More light on photosymbiosis in fossil mollusks: The case of Mercenaria “tridacnoides”

Palaeogeography, Palaeoclimatology, Palaeoecology, 64 (1988): 141 152 Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

141

MORE LIGHT ON PHOTOSYMBIOSIS IN FOSSIL MOLLUSKS: THE CASE OF MERCENARIA "TRIDACNOIDES" D O U G L A S S. J O N E S 1, D O U G L A S F. W I L L I A M S 2, and H O W A R D J. S P E R O 2 1Florida State Museum, University of Florida, Gainesville, FL 32611 (U.S.A.) 2Department of Geological Sciences, University of South Carolina, Columbia, SC 29208 (U.S.A.)

(Received October 1, 1987)

Abstract Jones, D. S., Williams, D. F. and Spero, H. J., 1988. More light on photosymbiosis in fossil mollusks: the case of Mercenaria "tridacnoides". Palaeogeogr., Palaeoclimatol., Palaeoecol., 64:141 152. Several morphological, paleoecological, and life history criteria have been traditionally employed when testing for possible cases of photosymbiosis among fossil mollusks. Recently, another criterion has been proposed based upon the offset observed in stable isotope patterns (particularly ~3C) in a modern photosymbiotic bivalve. This study combines stable isotope and growth increment analyses with traditional criteria for recognizing molluscan photosymbiosis in an investigation of the important but peculiar bivalve, Mercenaria "'tridacnoides", from the Neogene of the southeastern United States. M. "tridacnoides", as its name might hint, has been proposed as a possible photosymbiotic host. However, the geochemical and paleontological data presented here reinforce each other and suggest otherwise. This case illustrates the increased predictive power obtained by combining geochemical with more traditional paleontological approaches.

Introduction Algal symbiosis refers to the c o e x i s t e n c e of a h o s t o r g a n i s m with one or m o r e species of u n i c e l l u l a r algae. In such a s s o c i a t i o n s the algae are c o n t a i n e d w i t h i n the tissues of the host, either intra- or i n t e r c e l l u l a r l y (Trench, 1979). The i n t i m a c y of the a s s o c i a t i o n varies from f a c u l t a t i v e to obligate a n d is p r e s u m a b l y m u t u a l i s t i c in most cases. In a simplified model, the host benefits by utilizing s y m b i o n t photos y n t h a t e s w h i c h h a v e been released inside its tissues. The s y m b i o n t benefits by living inside a homeostatically controlled microenvironm e n t w h e r e its r e q u i r e m e n t s for light, nutrients, i n o r g a n i c c a r b o n (CO2), a n d t r a c e elem e n t s are provided (Trench, 1979). T h e r e are t h r e e m a i n g r o u p s of algal s y m b i o n t s particip a t i n g in s u c h relationships: blue-green algae 0031-0182/88/$03.50

(cyanobacteria), green algae (zoochlorellae),anddinoflagellates(zooxanthellae),withthe l a t t e r g r o u p being the most a b u n d a n t and w i d e s p r e a d in the m a r i n e e n v i r o n m e n t . P h o t o s y m b i o t i c associations, p e r h a p s most familiar in h e r m a t y p i c corals, are distributed across several e x t a n t m a r i n e g r o u p s i n c l u d i n g the p r o t o z o a n s , sponges, flatworms, cnidarians, mollusks, and ascidians. M a j o r questions exist r e g a r d i n g the e x t e n t of p h o t o s y m b i o s i s in the fossil r e c o r d and w h i c h species evolved into s u c h an association. W h e n and how often did symbiosis evolve and u n d e r w h a t conditions? The a n s w e r s to such questions depend u p o n o u r ability to r e c o g n i z e evidence of p h o t o s y m b i o s i s preserved in fossil taxa. D i r e c t evidence of symbiosis (i.e. discovery of the s y m b i o n t s themselves) is h i g h l y u n l i k e l y in the fossil r e c o r d b e c a u s e the s y m b i o n t s do

(~ 1988 Elsevier Science Publishers B.V.

