Mercenaria, Schumacher, 1817

Mikkelsen, Paula M., Bieler, Rüdiger, Kappner, Isabella & Rawlings, Timothy A., 2006, Phylogeny of Veneroidea (Mollusca: Bivalvia) based on morphology and molecules, Zoological Journal of the Linnean Society 148 (3), pp. 439-521 : 446-451

MERCENARIA : AN EXEMPLAR VENEROID

In the absence of undisputed synapomorphies and clear diagnoses of higher-level taxa, a useful means for beginning a discussion of Veneroidea is to examine one of its best understood members, Mercenaria mercenaria ( Linnaeus, 1758) ( Veneridae : Chioninae ), the hard-shelled clam or ‘quahog’, native to eastern North America and introduced to northern Europe, Puerto Rico, and north-western North America. This species has prompted a very large body of published literature, including that on its morphology and life history (e.g. Kellogg, 1903; Kraeuter & Castagna, 2001), as a result of its role in the commercial hard clam industry of the eastern USA. It has been harvested for food and/ or raised in aquaculture for c. 300 years in its native range, and was once (as wampum) used as a form of currency among indigenous peoples. Mercenaria mercenaria is also appropriate for this role here because it was long treated as the type species of the genus Venus ; it was designated as such, although invalidly according to ICZN rules, by Lamarck (1799), and many subsequent workers continued to use Mercenaria mercenaria as type throughout the 19th century ( Dodge, 1952). [The now-accepted type species of Venus , V. verrucosa Linnaeus, 1758 , is comparatively less well known.] This summary description of Mercenaria mercenaria will serve to exemplify the morphological characters that have served (or ultimately will serve) to define members of this superfamily and its components.

The shell ( Fig. 1 ) is thick walled, well inflated in the adult, and rounded trigonal in shape, with the umbones more anterior (at approximately one-quarter of the anteroposterior length), resulting in a shorter anterior end and a longer sloping (sometimes rather rostrate) posterior end. The umbones are prosogyrous over a distinctly demarcated, cordiform, and flattened lunule, the latter subequal in each valve and bounded by an incised line. From the anterior aspect, both the shell outline and the lunule are heart-shaped, hinting at the origins of Linnaeus’ taxon Venus (i.e. the proper name of the Roman goddess of love) and its resultant family name Veneridae . Externally, the shell is sculptured by crowded, coarse commarginal growth lines that are elevated as dense lamellae anteriorly, continuing over the lunule. The ventral surfaces of the lamellae have faint radial riblets. The commarginal lamellae are lowest, often smooth, at the centre of the valve. Posterodorsally, the escutcheon is broad, subequal in each valve, gently sloping towards the ligament, and not bounded by an impressed line or change in sculpture (although slightly heavier on the right side than the left); the shell edge at the posterior end of the right escutcheon overlaps the left. The ligament is external, extending from the lunule to approximately half the distance from the umbo to the posterior corner of the valves. Overall the shell is chalky greyish white, sometimes marked to a variable degree with brown chevrons (forma notata Say, 1822), or stained black by anoxic sediments. The periostracum is thin and yellow, but generally inconspicuous, evident in adult shells only as brown threads between the distalmost commarginal ridges. Structurally, the shell is aragonitic and composed of three layers: an outer composite prismatic layer, a middle cross-lamellar layer, and an inner homogenous layer; the inner shell layer has a greater proportion of conchiolin than the outer and middle layers ( Jones, 1979).

