsal region of last whorl), (3), clamping of the aperture onto a solid substrate, (broad tangential adult aperture), (4), stabilization of the shell when epifaunal, (broad adult outer lip, and at least three types of swellings located on the left ventrolateral side of the last whorl in the adult stage) and (5), righting after accidental overturning, (projecting dorsal tubercles or varix on the last or penultimate whorl, in one instance accompanied by hollow ventral tubercles that are removed by abrasion against the substrate in the adult stage).

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Paper III This paper presents the results of an experimental study investigating shell strength in the snail Nucella lamellosa from False Bay, San Juan Island, USA. The main goal was to see whether shell repair after unsuccessful predatory attacks has an effect on the strength of the shell. One of the major predators on N. lamellosa within its intertidal habitat is the crab Cancerproductus. C. productus is capable of both shell-crushing and shell-peeling techniques when attacking its prey, (Zipser and Vermeij, 1978). When testing the shells for strength in the laboratory it was only possible to test for crushing. The experiment included 59 repaired and 68 undamaged shells. There was no significant difference in overall shell strength of the two groups. However, there was a tendency observed for cracks to merge into and follow old shell repair lines in 43% of the individuals with previous scars. The reason for the break at the site of the old scar is probably due to differences in the shell material produced during repair, for example a higher organic content.

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Svensk sammanfattning

Funktionsmorfologi är den vetenskap som behandlar sambandet mellan form och funktion hos en organism och dess olika delar. Inom paleobiologin görs funktionsmorfologiska studier både på fossilt och nutida material. Hos både snäckor (Gastropoda) och musslor (Bivalvia) fyller skalet en viktig funktion – det skyddar de ömtåliga mjukdelarna mot den omgivande miljön. Hos snäckor anses skyddet mot rovdjur vara den primära funktionen av skalet och även vara orsaken till att det först utvecklades. Även hos musslor är skyddet mot rovdjur en viktig del tillsammans med det stöd skalet ger åt mjukdelarna. Skalform och skalskulpturer påverkas av flera olika faktorer bl.a. levnadssättet, närvaro av rovdjur, samt evolutionsmönster. Ofta kan en skalkaraktär härledas till flera olika funktioner, även om en viss funktion kan vara dominerande.

Snäckor tillhör idag de vanligast förekommande skalbärande organismerna i grundhavsmiljöer, men trots detta har de inte studerats i någon större utsträckning ur ett funktionsmorfologiskt perspektiv. Det har däremot musslor, men även inom denna grupp finns mycket kvar att utforska. De två första undersökningarna i denna avhandling behandlar därmed funktionsmorfologin hos snäckskal. Den tredje studien jämför två familjer musslor där vissa medlemmar har ett markant avvikande skalmönster från deras nära släktingar.

För att kunna göra en bra analys av en struktur eller forms ursprung behöver man kombinera flera olika sorters studier. För detta ändamål utvecklade Adolf Seilacher (1970) en arbetsmetod kallad Konstruktionsmorfologi. Han beskrev den grafiskt som en pyramid där varje hörna representerar en av de faktorer – fylogeni, funktion och konstruktion – som alla påverkar formen av en organism. Seilacher vidareutvecklade senare sin metod genom att inbegripa även faktorer i organismens direkta omgivning som kan påverka morfologin, tillväxten och evolutionen. Metoden fick då namnet biomorfodynamik. För att göra bästa möjliga analys ska man gärna studera flera arter samtidigt eftersom detta underlättar förståelsen av olika adaptiva strategier och man kan därmed jämföra deras ursprung.

Skalskulpturer kan framförallt bidra till att förstärka skalet, underlätta grävning, öka skalstorleken, samt stabilisera skalet på underlaget. Skalstärkande skulpturer förekommer ofta som kontinuerliga mönster över hela skalet och inkluderar bl.a. bucklor, taggar eller ribbor. De fungerar rent