142 not produce identifiable structures in the hard parts or skeleton of the host (Cowen, 1983). Therefore, indirect criteria (i.e. analogies with modern taxa) are traditionally used. Numerous ecological, morphological, and life history characteristics have been associated with modern photosymbiotic hosts. When these characteristics appear in fossil contexts, cases of photosymbiosis are frequently inferred. This approach is only moderately satisfactory, however, and has often led to inconclusive or controversial results (e.g. the case investigated here). Our principal objective in this paper is the recognition of molluscan paleophotosymbiosis. We first review established criteria used to identify photosymbiotic hosts in the fossil record and then briefly discuss a new criterion based on the stable isotopic composition of shell carbonate. We then apply stable isotope analysis, growth increment analysis, and other more traditional criteria to the case of Mercenaria "tridacnoides'" (Fig.l), a stratigraphically important albeit controversial Neogene bivalve from the Atlantic Coastal Plain which has been suggested to be a photosymbiotic host (Seilacher, 1985). This study illustrates the value of analyzing several criteria in concert when none seems to be completely diagnostic on its own.

Criteria for recognition of paleophotosymbiosis In an excellent review of algal symbiosis and its recognition in the fossil record, Cowen (1983) proposed a number of indirect criteria or correlates of photosymbiosis for evaluating potential photosymbiotic hosts among fossil foraminifera, corals, brachiopods, or mollusks (or other taxa). These correlates include: Light exposure: If it can be demonstrated that a fossil species maintained a characteristic life position such that body tissues were displayed to light, then an hypothesis of algal symbiosis may be proposed (Cowen, 1983). Caution must be exercised, however, because other factors such as gravitational stability,

food gathering, current direction, or even competition for space may also produce specific orientations. In addition to general body orientation and tissue exposure, particular structures may be shown by functional analysis to enhance exposure to light. Examples among the Bivalvia include the flanges of Tridacna, laterally flared extensions of the shell margin which support the display of algal-bearing mantle tissue (Cowen, 1983), and the localized areas ("windows") within certain shells such as Corculum that promote the transmission of light (Vogel, 1975; Watson and Signor, 1986). Calcification: It is a general observation that hosts of algal symbionts secrete carbonate more rapidly than their aposymbiotic counterparts (Cowen, 1983). Several hypotheses have been advanced to account for this observation: (1) CO2 removal by photosynthesis helps drive bicarbonate to carbonate (Goreau, 1959); (2) algal uptake of phosphate which could otherwise act as a crystal poison to inhibit carbonate deposition (Simkiss, 1964); (3) release of photosynthetic energy for calcification (Chalker, 1976); and (4) energy release for organic matrix formation to aid calcification (Wainwright, 1963). The consequences of increased calcification may be expressed as rapid skeletal growth rates, large size or massive structure, high skeleton-to-body ratios, or any combination of the three (Cowen, 1983). Studies of temporal markers in the shells of bivalves (i.e. periodic growth lines) suggest large size and rapid growth are inter-related (Jones, 1985). Cowen (1983) observed that regardless of taxa (i.e. mollusca, foraminifera, cnidaria, or radiolaria) symbiotic hosts are generally larger and faster growing than their aposymbiotic counterparts. Fortunately in the case of bivalve mollusks, most species possess periodic growth lines (Lutz and Rhoads, 1980) which may be used to distinguish between rapid versus slow calcification. Stable isotopes: During algal photosynthesis, the stable isotopes of carbon and oxygen are fractionated, and evidence of this fractionation

143

Fig.1. Specimen of Mercenaria "tridacnoides" (UF 11150)from Pliocene Pinecrest Beds, Sarasota, Florida. A. Marginal view showing undulatory commissure. B. Interior of left valve. Scale bar has cm divisions. may be p r e s e r v e d to v a r y i n g degrees in the c a r b o n a t e s k e l e t o n of the host (Cowen, 1983). E v i d e n c e for such p a t t e r n s has been r e p o r t e d in f o r a m i n i f e r a (e.g. Erez, 1978; Williams et al., 1981) and corals (e.g. Erez, 1978). In the latter, the symbionts seem to h a v e little effect on the

o x y g e n isotopic c o m p o s i t i o n of the skeleton, while c o n c e n t r a t i n g the h e a v i e r isotope of c a r b o n in the calcification pool (Swart, 1983). In f o r a m i n i f e r a , c a r b o n isotopic disequilibrium appears to be a f u n c t i o n of s y m b i o n t photosynt h e t i c r a t e (Spero, 1986).

