Shell Repair As a Response to Attempted Predation in Some Palaeozoic and Younger Gastropods

Shell Repair as a Response to Attempted Predation in some Palaeozoic and Younger Gastropods

ANNA LINDSTRÖM

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List of Papers

I Lindström, A. and Peel, J. S. 1997. Failed predation and shell repair in the gastropod Poleumita from the Silurian of Gotland, Sweden. Bulletin of the Czech Geological Survey 72, 115-126.

II Lindström, A. and Peel, J. S. 2003. Shell repair and mode of life of Praenatica gregaria (Gastropoda) from the Devonian of Bohemia (Czech Republic). Palaeontology 46, 623-633.

III Lindström, A. 2003. Shell breakage in two pleurotomarioid gastropods from the Upper Carboniferous of Texas, and its relation to shell morphology. GFF 125, 39- 46.

IV Lindström, A. and Peel, J. S. (in press). Repaired injuries and shell form in some Palaeozoic pleurotomarioid gastropods. Acta Palaeontologica Polonica 50.

V Lindström, A., Ebbestad, J. O. R. and Peel, J. S. (manuscript). Predation on bellerophontiform mollusks in the Paleozoic

VI Lindström, A. (manuscript). Shell repair and shell form in Jurassic pleurotomarioidean gastropods from England.

VII Lindström, A. (manuscript). Predator-prey interaction through the Phanerozoic: the history of shell repair in pleurotomarioid gastropods.

Reproduction of papers I-IV was made with permission of the copyright holder.

Paper I © 1997 Czech Geological Survey Paper II © 2003 The Palaeontological Association Paper III © 2003 Geologiska Föreningen Paper IV © 2005 Instytut Paleobiologii PAN Papers V-VII © by the authour(s)

Contents

Introduction ...... 9 Aims of this study...... 9 Predation in the fossil record...... 11 Detection of predation in fossils ...... 11 Drilling ...... 11 Shell breakage ...... 12 Unsuccessful predatory attacks...... 12 Shell repair frequency ...... 12 Predators past and present...... 13 Other causes of breakage...... 14 Adaptations in gastropods against predation ...... 14 The papers in this study...... 16 Poleumita, Praenatica and predation ...... 16 Predation on bellerophontiform molluscs...... 17 Shell repair in pleurotomarioid gastropods...... 17 Conclusions...... 19 Svensk sammanfattning...... 20 Bakgrund...... 20 Hur upptäcker man predation bland fossil? ...... 20 Artiklarna i avhandlingen ...... 21 Acknowledgements ...... 23 References ...... 24

Introduction

Organisms are well adapted to the environments in which they live, but the interaction of environmental change and natural selection has prompted the evolution of new morphologies throughout geologic time. In modern, as well as ancient seas the growth, size and shape of, for example, a gastropod’s shell are controlled by several factors, such as temperature, salinity, climate, metabolic rate, calcification and physical stress (Vermeij, 1978). One other factor is extremely important in ‘shaping’ communities and the organisms that live in them: predation. Predation is an every day phenomenon in modern animal communities and it has led to a great variety of adaptations among prey organisms in their quest to avoid being eaten, such as escape responses, camouflage, living in a cryptic habitat, chemical defence and the widespread development of armour. Gastropods afford an excellent opportunity for study since their shells are easily recognized from the Cambrian onwards, and usually contain a full record of their life history in their shells. The importance of predation as an evolutionary factor throughout the Phanerozoic, in a coevolution through geologic time between the prey and their predators, was emphasized by Vermeij (1977) in his paper on the ‘Mesozoic Marine Revolution’. Vermeij (1977, 1987) stated that predation increased with time from the Palaeozoic to Recent and that this development was seen in the evolution of shell morphology. Gastropod shell morphologies changed from simple unornamented forms in the Palaeozoic, to more sturdy forms with thick shells and protecting ornamentation in the Mesozoic. During the same time period an increase in the incidence of shell repair was also detected (Vermeij et al., 1981; Vermeij et al. 1982), coinciding with the evolution of new groups of predators (Vermeij, 1977, 1987). Increased predation pressure seemed to be one of the factors that fueled this radical evolution in shell morphology. Morphological changes induced by increased predation pressure have also been found in other groups of invertebrates (Meyer and Macurda, 1977; Signor and Brett, 1984; Aronson, 1991). As is frequently the case, increased awareness has stimulated description of more cases of repaired shell injuries after presumably failed predatory attacks in fossils other than gastropods (Strimple and Beane, 1966; Vorwald, 1982; Mapes and Hansen, 1984; Conway Morris and Jenkins, 1985; Stridsberg, 1985; Alexander, 1986; Bond and Saunders, 1989; Ebbestad and Högström, 2000, Kröger, 2004). A marked increase noted in the study of the relationships between predators and prey in fossil organisms, resulting in several publications, although this aspect is still in its infancy (Harper et al. 1998; Kowalewski and Kelley, 2002; Leighton, 2002; Kelley et al. 2003).