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fysikaliskt enligt samma principer som korrugerad plåt eller wellpapp där det ökade avståndet mellan två ytor bidrar till högre styvhet. Utstående skulpturer skapar även en större omkrets av skalet vilket gör det svårare för rovdjur att hantera. För att förhindra att en snäcka vänds upp och ner kan den ha anpassningar som ger mer stabilitet, t.ex. en ”svullnad” på motsatt sida av skalet som den yttre skalvingen. Detta gör att ytan som skalet vilar på blir större. Stabilitet (och ökad viloyta) kan också åstadkommas genom att den yttre skalvingen är förstorad och utsträckt i sidled. När en organism ökar den yta som den vilar på pratar man ibland om en ”snöskofunktion”. Principen är att sprida ut sin vikt över en större yta för att förhindra att organismen sjunker ner i sedimentet. Musslor som lever nedgrävda i sedimentet utnyttjar samma princip för att hålla sig på en lämplig nivå så att de står i kontinuerlig kontakt med gränsen mellan sediment och vatten. Utstående ribbor fungerar även som en förankringsmekanism som förhindrar att musslan flyttas ur sedimentet av turbulenta vattenströmmar. Exempel på ribbor med en sådan funktion förekommar hos två representanter av cardida musslor - Budmaniaspp. och Cardium costatum. Ribbornas ursprung och funktion såväl som andra specialiseringar av skalet diskuteras i artikel I.

Hos snäckor är det vanligt med förstärkningar av vissa delar av skalet som till exempel aperturen. Denna är ofta extra tjock eftersom det är den som först blir attackerad av ett rovdjur som använder sig av en skalande teknik för att komma åt mjukdelarna (t.ex. vissa krabbor). Aperturen kan även vara specialiserad för att sluta tätt till underlaget eller den kan ha anpassningar till att leva nedgrävd i sedimentet, t.ex. en sifonkanal som sticker upp och fungerar som ett sugrör vid inandning.

Majoriteten av de musslor som lever på mjuka bottnar lever helt eller delvis nedgrävda. Även bland snäckor finns många grävande former och en del lever nedgrävda mer eller mindre permanent. Grävprocessen är energikrävande och för att spara på energin har vissa snäckor och musslor utvecklat skalskulpturer som förhindrar att skalet glider tillbaka när det väl förflyttat sig. Funktionen är likvärdig med ett kugghjul. Skulpturen har en asymmetrisk profil som är svagt sluttande i grävriktningen, för att minimera friktionen, och har en skarp kant i motsatt riktning.

Artikel II i denna avhandling behandlar en stor grupp av snäckor som vi valt att benämna cerithiforma gastropoder baserat på vissa kriterier hos skalformen. Cerithiforma gastropoder visar exempel på flertalet av de specialiseringar av skalet som redan diskuterats ovan såsom grävskulpturer, sifonkanal, korrugerade skalskulptuer, specialiserade aperturer och förtjockningar/svullnader av skalet för ökad stabilitet och förstärkning.

Till följd av förmågan att producera sitt eget skal kan snäckor ofta reparera en skada som uppstår vid en attack från ett rovdjur (predation) förutsatt att den inte är för omfattande. Om snäckan efter attacken fortfarande kan dra sig in i sitt skal och gömma sig utan att blotta några mjukdelar har den en chans. Till följd av sådana attacker bildas ärr på skalet.

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De misslyckade försöken till predation är en viktig del av utvecklingen av försvarsmekaniskmer hos snäckor. Om det inte fanns individer som överlevde attacker skulle anlagen för försvarsstrukturer inte föras vidare. Hurvida ärrbildningar i snäckskal påverkar dess styrka diskuteras i artikel III i denna avhandling.

Resultatet av denna avhandling har bidragit med ny information om olika anpassningar av skalet hos både snäckor och musslor samt ökat förståelsen för den evolutionära processen och de faktorer som påverkar skalform och skalstruktur. Våra slutsatser och tolkningar kan användas för studier av andra familjer inom båda grupperna.

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Acknowledgements

These years have been filled with both good and bad days but only good people. To all of you I owe a big THANK YOU!

First of all I want to thank my former head supervisor Dr Enrico Savazzi. We have had a bumpy road but now we are finally here! I must admit I had my doubts about ever finishing but somehow you managed to push me through and I am forever grateful for that. You have helped me and supported my work throughout these five years. Your knowledge within this field is amazing and I hope you will continue to be a source of inspiration for researchers around the world for many years to come.

I want to thank my main supervisor during the last three years, Professor Lars Holmer, for help and support. I also would like to thank Professor John S. Peel for help during various stages of my thesis, Dr Jan-Ove Ebbestad for motivating me to keep working and always making time to help me with my manuscripts, and Professor Keith D. Bennett who gave financial support and helped to solve different problems during the way.

Thanks to friends and colleagues at the department that made work fun. Dr Martin Stockfors and I shared endless discussions on kitchen machines and many sushi lunches. Somehow we both made it! Sharing a room with Sofia and Ged has been a joy. Sofia – thanks for all the candy and I hope the heating system is better at Geocentrum. Sebastian – I will see you at Svettis. Åsa – always supportive and making me feel like I belong. Thank you Chris for support and help with proofreading.