Internally the shell is porcellaneous white, usually flushed with dark purple. The purple flush is usually located posterodorsally on the hinge plate, anteriorly outside of the anterior adductor muscle (AAM) scar, and especially, posteriorly, covering (to a variable extent) the posterior adductor muscle (PAM) scar, the pallial sinus, and the shell margin outside of the pallial line. The AAM and PAM scars are teardropshaped, with the posterior slightly broader than the anterior. The slightly impressed pallial line extends from the posteroventral points of each adductor muscle scar, parallel to the ventral shell margin, and includes a short, triangular, anteriorly directed pallial sinus adjacent to the PAM scar. The anterior pedal retractor muscle scar is impressed, near (but fully separated from) the AAM scar, on the ventral surface of the hinge plate. The posterior pedal retractor muscle scar is confluent with and forms the dorsalmost point of the PAM scar. The outer shell margin is indented at the distal end of the lunule. Across the lunular margin and ventral to the lunule, minute denticulations adorn the margin to the posterior corner of the valves. The margin is smooth from the posterior corner, including the siphonal area, to the distal end of the ligament.

The hinge plate is moderate in strength, and shows no attrition (defined in other bivalves as excavation of the hinge plate so that the hinge teeth effectively extend past the ventral margin). Each valve has three radiating cardinal teeth. In the left valve (LV), the anterior cardinal [2a, numbered following the hinge formula model of Félix Bernard (1895), based on ontogenetic development of the teeth] is strongest and slightly bifid, the middle (2b) is strongly bifid, and the posterior (4b) is blade-like and appressed to an irregularly rugose area between it and the ligamental nymph. In the right valve (RV), the anterior cardinal (3a) is blade-like, and the middle (1) and stronger posterior (3b) cardinals are strongly bifid. An elongated irregularly rugose area exists between the posterior cardinal and the nymph of each valve; these pronounced interlocking rugose areas, diagnostic of the genus Mercenaria , possibly function as additional ‘teeth’ to ensure proper valve occlusion ( Dall, 1902; Jones, 1979). No cardinal teeth are united dorsally, as occurs in some other venerid taxa (see below). Both anterior and posterior lateral teeth are absent (although anterior lateral teeth are present in other veneroids, see Appendix 1). The ligament is supported by a nymphal shelf, which terminates abruptly before the posterior end of the ligament or ligamental pit. Posterior to the ligament, the shell edges interlock via an elongated ridge in the LV and a corresponding elongated trough in the RV (also forming the shell overlap seen at the posterior end of the escutcheon).

Internally ( Fig. 2A), the Mercenaria mantle edges are unfused from the AAM to the ventral point of the siphonal retractor muscle, just behind the heel of the foot. The mantle edge is thickened by muscle fibres and has four folds: (1) the outer (which secretes the shell and periostracum), (2, 3) the middle, divided into two folds (a smaller outer-middle, which is sensory, and a larger inner-middle, which controls water flow), and (4) the inner (which possibly directs foreign particles out of the mantle cavity) ( Eble, 2001). Posteriorly, folds 3 and 4 are fused [siphonal fusion type B of Yonge (1957)] to form short (relatively longer in juveniles) incurrent (ventral) and excurrent (dorsal) siphons that are united for their entire length. The incurrent (= branchial) siphon is slightly larger in diameter. The excurrent (= anal) siphon is equipped with a conical valve, more obvious in juveniles. The terminus of each siphon is fringed with simple tentacles. Interiorly, the proximal ends of the siphons have siphonal membranes (to which the tips of the gills attach) and siphonal valves, whose slit-like openings control water flow in both directions. The siphons are retracted by siphonal retractor muscles, which form a triangular muscle mass on the surface of each mantle flap (and whose margins attach to the interior shell surface to produce the pallial sinus). Ciliary waste currents on the inner mantle surfaces pass particles posteriorly to a point at the base of the incurrent siphon; waste is discharged through the incurrent siphon upon contraction of the adductor muscles (rather than through the excurrent siphon as one might predict; Kellogg, 1915).

Each adductor muscle is comprised of two parts, a larger, more central, somewhat darker pinkish-to-red portion, composed of ‘quick’ muscle fibres, flanked on its outer surface by a crescent-shaped whitish portion, comprised of ‘catch’ fibres. The pink pigment of the adductor muscles has been identified as haemoglobin ( Eble, 2001).

