Paleontological Research, vol. 9, no. 2, pp. 169–187, June 30, 2005 6 by the Palaeontological Society of Japan The function and evolution of lateral asymmetry in boring endolithic bivalves ENRICO SAVAZZI Department of Palaeozoology, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden. Present address: Kyoto University Museum, Yoshida Honmachi, Sakyo-ku, Kyoto, Japan (e-mail: [email protected]) Received July 9, 2004; Revised manuscript accepted April 20, 2005 Abstract. A substantial lateral asymmetry of the shell is observed in the bivalve genera Claudiconcha (Petricolidae), Jouannetia (Pholadidae), Clavagella and Bryopa (Clavagellidae) that bore in rock or min- eralised biogenic substrates. Two general adaptive patterns emerge from this study. (1) Lateral asymmetry is associated with cementation of one valve to the substrate, or is otherwise functional in preventing one valve from moving within the borehole, and (2) it is associated with determinate shell growth and appears only in the adult stage. The only important exception to the latter pattern is Bryopa, which secondarily lost the determinate growth pattern originally present in clavagellids. These features have evolved in- dependently in each family, and differ in several constructional and functional respects among families. Key words: Mollusca, Bivalvia, endolithic, lateral asymmetry, functional morphology Introduction 1981, 1984a, 1984b, 1989) and the Corbulidae, in which one valve is smaller and its margin closes onto a con- Typical bivalve shells are bilaterally symmetric, with chiolin layer sandwiched between two calcareous layers the exception of small-scale characters. The latter in- of the opposite valve (Lewy and Samtleben, 1979). clude hinge teeth, which must fit within sockets of the Functional and constructional reasons can be in- opposite valve, and denticulations of the commissural voked to explain most of these examples of valve margin, which interlock with corresponding notches asymmetry, although the adaptive significance of a few on the commissure of the opposite valve. The lateral instances (e.g., the commissural asymmetry and sculp- asymmetry of these characters is justified by simple ture asymmetry of the arcid Scapharca; see Savazzi, functional constraints. 1982c, and references therein) remains unclear. On Representatives of several bivalve families possess the other hand, as a general rule-of-thumb, it can be shells that deviate more conspicuously from lateral stated that bilateral symmetry of the shell normally is symmetry. These include tellinids and comparable associated with a non-cemented life style and a life forms that burrow with the commissure plane hori- orientation in which the commissure plane is approxi- zontal or inclined and as a result have evolved a bent mately perpendicular to the surface of the substrate. commissure plane, forms cemented to the substrate by The above rule applies also to boring bivalves (i.e., one of the valves, like oysters, spondylids and chamids, bivalves that actively excavate a permanent cavity in and byssate or reclining bivalves that likewise always solid substrates). rest with the same valve in contact with the substrate. As discussed below, the large majority of boring bi- Cemented rudists, in which one valve often is reduced valves possess bilaterally symmetrical shells, and sev- to an operculum-like plate closing the aperture of a eral adaptive justifications can be formulated for this large, conical opposite valve, are extreme examples of preference. This is true also of the large majority of this type of asymmetry. Further examples include a taxa within the families Petricolidae and Pholadidae. few pteriomorph and ostreid mud stickers in which However, one genus within each of these families has one valve became reduced to an extremely thin, flexi- secondarily evolved a substantial amount of bilateral ble structure (Chinzei, 1982, 1986; Chinzei et al., 1982; asymmetry. Within the family Clavagellidae, a whole Savazzi, 1996), bivalves with twisted commissure planes lineage consisting of several genera (see below) dis- (McGhee, 1978; Tevesz and Carter, 1979; Savazzi, plays a lateral asymmetry of the shell and associated 170 Enrico Savazzi structures. This paper studies these instances of bilat- boreholes about the antero-posterior axis of the shell eral asymmetry in boring bivalves, the adaptive sig- during growth (Savazzi, 1999, and therein). This factor nificance of this feature in the context of their life his- should be expected to favour (1) a bilaterally sym- tories, and the possible evolutionary pathways leading metric shell geometry, (2) a roughly circular cross- to lateral asymmetry in these forms. section of the shell (allowing for geometric constraints imposed by