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Fig.2. Plot of carbon versus oxygen isotopic values for the photosymbiotic giant clam, Tridacna maxima, and the gastropod, Terebra areolata, from J o n e s et al. (1986). Offset in the carbon values between the two species is attributed to the presence of zooxanthellae in the giant clam.

Analogous isotopic studies on photosymbiotic mollusks are rare. However, recent studies involving modern symbiont-bearing Tridacna maxima (Jones et al., 1986; Romanek et al., 1987) suggest that isotopic fractionation patterns may be used to differentiate molluscan photosymbiotic hosts. Tridacna maxima showed a marked depletion in 13C by approximately 2% (Fig.2) when compared to nonsymbiotic mollusks from the same site (Jones et al., 1986). At the same time, no offsets in the oxygen isotopic records were observed. This depletion in the 513C composition of T. maxima was explained through the incorporation of excess metabolic CO2 (isotopically light) into the skeleton which originated from a zooxanthellae-enhanced metabolic rate in the host. This model was in accordance with the Erez (1978) model of calcification. This pattern of depletion in the carbon records of photosymbiotic mollusks should be considered preliminary in view of the need for further analysis of additional modern molluscan species and in light of recent criticisms of the Erez model as it applies to corals (Swart, 1983). Paleoenvironment: Shallow water depth (eu-

photic zone) and adequate water clarity are requirements for high symbiont primary productivity in oligotrophic environments. If sedimentological, faunal, or other evidence mitigates against these conditions, calcifying photosymbiotic organisms are unlikely to propagate extensively (Hallock and Schlager, 1986). Photosymbiosis is also predominantly a tropical phenomenon among benthic organisms today, particularly prevalent in reef environments. Therefore, fossil reef environments may be expected to contain greater concentrations of photosymbiotic hosts whereas paleogeographic evidence that indicates a non-tropical setting lessens the likelihood of finding paleophotosymbiotic hosts among the calcifying benthos.

Molluscan photosymbiotic hosts The distribution of photosymbiotic relationships among modern mollusks is limited to two bivalve lineages of highly modified cardiaceans. More familiar are the tridacnids or giant clams of the Indo-Pacific. These bivalves (including several species of Tridacna and Hippopus) possess strongly skewed body plans such that in life-position hypertrophied siphonal tissues bearing zooxanthellae are directed upward with the plane of commissure in the vertical orientation (Yonge, 1936; Rosewater, 1965). Mantle tissues fill the sizable gape between the corrugated valve margins, exposing the algal symbionts to sunlight. Less familiar are the heart cockle, Corculum, and the closely related strawberry cockle, Fragum. Unlike Tridacna, Corculum does not gape to expose zooxanthellae-laden mantle tissue to sunlight. Instead, Corculum reclines on the substrate and employs "windows" or localized transparent regions in the flattened upper surface of its thinned shell to enhance light penetration through the shell to the zooxanthellae (Kawaguti, 1950; Seilacher, 1972, 1973; Watson and Signor, 1986). Fragum fragum lives with the posterior side of the shell above the substrate and like Corculum, sustains zooxanthellae by light transmitted