The visceral mass is suspended by the anterior and posterior pedal retractor muscles. These originate in the anterior and posterior parts of the foot, respectively, and insert on the shell above the adductor muscles (see pedal retractor muscle scars, above). The foot extends along the entire ventral surface of the visceral mass. It is wedge-shaped, laterally compressed, keeled ventrally, and extended slightly posteriorly (as a ‘heel’) and greatly anteriorly. Serving as the main tool for burrowing into soft sediment, the foot is composed primarily of muscle fibres. The muscle fibres are irregularly distributed vertically and horizontally, and are interspersed with haemocoelic spaces, which allow expansion when filled. A pedal gland lies in the midline of the foot ( Jones, 1979), which produces a byssus in juvenile Mercenaria , but which is inactive in adults.

The plicate eulamellibranch ctenidia occupy much of the pallial cavity on either side of the visceral mass. Each consists of an outer and (longer) inner demibranch, extending from between the labial palps, along the ventral edge of the pericardium to the siphonal membrane. A supra-axial extension of the outer demibranch covers the pericardial space (= pericardial coelom) anterior to the PAM. The gill filaments are connected via tissue junctions and the lamellae are connected by interlamellar septa that, together with intervening plicae, define and delimit water tubes. Plicae are of two kinds, major and minor, the latter being secondary folds at the apices of the major plicae ( Eble, 2001). Ciliary currents on the gills pass particles on each surface to the food groove at the free edge of each demibranch then forward to the palps ( Kellogg, 1915). The anterior ends of the inner demibranchs are inserted into and fused with the distal oral groove [category II of Stasek (1963)]. The labial palps are elongated triangular structures posterior to the AAM on either side of the visceral mass. Each side comprises two palps, the inner surfaces of which are folded to form numerous fine ciliated ridges, which serve to further sort and channel food particles collected by the gills into the mouth opening.

The mouth opening lies between the labial palps just posteroventral to the AAM. It leads to a short oesophagus, lined by dense rugae, which passes posterodorsally to the stomach. The globose stomach lies in the dorsal part of the visceral mass, surrounded anteriorly by lobes of the digestive gland. It comprises a dorsal hood and larger ventral portion, separated by a shelf and possessing a large sorting area. A thin gastric shield covers the roof, most of the left interior wall, and part of the posterior floor of the stomach where it is strengthened by ribs. The ducts to the digestive gland open into the stomach via left and right caeca. Typhlosoles pass in and out of the two caeca [thus corresponding to the type V stomach of Purchon (1960)] and extend into the ventral midgut or intestine (conjoined to the style sack). A crystalline style secreted by the style sack extends well into the stomach in living specimens. The intestine continues ventrally from the distal end of the style sack to create a somewhat variable series of loops in the anteroventral part of the left side of the visceral mass ( Jones, 1979), then runs posterodorsally to exit the visceral mass near the posterior end of the heart. The intestine passes through the ventricle of the heart (presumably acting as a stabilizing structure for the contracting ventricle; Eble, 2001) and over the aortic bulb of the posterior aorta, then dorsally over the surface of the PAM to terminate at the anus near the inner opening of the excurrent siphon. The major typhlosole continues into the postmidgut part of the intestine to the point where it turns to ascend posteriorly towards the heart (= ascending intestine). The rectum ( Jegla & Greenberg, 1968) is highly muscular with numerous typhlosoles, producing unsculptured oval faeces of uniform composition, a format which has been called derived (vs. sculptured pellets with segregated sediments; Kornicker, 1962).

Gonadal tissue lies within the visceral mass, generally ventral to and surrounding the darker-coloured digestive gland. Gonoducts open into the suprabranchial cavity ventral to the pericardium.