Aims of this study In this project, Vermeij’s prediction concerning low rates of predation has been examined through studies of the frequency of shell repair in assemblages of Palaeozoic gastropods from different geological periods (Fig. 1). Comparative studies also explored the relationship between shell morphology and the frequency and form of shell breaks. Similar morphologies were examined through geological time to investigate potential variation in predatory strategies and responses. Studies of this kind usually require access to relatively large

9 collections of exquisitely preserved gastropods, which in itself has been a limiting factor in terms of the age and composition of the available fossil samples.

Figure 1. Geological time table with the papers in the thesis indicated by an arrow at their approximate position in time.

10 Predation in the fossil record

Detection of predation in fossils Widespread as predation is in every ecological community today, it is not a process which is easily measurable when it comes to fossils. In recent faunas, animals can be studied both in the laboratory and in the field, but how is predatory behaviour detected in fossils? Direct evidence of a predator caught ‘in action’ is unambiguous but such cases are extremely rare in the fossil record, for example the Ordovician asteroid humped over a bivalve in the extraoral feeding posture described by Blake and Guensburg (1994). Other unambiguous evidence of predatory behaviour concerns finds of other organisms in the gut contents of other animals, like the trilobite fragments found in the gut of the Burgess Shale arthropod Sidneyia (Bruton, 1981) or the hyolith conchs within Ottoia (Conway Morris, 1977). Jensen (1990) described hunting behaviour in an early Cambrian olenellid trilobite based on the juxtaposition of trilobite burrows and the burrows of a worm. The functional morphology of an animal can also point towards its mode of life as a predator, like having raptorial appendages, crushing dentition, crushing claws etc, although it can be difficult to prove that they were primarily used offensively rather than defensively. Another line of evidence, however, is the drilled holes and repaired fractures which can be preserved in the shells of hard shelled organisms. Drilling frequency and shell repair frequency (both expressed as a percentage) have been widely used as measurements of the relative predation intensity (but see discussion below) (e.g. Kitchell et al. 1981; Vermeij et al. 1981; Schindel et al. 1982; Vermeij, 1982b; Ebbestad and Peel, 1997; Dietl and Alexander, 1998).

Drilling Drilling activities seem to have been continously present throughout the Phanerozoic (Harper et al. 1998; Kowalewski et al. 1998, 2000; Dietl and Kelley, 2001; Harper, 2003; Kelley and Hansen, 2003, although at a steady low level before an increase in the Cretaceous. Possible predatorial bore holes are documented already from the late Precambrian (Bengtson and Yue Zhao, 1992; Hua et al. 2003) in microscopic, tube-like mineralized exoskeletons. Similar bore holes in inarticulate brachiopods and the enigmatic genus Mobergella are also described from the Cambrian by Conway Morris and Bengtson (1994). Other examples of bore holes from the Palaeozoic are predominantely found in brachiopods (Cameron, 1967; Rohr, 1976; Smith et al., 1985; Chatterton and Whitehead, 1987; Baumiller et al. 1999; Kowalewski et al. 2000; Leighton, 2001) but there are cases in gastropods (Rohr, 1991), bivalves (Kowalewski et al. 2000) and cephalopods (Stridsberg, 1985). Not all bored holes are predatory. Baumiller (1990, 1993, 1996) found bore holes in Palaeozoic crinoids and blastoids which he referred to non-predatory activity such as parasitism by platyceratid gastropods. Other holes are interpreted as dwelling cavities made by bioeroders into shells of other organisms (Ebbestad and Tapanila, 2005; Stockfors and Peel, in press). This study does not include drilled holes, simply because they were not found in any of the examined collections.

11 Shell breakage Except for bored holes, which is usually a successful technique, successful predation is generally undetectable in fossils. The shell might be swallowed whole and pass through the digestive system without damage or, at the other end of the spectrum, it can be completely triturated by the predator in the process of handling. Fragments of a shell smashed to pieces by a predator are usually indistinguishable from those produced by mechanical causes such as post-mortem breakage through sediment overload. The best evidence of predatory behaviour is provided by unsuccessful, non-lethal attacks that are preserved as repaired injuries in the shells of organisms that have accretionary growth (e.g. molluscs and brachiopods). These fractures are easily distinguished from normal shell growth. A typical break cuts across the growth lines (and collabral ornamentation) abaperturally and new shell material fills the scar (Fig. 2). The new shell material is usually produced rather rapidly so the growth lines are more widely spaced than in normal growth. Often the scar develops a swollen appearance as new shell emerges from below the broken shell margin. The shape of the injury can vary, from evenly rounded to irregular and jagged in outline, depending on the nature of the prey and the techniques of the aggressor. While some analogies can be drawn with modern injuries, the identity of the ancient predators is often obscure.

Figure 2. Drawing of a gastropod shell with a typical repaired shell break.