145 through windows in the shell. In contrast, Fragum unedo lives burrowed just below the sediment water interface, keeping its flattened posterior upward with its valves open wide. An expanded posterior mantle bearing a heavy concentration of zooxanthellae surrounds the siphons and is spread over the sand bottom like a carpet, well beyond the shell margins, exposing the tissue to sunlight (Kawaguti, 1983). When the criteria for recognition of paleophotosymbiosis outlined above are applied to these modern mollusks, some of the problems t h a t could arise while attempting to identify photosymbiotic hosts among fossil mollusks become evident. For example, Corculum possesses special structures (windows) and lives in an orientation which enhances exposure to light (Watson and Signor, 1986). However, its thin shell and small size (especially when compared to the tridacnids) suggest only modest calcification rates, contrary to conventional wisdom. Fragum fragum is still smaller and lacks morphological features in its shell that indicate it lives in a shallow burrow with the posterior portion exposed. The most complicated situation involves Fragum unedo. This cockle is also relatively small, lives burrowed in nmddy sand (which might be cited as evidence against water clarity), and its shell architecture contains no evidence suggesting its mantle is spread over the sand. If Fragum unedo were known only from the fossil record, it is quite probable that its photosymbiotic existence would never have been hypothesized. Several fossil molluscan groups have been implicated as photosymbiotic hosts (see summaries by Cowen, 1983; Seilacher, 1985). Most of these groups are extinct, however, and considerable debate has surrounded the interpretations used to argue for symbiosis. Little insight into the evolution of molluscan symbiosis has been gained through examination of fossil ancestors of the modern photosymbiotic cardiacean group, as this group remains incompletely known (Stasek, 1962). Certain rudists may have had symbiotic algae (Kauffman, 1969) and Philip (1972) has

argued in favor of this hypothesis, citing evidence for exposure of mantle to light, phototropism, rapid calcification, and growth to enormous size. Further discussions presented by Kauffman and Sohl (1974), Vogel (1975), and Skelton (1979) are treated in the summary by Cowen (1983). The alatoconchids are the oldest group of bivalves presently believed to have housed algal symbionts (Yancey, 1982). They represent a large arid unusual group of bivalves known from Permian strata of the Tethyan Province. Apparently the alatoconchids maintained a vertical plane of commissure, similar to modern Corculum and Tridacna, while their microstructure may have also transmitted light in a fashion similar to Corculum. Other large bivalves such as ostreids and inoceramids have been proposed as photosymbiotic hosts. Though no living oysters are known to have algal symbionts, certain fossil species represent reasonable candidates (e.g. species with massive lower valves and small upper valves). Cowen (1983) discusses these and provides some alternative interpretations so that the question of symbiosis in fossil ostreids clearly requires further study. The inoceramids, on the other hand, seem unlikely to have had symbionts. Their broad environmental tolerance and their occurrence in habitats characterized by turbid water and/or considerable water depth argue against symbiosis (Cowen, 1983).

Mercenaria "tridacnoides" Application of the indirect criteria used to recognize photosymbiosis among fossil mollusks has often resulted in controversial conclusions. Perhaps no case better exemplifies this than the current disagreement surrounding the large venerid, Mercenaria "tridacnoides", from the Pliocene of the southeastern United States. Mercenaria "tridacnoides" is a very distinctive fossil (Fig.l). The large, heavy valves with conspicuous, broad undulations otherwise unknown in the genus Mercenaria, are widely

146 regarded as ~'abnormal" or "pathological" forms (Wilson, 1983). They occur together with the ~'normal" form, Mercenaria campechiensis, in coastal plain sequences of Yorktown age ranging from Virginia southward to Florida (Gardner, 1943; Stanley, 1986). Wilson (1983) has recently pointed out that to be taxonomically correct this species should be referred to as Mercenaria corrugata (Lamarck) and suggested the informal term Mercenaria corrugata "tridacnoides" for the striking variant under discussion here. Because the '~normal" form appears identical to modern Mercenaria campechiensis and because the name Mercenaria tridacnoides is so ingrained in the literature, we have elected to follow the usage of Stanley (1986) and employ the name Mercenaria "tridacnoides'" in this paper. The undulating shell margin and the large, thick valves of Mercenaria "tridacnoides'" prompted Seilacher (1985) to draw analogies with modern Tridacna and propose that Mercenaria "tridacnoides'" was a photosymbiotic host. He felt such shallow burrowing forms had been "lured" back to the surface (evolutionarily) as a result of the establishment of a photosymbiotic association. He envisioned the bivalve as having lived epibenthically in an orientation like that of Tridacna, with the undulating valve margins directed upward exposing mantle tissue to sunlight. An opposing viewpoint is held by S. M. Stanley (pers. comm., 1985, 1986) who believes the peculiar morphology of Mercenaria "tridacnoides" is the result of ecophenotypic variation and that in fact, Mercenaria ~'tridacnoides'" is conspecific with Mercenaria campechiensis. The controversy surrounding Mercenaria "tridacnoides" provided an opportunity to apply the growth line and stable isotope techniques discussed earlier along with the traditional criteria used to recognize photosymbiosis in fossil mollusks. The goal of the project was two-fold: (1) to resolve the controversy concerning the mode of life of Mercenaria "tridacnoides"; and (2) to evaluate the various criteria traditionally used to identify paleophotosymbiosis.