The large pericardium lies at the dorsal midline, posterior to the visceral mass and anterior to the PAM. The heart consists of a single ventricle and two auricles, connected laterally to the ventricle via valved openings. Paired dark brown pericardial glands open into the pericardial space ( Eble, 2001). The anterior aorta passes dorsal to the intestine to supply anterior haemocoelic sinuses. The posterior aorta continues posteriorly ventral to the intestine to supply posterior sinuses, interrupted by a muscular, spongy aortic bulb posterior to the pericardium. The haemolymph contains several types of granulocyte capable of phagocytosis (summarized by Eble, 2001). The kidneys lie along the ventral side of the pericardial space, communicating with the auricles and emptying via renopores into the epibranchial chamber.

The nervous system has three main pairs of yellowish ganglia: cerebral (near the anterior pedal retractor muscles; innervating the palps, mantle, visceral mass, pedal retractor muscles, and AAM), visceral (on the anterior face of the PAM; innervating the mantle, ctenidia, kidneys, heart, and PAM), and the more fully fused pedal (just anteroventral to the distal end of the midgut; innervating the foot). Smaller auxiliary siphonal ganglia communicate via large nerves with the visceral ganglia. The complex system of nerves in Mercenaria mercenaria was detailed by Jones (1979).

Mercenaria mercenaria is a protandrous hermaphrodite (although some individuals mature directly into females, whereas others are simultaneous hermaphrodites; Loosanoff, 1937a, b; Jones, 1979) and has 19 pairs of chromosomes ( Menzel & Menzel, 1965). Gametes are spawned freely into the water column. Mature spermatozoa have been observed in specimens only 5–7 mm in length ( Loosanoff, 1937a). Larval development is planktotrophic, with veligers settling after approximately 12 days; the prodissoconch ranges in size from 170 to 240 µm in length; the plantigrade juvenile (early benthic stage) is byssate, with an unformed incurrent siphon ( Carriker, 2001). The growth rate is variable with environmental conditions; growth to a marketable size (‘littleneck’ or 48 mm shell length) can take 15 months in warm southern waters, but 4 years in cooler northern waters. Shell layers in cross-section reveal annual growth increments through periodic winter growth cessation marks; very large specimens (c. 15 cm length) are estimated to be at least 40 years old ( Fritz, 2001).

Perhaps because of its commercial status, Mercenaria mercenaria is one of the most used veneroids for molecular phylogenetic work. At the time of writing, at least ten independent sequences have been generated for phylogenetic use and either cited or posted on GenBank: 16S (Ó Foighil, Hilbish & Showman, 1996; Canapa et al., 2003), 18S ( Adamkewicz et al., 1997; Campbell, 2000; Giribet & Wheeler, 2002), 28S ( Rosenberg et al., 1997; Park & Ó Foighil, 2000; Giribet & Wheeler, 2002), and COI ( Peek et al., 1997; Giribet & Wheeler, 2002) (see below). An additional 18 microsatellite sequences reside on GenBank from an unpublished study by Gjetvaj, King & Lubinski, as does a complete 1628 bp cytochrome P450 30 mRNA sequence ( Brown, Clark & Van Beneden, 1998).

Ecologically, Mercenaria mercenaria generally inhabits intertidal to shallow subtidal mud, sand or seagrass habitats; the maximum recorded water depth of living specimens is 12 m ( Harte, 2001). It is a relatively rapid burrower ( Stanley, 1970), and its adult size and shell thickness aid in deterring most predators (e.g. crustaceans, fish; Harte, 2001). The species is tolerant of wide ranges of salinity and temperature, but relies on oceanic conditions for spawning.

Figures

Figure 1. Mercenaria mercenaria, showing features of venerid shell morphology coded by this analysis. A, right lateral view of exterior of right valve. B, right lateral view of interior of left valve. C, dorsal view of articulated valves, anterior to the right. aams, anterior adductor muscle scar; aprms, anterior pedal retractor muscle scar; com, commarginal sculpture; esc, escutcheon; hp, hinge plate (with cardinal teeth); lig, ligament; ligp, ligamental pit; lun, lunule; mar, shell margin; pams, posterior adductor muscle scar; pl, pallial line; ps, pallial sinus; u, umbo.