Repaired shell injuries have been documented throughout the fossil record in a variety of organisms. A variety of case studies indicates that organisms were frequently attacked, or damaged sublethally, in the early Palaeozoic. Traces of predation has been reported in trilobites from the Cambrian (Alpert and Moore, 1975; Vorwald, 1982; Conway Morris and Jenkins, 1985; Babcock, 1993). Among gastropods, there are findings as early as in the Ordovician (Clarkson et al. 1995; Ebbestad and Peel, 1997; Horný, 1997a, b; Ebbestad, 1998; Horný, 2004) and Silurian (Peel, 1984; Horný, 1998). Other Palaeozoic reports concern cephalopods (Mapes and Hansen, 1984; Stridsberg, 1985; Bond and Saunders, 1989; Kröger, 2004) and brachiopods (Alexander, 1986; Ebbestad and Högström, 2000).

Unsuccessful predatory attacks Shell repair frequency Unsuccessful predatory attacks are a necessary condition for the evolution of antipredatory characters (Vermeij, 1982a). No predator has a 100 % killing rate and some individuals will survive to pass along antipredatory traits to their descendants. The frequency of repaired injuries in a gastropod fauna can be used as a measure of the level of predation, i.e a measure of the abundance and efficiency of the predator relative to the prey. Simply put: the more repair scars found in a prey population, the more often that prey population was attacked.

12 Repair frequency may be calculated as the number of individuals with at least one repaired injury divided by the total number of specimens in the sample (‘individuals with repair’ method) or as the total number of repaired injuries divided by the total numbers of specimens (‘scars per shell’ method). Both methods are used widely in studies on fossil and modern gastropods (e.g. Raffaelli, 1978; Vermeij et al. 1981; Schindel et al. 1982; Vermeij, 1982b; Cadée et al. 1997; Dietl and Alexander, 1998). One problem, however, is that these two methods can yield different results, especially if individuals have multiple repaired injuries on their shell (Alexander and Dietl, 2003). The scars per shell method would then exaggerate the percentage of individuals with repaired injuries. On the other hand, if individuals with multiple repair are only counted once, the frequency of attacks on the population will be underestimated (Alexander and Dietl, 2003). It seems to be a choice of focus for a particular study, the repairs (scars per shell method) or the individual specimens (individuals with repair method). In my studies I have lately used both methods, since they both yield valuable information. There are some other pitfalls as well. A high figure of shell repair frequency means that predators were abundant and/or that the prey were strong enough to resist shell damage. A low figure of repair frequency can mean either that predators are scarce or that they are so efficient in killing their prey that hardly any individual survive. The frequency of repair is usually relatively high within species that show antipredatory features, such as a narrow aperture, thick shell and the capacity of deep withdrawal in gastropods (Vermeij, 1982a, b). Thus, the frequency of repair becomes a measure of the effectiveness of the shell as protection against breakage (and a failure rate of predators), but it cannot be used indiscriminately as a reliable measure of the intensity of predation (Vermeij, 1982b).

Predators past and present Although predators are readily traced today it is not that easy to pinpoint the responsibility for the repaired injuries found among fossil shells, particularily in the lower Palaeozoic There are several possible groups, for example cephalopods, arthropods and the early jawed fishes, but none of these groups has with certainty been proven to be durophagous at that time (see reviews by Vermeij, 1987; Brett and Walker, 2002; Brett, 2003 with references therein). The earliest radiation of shell crushing fishes took place in the Devonian (Brett and Walker, 2002) and later on in the Mesozoic the first shell-crushing crustaceans and reptiles appeared (Walker and Brett, 2002). All that is found in much of the fossil record are the traces of predation which suggest that predators existed from early in the geological history of life. As usual, our increasing knowledge about early Palaeozoic animals and their ecology indicates a more complex story of their relationships (Conway Morris and Bengtson, 1994; Budd, 2001). In general, a modern gastropod shell can be broken in two ways, either by crushing or peeling. Crushing is the technique where the shell is squeezed between two opposing surfaces until it breaks, and it is used by many fishes, reptiles and crustaceans (See Vermeij, 1987; table 6.3 for a list of Recent molluscivores specialized in breaking shells). The mechanical advantage of a crustacean claw is a measurement of its strength, and although the crushing forces among modern crustaceans vary, all crustaceans are potent shell-crushers (Warner and Jones, 1976; Vermeij, 1987). Predators which peel their gastropod prey start breaking the shell at the aperture piece by piece, and continue doing so until the soft parts are reached. This method is mostly employed by crustaceans and some, like palinurid lobsters and the crab Calappa, are specialized to use this method (Shoup, 1968; Vermeij, 1978, 1982b). The size of a shelled prey has an important influence on the predatory technique. When a gastropod shell is small it will almost certainly be crushed by the crab's claw perpendicular to the axis of coiling and broken in half. In larger individuals, increased shell thickness inhibits breaks of this kind and crabs then try to peel back the apertural margin (Zipser and Vermeij, 1978; Elner and Raffaelli, 1980; Bertness and Cunningham, 1981).