I have been fortunate to travel a lot for my research. Funding for travel and work at other institutions has been provided by different grants. Coursework at Friday Harbor Laboratories (FHL), San Juan Island, USA, in the summer of 2002, was funded by a grant from KVA and financial aid from FHL. Sederholm’s travel grant from Uppsala University took me to the University of Wollongong in NSW, Australia, in February 2003, for a course on molluscan biology. Sweden-Japan Foundation funded most of my two months in Japan in 2003. I returned for two months in 2004 funded by JSPS (The Japan Society for the Promotion of Science). Additional funding throughout the years came from the Department of Earth Sciences, Uppsala University. I am very grateful for the opportunities given to me by these grants. I have learned a lot both in my professional and personal life. Travel makes you grow. Living in Japan for an extended period of time was a challenge, but also one of the best experiences of my life.

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As a guest at Tokyo University my hosts were Professor Kazushige Tanabe, Department of Earth and Planetary Science, and Dr Takenori Sasaki, The University Museum. Tanabe-san has helped me a lot in my contacts with Japan. Sasaki-san made all the arrangements for my stay both years, provided working space at the museum, taught me how to get around in Tokyo and was invaluable in every way. Dr Tatsuo Oji has been a great support for me in my research. Thank you to the students at Tokyo University for taking care of me, especially, Robert-san, Yuki-san and Tsuzumi-san.

Dr Michael LaBarbera, University of Chicago, and Dr MichaKowalewski, Virginia Tech, were my teachers at FHL and helped with preparations of one of my manuscripts. Dr Liz Harper, Cambridge, gave me access to the museum collections in Cambrige in 2001. Dr Ki Andersson gave me invaluable help with statistics. Dr Anders Warén gave me access to the collections at The Swedish Museum of Natural History, Stockhom, and provided literature.

I am blessed with many good friends in my life who always believe in me. Without them I wouldn’t be here. Peter, Mattias and Jenny made my time as an undergraduate in Lund special. Nina and Lisa introduced me to Uppsala and became two of my best friends. My “mommy-friends” - Linda, Karolina, Caroline, Evelina, Karin, Frida and Erika. We had a fantastic year together! L and K – thank you for always standing by my side. I am fortunate to have you as friends! Thanks to my best friends - Hanna, Maria, Anna-Karin and Ylva – for endless support and love through all stages of life without any obligations. Annerd – When life got rough we re-established our friendship that is now bringing us both up, and that is what a friendship should do! Your encouragement keeps me going.

My family in Seattle, Washington, USA – Carl, Grace, John, Jennifer, Jill, Rob, Brian and the kids - took care of me and made their home mine.

My sister Lena knows nothing about what I do (“something with snails…”), but is full of support! The rest of my family is also acknowledged for their love and care.

My parents – this thesis is dedicated to you because of your endless love and support. No matter what, you always believe in my capability, something I seem to forget every now and then. You have been there all the way.

Henrik – without a doubt you moved to Uppsala with me when I got this position. You have really tried to understand the weird world of academia. Thanks for help with fieldwork in Japan in 2003 (even though your own experiments with hermit crabs seemed more interesting than mine). Thank you for still being in my life and for being a great dad!

My daughter Ebba – The greatest source of happiness! You make this world a better place and I cannot imagine life without you.

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Acta Universitatis UpsaliensisDigital Comprehensive Summaries of Uppsala Dissertationsfrom the Faculty of Science and Technology 257

Editor: The Dean of the Faculty of Science and Technology

A doctoral dissertation from the Faculty of Science andTechnology, Uppsala University, is usually a summary of anumber of papers. A few copies of the complete dissertationare kept at major Swedish research libraries, while thesummary alone is distributed internationally through theseries Digital Comprehensive Summaries of UppsalaDissertations from the Faculty of Science and Technology.(Prior to January, 2005, the series was published under thetitle “Comprehensive Summaries of Uppsala Dissertationsfrom the Faculty of Science and Technology”.)

Distribution: publications.uu.seurn:nbn:se:uu:diva-7424

ACTAUNIVERSITATISUPSALIENSISUPPSALA2006

AbstractList of papersContentsIntroductionAims of this study

Living with a shellFunction of the shellShell sculptureShell strengthAdaptations to habitat

The papers in this studyPaper IPaper IIPaper III

Svensk sammanfattningAcknowledgementsReferences