Specimens for this study came primarily from the richly fossiliferous Pliocene Pinecrest Beds of southwest Florida. The Pinecrest sands are exposed in a famous shell pit (APAC, Inc.; formerly Macasphalt, Inc.; Newburn Road or Warren Brothers Pit of earlier authors) located adjacent to interstate 1-75 south in Sarasota, Florida. The section has been described by Petuch (1982) and the fauna has been used by Stanley (1986) to investigate the Plio-Pleistocene extinction of western Atlantic bivalve mollusks. Shells of Mercenaria are among the most conspicuous fossils at this locality and hundreds of specimens along with other faunal elements were stratigraphically collected, cleaned, and housed for study in the Invertebrate Paleontology Collection of The Florida State Museum. Other specimens from Tar Heel, NC (Duplin Formation), collected by Mr. R. Jerry Britt, Jr., and Yorktown, VA (Yorktown Formation), from the museum collection, were also examined for comparative purposes. The following six lines of evidence were considered in addressing the question of paleophotosymbiosis in Mercenaria "tridacnoides": (1) Shell growth rate: Shells of both Mercenaria "tridacnoides" and M. campechiensis from the Pinecrest Beds possess prominent internal growth increments of the size and pattern that form annually in modern M. mercenaria (e.g. Kennish, 1980; Peterson et al., 1983) and M. campechiensis (e.g. Menzel, 1961; Saloman and Taylor, 1969). A polished radial section from umbo to shell margin reveals the alternating light and dark seasonal increments which then can be readily measured (see Jones, 1983, 1985). Thus it is possible to test for shell growth rate differences (as a proxy for calcification rate) between the two variants and determine if rates are abnormally higher in M. ~'tridacnoides". A subset of 100 of the better fossil specimens of Mercenaria campechiensis from Sarasota with both valves articulated were cleaned, sectioned, polished, and measured. The resulting size versus age plot is shown in Fig.3. The dashed curves represent a smoothed ±1 s.d. envelope about the mean growth curve for the

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100 measured specimens. Within the envelope are the means (dots) and + 1 s.d. errors bars for 50 specimens of M. "tridacnoides" of comparable preservation from the same site. It is clear from the overlap of the two curves t ha t little if any difference exists between the shell growth rates (and by implication the calcification rates) of the two forms. (2) Stable isotopes: Stable isotopic analyses were also performed on specimens of Mercenaria campechiensis and M. "tridacnoides" from the Sarasota shell pit. The specimens were recovered from the same horizon, within 0.3 m of one another, and each had both valves articulated, thus minimizing paleoenvironmental v a riatio n as much as possible. One valve from each specimen was selected and radiallysectioned along the axis of maximum shell height. Beginning at a shell height of 40 mm, the outermost shell material was ground off to avoid possible contamination. Next, 25 consecutive powdered CaCO3 samples were recovered

from the inner portion of the outer shell layer of each shell at a sampling interval of 2 mm using a 0.5 mm dental drill (see Jones et al., 1983 for techniques). This scheme yielded detailed samples spanning several years of shell growth in each specimen and so was sufficient to capture the range in yearly isotopic variation. Two or three samples were also recovered from the inner shell layer of each specimen to check for internal variability and consistency. All samples were roasted in vacuo for 1 hr at 380°C. X-ray diffraction analysis of powders before and after roasting confirmed t hat only aragonite was present. Individual samples analyzed according to standard techniques (Williams et al., 1977) were then reacted in vacuo with purified orthophosphoric acid at 60°C. Isotopic differences between the derived sample CO 2 and the PDB standard were determined with a VG Sira-24 mass spectrometer at the Stable Isotope Laboratory, Depart m ent of Geological Sciences, University of South Carolina, and are expressed in standard delta (5) not at i on (Epstein et al., 1953). Shown in Fig.4 is a carbon versus oxygen plot of the isotopic determinations from both