13 Stomatopod crustaceans employ a third technique, using their second maxillipeds as powerful pounding hammers to smash the shell. This activity can leave relatively large and irregular holes through the body whorl of gastropods (Kohn, 1992; Baáuk and RadwaĔski, 1996) which might be repaired, but the most probable scenario is that the shell is destroyed and the snail eaten. Large and irregular holes in the body whorl can also be made by the tip of a crab’s chela penetrating through the internal surface of the shell when the crab fail to peel the outer lip (Savazzi, 1991, fig. 11L, M).

Other causes of breakage Predation is not the only cause of shell breakage in gastropods. Damage may result from battering by waves, saltating clasts, or grinding between boulders in a storm or in the surf zone (Savazzi, 1991; Cadée, 1999). Horný (1998) attributed a large repaired shell injury in a Silurian gastropod to the falling of a volcanic bomb. The whelks Busycon and Buccinum often break their apertural lip when trying to wedge open bivalve prey (Nielsen, 1975; Alexander and Dietl, 2003, fig. 6B). Mode of life of a gastropod can cause malformations in the shell, as seen in platyceratids conforming the apertural margin to the outline of the crinoid host (Bowsher, 1955) which may be misinterpreted. Walker and Yamada (1993) cautioned about mistaken predation by crabs on empty gastropod shells as it would bias the interpretation of predation intensity, but since the gastropod shells were empty (and could therefore not be repaired) it is only a problem when successful (lethal) predation is included in the study of predation. In modern shallow marine environments predation is the dominant shell-breaking agent (Vermeij, 1987; Feige and Fürsich, 1991; Cate and Evans, 1994). If physical agencies are important in causing shell damage then a higher incidence of repaired injuries should be found among gastropods that live in turbulent environments, but that appears not to be the case. Several studies has shown that shell thickness increase and repaired injuries are more common on less exposed shores, where the predators also live (Raffaelli, 1978; Elner and Raffaelli, 1980; Currey and Hughes, 1982). Extant tropical shells often show a higher frequency of repaired injuries than temperate shells although wave action is less intense in the tropics; and after storms there are no indications of a higher proportion of damaged shells (Vermeij 1979; 1983).

Adaptations in gastropods against predation Vermeij found a clear trend in gastropod shell morphology with time through his studies of predation in both Recent and fossil gastropods (Vermeij, 1977, 1978, 1982b, 1987; see also exhaustive review by Alexander and Dietl, 2003 and refrences therein). Loosely coiled shells with wide umbilici and round apertures, and no particular protective ornamentation, made up a larger part of the Palaeozoic gastropod fauna than of that in the Mesozoic. In the Mesozoic new shell traits appeared that were more resistant to shell breakage, such as narrow and elongated apertures, thick shells (especially a thickened outer lip), tighter coiling with the development of an inner columella, and external sculpture such as varices, knobs and spines. This notable change in shell morphological traits coincided with the appearance of several new groups of predators, especially the modern crustaceans, in the early Mesozoic in what has since been called the ‘Mesozoic marine revolution’ (Vermeij, 1977). A similar change in morphology in several organisms was referred to by Signor and Brett (1984) as the ‘Mid- Palaezoic marine revolution’, reflecting the time when the jawed fishes radiated. Vermeij et al. (1981) argued that gastropods developed new shell traits in response to the increasing abundance and strength of shell-breaking predators. The resultant arms race implied that the frequency of repaired injuries in gastropods should also increase through geologic time.

14 It has been demonstrated that certain types of shell traits among molluscs today offer very good protection against predators. The knobs and spines of thaidid gastropods protect them from predatory fishes by increasing the effective diameter of the shell and distributing the stress of the force (Palmer, 1979). Other examples are thickened outer lips in genera with determinate growth, seen in Cypraea and Strombus (Kohn, 1999). The varices of Ceratostoma deterred lethal predation by crabs (Donovan et al. 1999). When the varices were experimentally removed, crabs were more successful in crushing the shells. Leighton (2002) cautioned against using changes in prey morphology seen in the fossil record as evidence of increasing predation intensity, as there is a risk of circularity if shell morphology alone is used. Nevertheless, the increase in abundance of shell morphologies with antipredatory traits in the Mesozoic and Cenozoic, together with the increase in diversity of predators and in shell repair frequency, suggest escalation with time between gastropods and their durophagous enemies (Vermeij, 1987)

Figure 3. The Silurian Poleumita discors from Gotland, Sweden. Scale bars equal 1 cm. A. Drawing of specimen with three repaired injuries on the last whorl. B. Specimen with two repaired injuries on penultimate whorl. Note that the missing apex leaves a hole through to the umbilical side.