helical shell growth) and (3) a circular General characters of boring bivalves cross-section of the borehole. Point (3) is a simple Two boring mechanisms exist in bivalves. Chemi- consequence of rotation of the shell within the sub- cal boring involves the secretion of substances to dis- strate. For the same reason, drilled holes, machine solve the substrate, and is restricted to calcareous parts manufactured on a lathe and pottery turned on a substrates, including biogenic and nonbiogenic ones, wheel are all round in cross-section. Points (1) and (2) as well as carbonate-cemented sandstones and silt- allow shell rotation within the borehole and minimise stones containing non-carbonate grains (Hodgkin, the ‘‘wasted’’ space (i.e., the space not occupied by the 1962; Kleemann, 1973, 1974, 1980; Carter, 1978; Bo- organism) within the borehole. It is useful to remem- lognani Fantin and Bolognani, 1979; Savazzi, 1999; ber that space within the borehole is expensive to the discussions and references therein). Mechanical bor- organism, because it requires a large amount of en- ing involves abrasion of the substrate by friction of the ergy to produce. shell (and/or clasts wedged on the surface of the shell). Rotation within the borehole is also advantageous Mechanical boring takes place in a broad variety of to the organism in that it allows all portions of the substrates, including calcareous, non-calcareous and anterior region of the borehole to be equally accessi- metamorphic rocks, wood, bone, concrete, softer met- ble to the boring parts. In this way, the structures in- als and plastics (e.g., Boreske et al., 1972; Wilson and volved in both mechanical and chemical boring can be Kennedy, 1984; Kelly, 1988; Savazzi, 1999, Jenner located in a region of the organism where they are et al., 2003, and therein). optimally placed to perform their function. This is the In calcareous substrates, both mechanisms are fre- example, for instance, of the teeth and spines located quently combined, although a few bivalve taxa show a around the pedal gape in the Pholadidae and Ter- clear predominance of one or the other mechanism edinidae (Ro¨ der, 1977). In these families, the pedal (Ansell, 1970; Savazzi, 1999, and therein). Most often, gape is in an antero-ventral, rather than anterior mechanical borers are attached to the substrate by a position, because of biomechanical constraints. Thus, large and muscular foot or by a strong byssus, which each individual rasping action of these structures allows the valves to be pressed against the substrate in erodes the substrate in a corresponding oblique direc- order to exert friction. tion, rather than in the anterior direction (i.e., the di- With few exceptions, mostly found in very early rection of elongation of the shell). Rotation of the or unusual representatives (e.g., Pojeta and Palmer, shell within the borehole averages the direction of 1976; Savazzi, 1999), the shells of boring bivalves are boring over a period of time, resulting in an overall elongated in the antero-posterior direction and pene- penetration of the substrate along the antero-posterior trate the substrate roughly in the anterior direction axis of the shell. A placement of the pedal gape in an (Savazzi, 1999, and therein). This minimizes the cross- anterior position on the shell is precluded by the fact sectional area of the borehole and maximises its depth that the foot would attach to the substrate perma- (and consequently, the speed with which a suitable nently at the bottom of the borehole, and therefore depth is reached). Both factors afford a better protec- the foot attachment area would not be accessible to tion against potential epifaunal predators and other the boring structures (a comparable constraint is endolithic organisms crowding the substrate. The si- posed by the permanent byssal attachment of rock- phonal opening of the borehole, which is necessary for boring Tridacnidae; see Savazzi, 1999). However, the respiration and filter feeding, constitutes a weak ele- pholadid Jouannetia may have evolved adaptations ment in this strategy, because it can provide a passage that lessen these restrictions (see below). for predators and is vulnerable both to erosion of the Bivalves that rotate within their boreholes include substrate and to overgrowth by epifaunal organisms. the Gastrochaenidae, Teredinidae, Hiatellidae and Most boring bivalves possess adaptations that lessen most Pholadidae and Lithophaginae (Purchon, 1955; these risks (e.g., Carter, 1978; Savazzi, 1982a, 1999; Carter, 1978; Ro¨ der, 1977; Savazzi, 1982a, 1999). Bi- Morton, 1993; and therein). valves that do not rotate within their boreholes typi- Most boring bivalves, including representatives of cally produce boreholes with a non-circular