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Fig.4. Plot of carbon versus oxygen isotopic values for Mercenaria campechiensis (circles) and M. "tridacnoides" (triangles) from the Pliocene Pinecrest Beds of Sarasota, Florida.

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Mercenaria campechiensis (circles) and M. "tridacnoides" (triangles). The 51so values vary between about - 2 and ÷ 2 per mil while the 513C values plot between - 1 and ÷ 1%o. It is apparent from Fig.4 t h a t the two sets of values intermingle considerably and are not readily separable into distinct fields. Furthermore, there is no offset along the carbon axis as was noted for modern photosymbiotic Tridacna (Fig.2). Clearly both populations of fossil clams experienced the same set of environmental conditions and responded in a similar fashion. (3) Epibionts: The fossil shells at Sarasota do not normally occur in life position but instead represent concentrations potentially the result of several causes (see Kidwell et al., 1986). Therefore, the presence of epibionts on the shells may be used to help reconstruct original orientations. Fig.5A depicts one example of many specimens of Mercenaria "tridacnoides"

collected with barnacles and small serpulid worm tubes encrusting the posterior margin of the shell. The restriction of such epibionts to this region of the shell suggests the clams lived burrowed to a shallow depth with only the posterior-most tip of the shell exposed above the surface (Fig.5B) and not like modern Tridacna. Extensive collecting of Mercenaria campechiensis along Florida's west coast reveals that such partially-exposed life-positions are commonly adopted by this species today. (4) Corrugation continuum: The valves of fossil Mercenaria from the Sarasota locality are not clearly separable into two discrete populations having either straight (M. campechiensis) or highly corrugated (M. "tridacnoides') commissure lines. Instead, a continuum exists ranging from straight (the "normal" and numerically most abundant variety) to slightly undulatory, to zig-zag (Fig.6A, B). The full

Fig.5. Epibionts on Mercenaria "tridacnoides" (UF 11149). A. Left valve with barnacles and serpulid tubes restricted to posterior margin. Shell length = 134 mm. B. Reconstruction of life position with posteriormost portion of valves exposed.

149

Fig.6. Fossil and modern specimens of Mercenaria showing variation in undulatory nature of the valve margins. A, B. Pliocene specimens from Sarasota, Florida with slightly undulatory (A, shell length=141 ram, UF 11151) to strongly undulatory (B, shell length= 140 mm, UF 11150) commissure. C, D. Analogous modern specimens of M. campechiensis captured live in Charlotte Harbor, Florida (C, shell length= 95 mm, UF 110565; D, shell length = 76 mm, UF 110566).

s p e c t r u m of m o r p h o t y p e s m a y be f o u n d coo c c u r r i n g at the s a m e horizon. F u r t h e r m o r e , a n a n a l o g o u s p a t t e r n of v a r i a bility h a s b e e n d i s c o v e r e d a m o n g m o d e r n p o p u l a t i o n s of Mercenaria campechiensis f r o m c o a s t a l Florida. S p e c i m e n s w e r e r e c e n t l y collected at m o n t h l y i n t e r v a l s b e t w e n M a r c h 1986 a n d M a r c h 1987 f r o m s e v e r a l s u b - p o p u l a t i o n s w i t h i n C h a r l o t t e H a r b o r , s o u t h w e s t Florida, in a s t u d y a s s e s s i n g s e a s o n a l i t y of g r o w t h increm e n t f o r m a t i o n . D u r i n g this c o l l e c t i n g ~ffort, it was d i s c o v e r e d t h a t a small percent~.ge of each month's catch (typically 3 - 5 0 ) had an u n d u l a t i n g c o m m i s s u r e line w h i c h c o u l d v a r y f r o m slightly to h i g h l y u n d u l a t o r y (Fig.6C, D).