15 The papers in this study

Poleumita, Praenatica and predation Failed predation and shell repair in the gastropod Poleumita from the Silurian of Gotland, Sweden. Lindström, A. and Peel, J. S. 1997. Bulletin of the Czech Geological Survey 72, 115- 126 (Paper I)

Shell repair and mode of life of Praenatica gregaria (Gastropoda) from the Devonian of Bohemia (Czech Republic). Lindström, A. and Peel, J. S. 2003. Palaeontology 46, 623-633. (Paper II)

The two first papers presented here (Paper I and II), on Poleumita discors from the Silurian of Gotland, and Praenatica gregaria from the Devonian of Bohemia involved the study of hundreds of specimens of two species which belong to characteristic Palaeozoic families (Euomphalidae and Platyceratidae, respectively). In Poleumita the frequency of repaired injuries was 10 %, but in Praenatica it was only 4 %. Poleumita shows a shell morphology typical of an archaeogastropod from the Palaeozoic, with a wide umbilicus and almost circular aperture (Fig. 3); compared with modern shells it is a shell easily crushed, although Poleumita is both widespread and abundant in the Silurian. Praenatica (Fig. 4) has a morphology not unlike that of living naticids (hence the name); it is more globose and robust than Poleumita, which could be one explanation for the very low rates of shell repair found. Platyceratids, however, follow a quite different mode of life than shell-boring naticids. Several platyceratid species are found attached above the anus of crinoids and they tend to develop irregularities in the apertural margin as they conform to the uneven crinoid tegmen. This has led to the generally accepted idea that platyceratids were coprophagous and sedentary on crinoids (Bowsher, 1955; Levin and Fay, 1964). More recent suggestions are that platyceratids were parasitic and actually bored holes into the host crinoids or blastoids (Baumiller, 1990, 1993, 1996).

Figure 4. Praenatica gregaria from the Devonian of Czech Republic. A large repaired injury can be seen at the aperture. Scale bar equals 1 cm.

16 Predation on bellerophontiform molluscs Predation on bellerophontiform mollusks in the Paleozoic. Lindström, A., Ebbestad, J. O. R. and Peel, J. S. (manuscript). (Paper V)

Paper V examines a group with another typical Palaeozoic shell morphology, the bilaterally symmetrical bellerophontiform molluscs (tergomyans and gastropods) which are now extinct. It is a shell morphology that is usually mechanically weak and susceptible to crushing (Vermeij, 1977). This paper explores the distribution of repaired injuries in relation to shell form, and the presence (or absence) of a slit/sinus in the apertural margin. The species that are lenticular in shell form usually had a deep and narrow slit and was often crushed across the whole shell. Other, more round species either have a short slit or a shallow sinus, and scallop shaped injuries were found along the whole apertural margin. The species Pharkidonotus percarinatus show a shell repair frequency of 3.2 % (Fig. 5). Shell form, and the presence of a slit/sinus seem to be the most important factor governing the way in which a bellerophontiform shell breaks. Predation strategies on bellerophontiform molluscs thus seem to be dependent on the morphological features of the shells rather than their interpretation as tergomyan or gastropod. The Bellerophontiform molluscs display clear morphological changes during the Palaeozoic towards more breakage resistant forms (Signor and Brett, 1984).

Figure 5. Two bellerophontiform molluscs. Scale bars equal 0.5 cm. A. Pharkidonotus percarinatus, a gastropod from the Upper Carboniferous, USA. Dorsal view with a large repaired injury across the selenizone. B. Gamadiscus nitidus, a tergomyan from the Ordovician of Czech Republic. Left lateral view of shell with repaired injury.

Shell repair in pleurotomarioid gastropods Shell breakage in two pleurotomarioid gastropods from the Upper Carboniferous of Texas, and its relation to shell morphology. Lindström, A. 2003. GFF 125, 39-46. (Paper III)

Repaired injuries and shell form in some Palaeozoic pleurotomarioid gastropods. Lindström, A. and Peel, J. S. (in press). Acta Palaeontologica Polonica 50, xx-xx. (Paper IV)

Shell repair and shell form in Jurassic pleurotomarioidean gastropods from England. Lindström, A. (manuscript). (Paper VI)

Predator-prey interaction through the Phanerozoic: the history of shell repair in pleurotomarioid gastropods. Lindström, A. (manuscript). (Paper VII)

17 The remaining four papers (Papers III, IV, VI and VII) deal with pleurotomarioid gastropods. It is a group with a long geological record, from the Cambrian to the Recent (Knight et al. 1960). They were abundant in shallow water faunas and showed a high diversity throughout the Palaeozoic and Mesozoic. In the Cenozoic they became rarer in the fossil record and lived in deeper waters (Hickman, 1976). Today they live at depths from 100 m to 900 m (Anseeuw and Goto, 1996; Harasewych, 2002). Throughout their long record they have retained the same general shell morphology (i.e. trochiform with more or less high spire). They have also kept a most conspicuous slit in the apertural margin that when it closes forms a band in the shell called the selenizone. As in the bellerophontiform molluscs, it is generally proposed that the slit is the location for the exhalant water current expelled from the mantle cavity, although recent work on living pleurotomarioids has suggested that also the inhalant current is located here (Voltzow et al. 2004). The slit divides the aperture margin into two more or less conspicuous free lips which are supposedly mechanically weaker than a normal gastropod aperture. This division might be expected to affect the resistance of the shell to predation or other causes of shell damage. At the same time, the length of the slit can affect the extent of injuries, since propagating fractures often come to a stop at the margin of the slit. Thus, the longer the slit the more common the less harmful injuries tend to be. Pleurotomarioids form an excellent group to study predation through geological time because of their long geological record and conservative morphology (Fig. 6).

Figure 6. Pleurotomarioid gastropods from different geological periods. Scale bars equal 1 cm. A. Arjamannia thraivensis, Ordovician, Scotland, shows a repaired injury below the selenizone. B. Worthenia tabulata, Carboniferous, USA, with an injury across the selenizone. C. Jurassic Pleurotomaria anglica from England with a major repaired injury on the last whorl. D. Recent Mikadotrochus hirasei from Japan with large repaired injury.

18 The shell repair frequency were calculated for pleurotomarioids from different geological periods. The Carboniferous Worthenia tabulata and Glabrocingulum grayvillense showed repair frequencies of 17.1 % and 4.2 %. The frequency increased in the Mesozoic Pleurotomaria anglica, P. actinomphala and Pyrgotrochus sp. to between 28.8 % and 46.6 %, while in the Recent pleurotomarioids, all shells in the study showed several repaired injuries (100 %). Remarkably, the repaired injuries found do not change in appearance through time, which probably reflects presence of the slit. A relative shift with time in which type of injury is the most abundant can be seen, as well as an increase in size with time. This may be defensive strategies taken up by the pleurotomarioids as a response to more abundant predators or modified predatorial strategies.

Conclusions The development of external shells witnessed by the ‘Cambrian Explosion’ is a simple demonstration of a growing response to predation initiated more than half a billion years ago. As with many evolutionary processes, the dynamic relationship between predators and their prey is poorly understood in many parts of the geological record, although familiar and common place at the present day. The papers forming this thesis help to resolve this deficit by describing numerous examples of shell repair attributed to attempted predation in fossils of one of the most successful groups of invertebrates, the Gastropoda. Among Palaeozoic gastropods such injuries have been found and described in a wide variety of genera with different shell morphologies and modes of life, also demonstrating that repaired shell injuries, though uncommon, are more abundant than was previously thought. The individual case studies of Poleumita, Praenatica and the bellerophontiform molluscs confirm the suggestion by Vermeij (1983) and others that durophagous predation was less frequent in the Palaeozoic than the today. The series of studies of pleurotomarioids support Vermeij’s (1983) hypothesis that the frequency of shell repair increased from the Palaeozoic, through the Mesozoic, to the present day, as an indicator of the rising importance of predation as a evolutionary force.

19 Svensk sammanfattning

Bakgrund Alltsedan livets begynnelse på jorden har organismer anpassat sig för att överleva i olika typer av miljöer där olika förutsättningar existerar, som t ex variationer i tillgången på näring, klimatvariationer, skillnad i salthalt i haven, temperaturskillnader. Döden, i sin oundviklighet, är ständigt närvarande och gör sig påmind hela tiden genom konkurrensen mellan olika organismer om utrymme och föda mm. Konkurrensen inom och mellan arter spelar en viktig roll för evolutionen av nya egenskaper. Genom naturligt urval uppkommer kontinuerligt nya egenskaper som ger organismer bättre förutsättningar att överleva. En viktig faktor som driver evolutionen av egenskaper framåt är hotet från predatorer (rovdjur). För att överleva och föra sina gener vidare till nästa generation måste organismer komma på nya sätt att undvika att bli uppätna. Det finns många olika anpassningar som bytesdjur kan göra för att försvåra för predatorer: att leva gömd eller kamouflera sig, utveckla ett flyktbeteende, ha ett kemiskt försvar, eller helt enkelt skaffa sig ett yttre skyddande skal starkt nog att motstå predatorer. Eftersom organismers mjukdelar inte bevaras som fossil utom i exceptionella fall (och inte heller beteenden eller kemiska föreningar) är det skalen som blir den främsta källan för studier av betydelsen av predation genom livets historia. I skalen bevaras händelser under en individs liv och kan tolkas när de senare hittas som fossil. Predatorerna å sin sida måste ständigt utveckla nya sätt att fånga, döda och äta upp sina byten. Kapprustningen mellan byten och predatorer pågår ständigt och har pågått från början av livets historia (Phanerozoikum). Geerat Vermeij har i ett flertal artiklar och böcker (Vermeij, 1977, 1978, 1983, 1987) diskuterat denna kapprustning (‘arms race’), och genom studier på främst gastropoder (snäckor) har han dragit slutsatsen att predationstrycket har ökat genom hela den geologiska tidsperioden fram till nutid. Det Vermeij lade märke till var att gastropoders skalmorfologi ändrades med tiden. I Palaeozoikum var en större andel av gastropoders skal lösare snurrade, dvs. varven i skalet hade inte så stor kontaktyta med varandra vilket skapade ett hålrum på undersidan av snäckskalet som kallas umbilicus. Aperturerna var ofta runda och skalen hade sällan någon ornamentering (Knight et al. 1960). I Mesozoikum märktes en förändring, en ny typ av skalmorfologier uppstod som var arkitektoniskt starkare. Ornamentering blev vanlig i form av taggar, knoppar, ribbor och förtjockningar som förstärkte skalen. Aperturerna (skalöppningen) blev smalare, trängre och mer svåråtkomliga för predatorer. Framförallt minskade former med umbilicus till förmån för nya former med en inre stark pelare, columella. Nästan alla moderna gastropoder har idag varven snävt snurrade så att kontakten mellan varven blir hög och det bildas en pelare i mitten av skalet. De här förändringarna skedde samtidigt som en mängd nya predatorer uppstod i början av Mesozoikum, framförallt moderna crustaceer (kräftdjur) som hade utvecklat nya tekniker att komma åt skalbärande byten, och begreppet den ‘Mesozoiska marina revolutionen’ (Mesozoic marine revolution) myntades av Vermeij (1977). En tidigare ‘revolution’ i mitten av Palaeozoikum har senare uppdagats av Signor och Brett (1984) då framförallt evolutionen av käkförsedda fiskar tog fart.