T h e s e s p e c i m e n s s h o w e d no e v i d e n c e of i n j u r y or shell repair, w e r e in good p h y s i o l o g i c a l c o n d i t i o n w h e n c a p t u r e d , a n d did n o t c o n t a i n p h o t o s y m b i o t i c algae. T h e y lived b u r r o w e d to s h a l l o w d e p t h s in the s t a n d a r d o r i e n t a t i o n of the o t h e r s p e c i m e n s of Mercenaria a m o n g w h i c h t h e y w e r e found. S u c h a v a r i a b i l i t y c o n t i n u u m a r g u e s a g a i n s t r e c o g n i t i o n of two d i s t i n c t species o c c u p y i n g different niches, e i t h e r a m o n g the fossil or m o d e r n specimens. (5) Paleolatitudes and paleoenvironments: Mercenaria "tridacnoides'" is k n o w n to h a v e i n h a b i t e d c o a s t a l P l i o c e n e seas f r o m F l o r i d a n o r t h w a r d t h r o u g h the C a r o l i n a s a n d into V i r g i n i a ( G a r d n e r , 1943; C a m p b e l l et al., 1975).

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This broad latitudinal distribution extended from warmer, semitropical zones in the south to cooler, temperate waters in the north, well out of the range of reef environments existing at the time. Also, M. "tridacnoides" occurs in largely clastic units (e.g. Yorktown, Duplin, Pinecrest) composed of sands, silts, and clays of terrigenous origin. The sedimentological evidence argues against excessive water clarity so that an hypothesis of photosymbiosis must be questioned on both paleolatitudinal and paleoenvironmental grounds. It should be noted that not all modern photosymbiotic hosts are confined to low latitudes (e.g. temperate zone anemones) or to environments free of clastic input (e.g. Fragum). Nevertheless, the habitat generalizations expressed here are valid for most calcifying photosymbiotic organisms (Cowen, 1983). For this reason the habitat argument is included with the observation that it is consistent with the other lines of evidence but perhaps not as definitive. (6) Gape: Stanley (1970, pp. 29, 30) showed by graphic analysis that for a given angle of shell opening, a simple zig-zag or wavy commissure (like t h a t of Mercenaria "tridacnoides") produces no greater area of gape than if the commissure were planar. Rudwick (1964) had pointed this out earlier for zig-zag commissures in brachiopods. To increase their gape area, many species of Tridacna have sacrificed complete closure with pointed projections of the valve margins which are narrower t h a n the corresponding embayments on the other valve into which they fit (Stanley, 1970). Thus, with the tightly-closing valve margins of M. "tridacnoides", there is no compelling reason to postulate a photosymbiotic relationship, zigzag commissure notwithstanding. Discussion

The stable isotopic data of Fig.4 show no evidence of dissimilar fractionation patterns between the carbon records of Mercenaria campechiensis and M. "tridacnoides". Therefore, these data do not support the photosym-

biosis hypothesis for M. "tridacnoides". In a similar fashion, the shell growth increment data indicate no difference in the shell growth rates between the two forms. These data also do not support an hypothesis of symbiosis. From these analyses and the other arguments cited above, we conclude t h a t M. "tridacnoides" was not photosymbiotic. Cowen (1983) has stated that one can never prove the presence of algal symbionts in a particular fossil taxon, only show that an hypothesis of symbiosis has survived a number of tests, any of which could have destroyed the hypothesis. The six independent lines of reasoning presented in the previous section appear sufficient to disprove the hypothesis of Seilacher (1985) that Mercenaria "tridacnoides'" possessed algal symbionts and lived in a fashion analogous to modern Tridacna. After evaluating the evidence in the case of Mercenaria "tridacnoides" as well as considering some of the peculiarities of modern photosymbiotic bivalves, it seems clear that analytical techniques such as growth increment and stable isotope analyses can be very useful in testing for paleophotosymbiosis. Yet, a survey of the literature reveals t h a t neither technique is normally applied in this context. One notable exception is the recent study by Accorsi Benini (1985) of the large Liassic bivalves, Lithiotis, Cochlearites, and Lithoperna, in which growth lines were used to suggest t h a t the large shell sizes were a result of average growth rates over a long life rather than a result of symbiont-induced rapid calcification rates. It is important to recognize that none of the criteria traditionally used to identify photosymbiotic host taxa are completely diagnostic, even when properly interpreted. We saw earlier that many bivalves which were rapid calcifiers and achieved large sizes lacked symbionts while small forms with rather typical shells such as Fragum were photosymbiotic. Translucent ~'windows" such as those found in the shell of Corculum are obviously designed to facilitate light transmission. Yet, if found in an extinct mollusk, a case of photosymbiosis is