Hur upptäcker man predation bland fossil? Bland nulevande organismer är det relativt lätt att undersöka relationerna mellan predatorer och bytesdjur, genom undersökningar i fält och i laboratorium. När det gäller fossila

20 organismer blir det genast svårare att mäta tex predationstrycket på en population av gastropoder. Man kan finna direkta bevis på predation som t ex fyndet av trilobitfragment i magen på Sidneyia, en artropod från Burgess Shale (Bruton, 1981) men det är mycket ovanligt. Det vanligaste är att man bland skalbärande organismer hittar spåren efter predation i form av borrhål eller reparerade skalskador. En predator har försökt attackera t ex en gastropod som har lyckats undkomma med skadad apertur och senare reparerat sitt skal. Kvar blir ett ärr som är lätt urskiljbart från utseendet av det normala skalet (Fig. 2). Den procentuella andelen borrhål eller reparerade skalskador blir ett mått på hur ofta en population är utsatt för predationsförsök (Vermeij et al. 1981, Vermeij, 1987, Alexander och Dietl, 2003) och även ett mått på hur vanliga predatorerna är. En hög frekvens av skalskador eller borrhål tyder på att predatorer var vanliga i omgivningarna, men även att t ex gastropodens skal var ett effektivt skydd. Om skalet hade de antipredatoriska egenskaper som nämnts ovan borde chansen att överleva en predators attack vara större. Resultat i undersökningar av frekvensen av borrhål och skalskador har visat att predationen har ökat med tiden fram till dagens höga nivå (Vermeij et al. 1981; Vermeij, 1983, 1987; Signor and Brett, 1984; Kowalewski et al. 1998; Alexander and Dietl, 2003). De låga värdena i Palaeozoikum skulle bero på att det inte fanns så många predatorer eller att de som fanns inte var tillräckligt effektiva eller starka nog att bryta sönder skal. Därefter skedde en ökning i Mesozoikum som pågått fram till nutid. Denna ökning sammanfaller väl med evolutionen av nya predatorer vid olika tidpunkter.

Artiklarna i avhandlingen Syftet med denna avhandling har varit att undersöka frekvensen av skalskador bland gastropoder från Palaeozoikum. Trots att intresset inom det här området är stort har fortfarande inte så många studier gjorts på gastropoder från den tidsperioden, kanske för att det inte förväntas några resultat andra än låga värden. Dels är det svårt att finna tillräckligt välbevarade gastropoder i ett stort antal, vilket behövs för sådana här studier. Det gjordes jämförande studier för att se hur frekvensen av, och formen på skalskador påverkas av olika typer av skalmorfologier. Lika skalmorfologier kan också studeras genom den geologiska tidsrymden för att se om förändringar sker med tiden. Den siluriska gastropoden Poleumita discors från Gotland visade upp en frekvens av skalskador på 10 %. Poleumita är en typisk palaeozoisk gastropod vad gäller skalmorfologi med rund apertur och en öppen umbilicus på undersidan, vilket anses vara en arkitektoniskt svag konstruktion. En annan gastropod som undersöktes var Praenatica gregaria från devonska lager i Tjeckien, där skalskadorna bara utgjorde 4 %. Praenatica har en annan morfologi och är mer kompakt och rund. Att den visar upp lägre frekvens av skalskador kan bero på att den inte blev attackerad så ofta. Praenatica tillhör en grupp av fossila gastropoder, platyceratider, som har hittats sittande på crinoidéers (sjöliljor) calyx, och även att en del medlemmar i familjen borrade hål vilket skulle tyda på parasitism. Det finns inga fynd som tyder på att Praenatica gjorde det, men skalen visar ofta upp ojämnheter som tyder på att aperturen formats efter underlaget vid ett stillasittande liv. En tredje form av skalmorfologi uppvisas av bellerofontiforma mollusker (i begreppet ingår både gastropoder och tergomyer). De är planispirala (snurrade i ett plan) vilket är en typ av skalmorfologi som numera försvunnit bland marina gastropoder, men finns hos en del gastropoder i sötvatten och på land. Den planispirala skalformen är vek och lätt att krossa. Vissa bellerofontiforma mollusker har även en inbuktning i aperturkanten som kallas sinus eller skåra. Två grupper i materialet utkristalliserades; de med smala, platta skal och oftast en djup sinus eller skåra, och de med mer runda skal där det sällan finns en djup sinus eller skåra. Bland arten Pharkidonotus percarinatus var det endast 3.2 % som uppvisade reparerade

21 skalskador. Relationen mellan skalmorfologi (närvaron av en sinus/skåra) och skadornas utseende diskuteras. Fyra artiklar avhandlar en grupp gastropoder som existerat från Kambrium och fram till idag, pleurotomarioiderna. Detta ger en möjlighet att följa en grupp och studera frekvensen av skalskador genom den geologiska tidsrymden. Pleurotomarioider uppvisade en hög diversitet under hela Paleozoikum och var vanliga i grunda marina miljöer, medan de nulevande 29 arterna lever på mycket stort djup (>100 meter). Den typiska skalmorfologin hos pleurotomaroider är en relativt hög spira med rundad eller flat bas (turbiniform eller trochiform), som en ‘vanlig’ snäcka. Det utmärkande är en skåra i aperturkanten där vattnet som strömmat igenom mantelhålan kommer ut, och när den sluts vartefter skalet blir större, bildas ett band i skalet som kallas selenizon. Pleurotomarioider från olika tidsperioder har studerats och frekvensen av reparerade skalskador har beräknats. I de karbonska arterna Worthenia tabulata och Glabrocingulum grayvillense är frekvensen 17.1 % och 4.2 %. Andelen skadade ökar i de Jurassiska Pleurotmaria anglica, P. actinomphala och Pyrgotrochus sp. till mellan 28.8 och 46.6 %, medan de nulevnade arterna i den här studien alla uppvisar någon skada (100 %). Detta kan bero på en ökning i diversitet med tiden av predatorer som föreslagits av Vermeij. Skadorna har dock under årmiljonerna genomgående samma karaktär och utseende, vilket skulle tyda på att det är skalets form och framförallt skåran/selenizonen som avgör hur ett pleurotomarioidskal bryts.

22 Acknowledgements

I want to thank my supervisor John S. Peel for always offering encouragement, his endless patience and for sharing his knowledge of Palaeozoic gastropods over the years. All friends and colleagues at the department, past and present, made ‘Pallen’ a warm and nice working place. We have had many good times together, both inside and outside the house; numerous coffee breaks, parties, discussions, field trips, movie nights, piano lessons, adventures moving furniture (both institutional and personal) and, in recent years, a lot of children’s birthday parties. A stipend from Bjurzons resestipendiestiftelse, Uppsala universitet, took me to Gotland in the summer 1998, and Stiftelsen Hierta-Retzius stipendiefond, Kungliga Vetenskapsakademien, financed a trip to The Natural History Museum, London, in the autumn 2000. Travels to Národní Museum, Prague (1998); Carnegie Museum of Natural History, Pittsburgh, and Smithsonian Institution, National Museum of Natural History, Washington, D.C. (1999) were carried out with support from NFR (now Vetenskapsrådet) through grants to John S. Peel, and from Institutionen för Geovetenskaper (Historical Geology and Palaeontology, now Palaeobiology). A second trip in 2003 to the Natural History Museum, London, was possible with a grant from Liljewalchs resestipendium, Uppsala universitet. Over the years I have had a lot of fun outside palaeontolgy and I would like to thank all of my friends for making the time as an undergraduate and graduate student in Uppsala enjoyable and memorable. My best friend Britta Alstad has always been a rock to rely on. With Rike Pirntke and Sven Schultz, I have literally spent hours and hours outdoors in all kinds of weather at different playgrounds. Last, but not least, I would like to thank my beloved Henning who has always supported and comforted me, pushing me when needed, and helping me with different computer tasks. His computer skills are very good and I have always trusted him completely (although I can recall at least one computer crash after his fiddling!). Henning and I have two wonderful daughters, Selma and Agnes, whose mere existence is a constant source of love and happiness.

23 References

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