151 n o t a s s u r e d as s i m i l a r l i g h t - t r a n s m i t t i n g s p o t s o c c u r i n m o d e r n l i m p e t s k n o w n to l a c k z o o x a n t h e l l a e ( L i n d b e r g et al., 1975). A p p a r e n t l y t h e s p o t s of t h e s e l i m p e t s h e l l s c o n d u c t l i g h t w h i c h produces a strong negative phototaxis. Paleoe n v i r o n m e n t a l criteria are also complicated. D e s p i t e c o n v e n t i o n a l w i s d o m f a v o r i n g w a t e r of h i g h c l a r i t y a n d r e e f a l e n v i r o n m e n t s for p h o t o s y m b i o s i s , Fragum fragum a n d F. unedo, "... live not on a c t u a l reefs b u t on r a t h e r m u d d y s a n d flats ..." ( K a w a g u t i , 1983, p. 17). T h e s e e x a m p l e s u n d e r s c o r e t h e n e e d to e m p l o y as m a n y c r i t e r i a as p o s s i b l e w h e n e v a l u a t i n g a n h y p o t h e s i s of photosymbiosis. If a l l e v i d e n c e p o i n t s to t h e s a m e g e n e r a l c o n c l u s i o n as i n t h e c a s e of Mercenaria "tridacnoides" a b o v e , t h e n a h i g h d e g r e e of c o n f i d e n c e c a n be a t t a i n e d . T h e s e e x a m p l e s a l s o e m p h a size t h e n e e d :for o t h e r c r i t e r i a s u c h as s t a b l e i s o t o p e a n a l y s e s w h i c h c a n be i m p o r t a n t i n those instances when traditional criteria yield ambiguous conclusions. Studies in progress on t h e i s o t o p i c s y s t e m a t i c s of o t h e r m o d e r n p h o t o s y m b i o t i c m o l l u s k s ( J o n e s , i n prep.) w i l l g a u g e h o w g e n e r a l l y t h e "Tridacna m o d e l " of J o n e s et al. (1986) m a y be a p p l i e d . H o p e f u l l y t h i s approach will provide an important criterion to be u s e d i n c o n j u n c t i o n w i t h u s u a l t e c h n i q u e s in r e c o g n i z i n g p h o t o s y m b i o s i s a m o n g fossil m o l l u s k s .

Acknowledgements W e t h a n k A. S e i l a c h e r for i n i t i a l l y s u g g e s t i n g t h e i s o t o p i c i n v e s t i g a t i o n of M. "tridacnoides". A t v a r i o u s p o i n t s i n t h i s s t u d y we have benefited from conversations with Druid Wilson, Dave Jacobs, and especially Steven Stanley. For assistance in collecting specimens we t h a n k R. J e r r y B r i t t , Jr., E r n e s t a n d E v e l y n Bradley, and Roger Portell. Mary Ann Kovarik sectioned and measured many specimens while Wendy Zomlefer provided the artwork. Figured specimens are deposited in the Invertebrate P a l e o n t o l o g y (fossil s h e l l s ) or M a l a c o l o g y ( m o d e r n s h e l l s ) c o l l e c t i o n s of t h e F l o r i d a S t a t e Museum. This article represents Florida State M u s e u m C o n t r i b u t i o n to P a l e o b i o l o g y no. 318.

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