Photosymbiosis in Clinocardium Nuttalli: Implications for Tests of Photosymbiosis in Fossil Molluscs Author(S): Douglas S
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Photosymbiosis in Clinocardium nuttalli: Implications for Tests of Photosymbiosis in Fossil Molluscs Author(s): Douglas S. Jones and David K. Jacobs Source: PALAIOS, Vol. 7, No. 1 (Feb., 1992), pp. 86-95 Published by: SEPM Society for Sedimentary Geology Stable URL: http://www.jstor.org/stable/3514798 Accessed: 23/02/2010 16:24 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=sepm. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. SEPM Society for Sedimentary Geology is collaborating with JSTOR to digitize, preserve and extend access to PALAIOS. http://www.jstor.org 86 RESEARCHLETTERS I environmental correlates such as shallow, clear water in nutrient-poor, low latitude, reefal settings. When Photosymbiosis in these characteristics appear in fossil contexts, cases of symbiotic associa- Clinocardium nuttalli: tions are frequently inferred. This for Tests of approach has proven only moderate- Implications ly satisfactory, however, and has of- Photosymbiosis in Fossil Molluscs ten led to ambiguity (see Jones et al., 1988). The principal objective of this paper is to evaluate the traditional criteria used to identify molluscan photosymbiotic hosts in the fossil record. This evaluation is accom- DOUGLAS S. JONES photosymbiotic relationship of C. plished through: 1) an examination Florida Museum of Natural History, nuttalli (and other photosymbiont- of photosymbiosis in the modern University of Florida, bearing bivalves) contradict ecolog- heart cockle (Clinocardium nuttal- Gainesville, FL 32611 ical, morphological,geochemical, and li); and 2) a re-analysis of the tradi- life history characteristics tradition- tional criteria in light of the Clino- DAVID K. JACOBS1 ally used to recognize such associa- cardium results as well as recent work Department of Geological Sciences, tions in the fossil record. While these involving other photosymbiotic mol- Virginia Polytechnic Institute and characteristics remain valid as sup- luscan species. State University, porting arguments for suspected The heart cockle, Clinocardium Blacksburg, VA 24061 cases of paleophotosymbiosis, pale- nuttalli (Conrad, 1837), is widely dis- ontologists are cautioned that nu- tributed in littoral settings from San merous photosymbiotic taxa do not Diego, California, north to the Nu- PALAIOS, 1992, V. 7, p. 86-95 display these characteristics and nivak, Pribiloff, and Commander Is- hence many cases of paleophoto- lands, and south in the eastern Pa- The endosymbiotic association be- symbiosis probably go undetected. cific to Japan (Fraser, 1931). Although tween the heart cockle, Clinocar- Paleontologists are encouraged to it is of limited commercial signifi- dium nuttalli, and an endosymbiotic develop better criteria for recogniz- cance, this shallow burrower is com- green alga (zoochlorella) was inves- ing photosymbiotic molluscan hosts. monly collected by recreational clam tigated in the field and laboratory. diggers from intertidal sandy mud Specimens were obtained from False flats and sand beaches throughout its Bay, San Juan Island, Washington. INTRODUCTION range. Clinocardium nuttalli is also Infaunal clams did not contain sym- one of a small but growing number bionts while slightly larger and older Identifying photosymbiotic rela- of molluscan species that has been semi-infaunal individuals harbored tionships in the fossil record is prob- reported to harbor endosymbiotic al- algae in siphonal and mantle tis- lematic because the symbionts are not gae (Hartman and Pratt, 1976); it is sues. Epifaunal clams were the larg- preserved, nor do they produce iden- this relationship that is of particular est and oldest (up to six years old) tifiable structures in the hard parts interest here. and contained the greatest concen- or skeleton of the host (Cowen, 1983). Algae and chloroplast symbionts tration of algae. The three mode-of- Because direct evidence of such re- are known from only two modern life groups apparently represent an lationships is lacking, indirect crite- molluscan classes, the bivalves and ontogenetic continuum with pro- ria (i.e., analogies with modern taxa) the gastropods. Three types of sym- gressive emergence from the sub- are traditionally used to argue for bionts are involved: 1) zoochlorellae strate related to the acquisition of suspected cases of photosymbiosis. (Chlorophyceae, Chlorocaccales); 2) algal symbionts after the clams' sec- These arguments have been applied zooxanthellae (Dinophyceae, Peridi- ond year of life. No symbiont-in- to diverse taxa, but especially to fos- niales); and 3) free chloroplasts (de- duced effects were observed on either sil molluscs. rived from several plant orders) shell growth rates or on oxygen and Selected ecological, morphological, (Muscatine and Greene, 1973). En- carbon isotopic composition of shell geochemical, and life history char- dosymbiotic chloroplasts occur in carbonate. Several aspects of the acteristics have been associated with several species of marine, hermaph- modern photosymbiotic molluscan roditic snails of the order Sacoglossa hosts. Among these are: 1) special- (Gastropoda,Opisthobranchia). More ized which enhance 1Present address: Department of Inverte- morphologies familiar are the endosymbiotic algae brates, American Museum of Natural His- light exposure; 2) rapid calcification (dinoflagellates) known as zooxan- tory, Central Park West at 79th St., New producing large skeletal sizes; 3) frac- thellae. These occur among a wide York, NY 10024. tionation of carbon isotopes; and 4) range of opisthobranchs, but are best Copyright? 1992, SEPM (Society for SedimentaryGeology) 0883-1351 /92/0007-0086/$3.00 PHOTOSYMBIOSISIN FOSSIL MOLLUSCS 87 known for their sustained, intimate association with bivalves of the su- perfamily Cardiacea, particularly the family Tridacnidae (Muscatine and Greene, 1973). Associations involving zoochlorel- lae are generally less familiar than the other two groups and often in- volve algae which become parasitic (Muscatine and Greene, 1973). The term "zoochlorellae" has no real tax- onomic significance and has tradi- tionally been used to refer to those green algae found as endosymbionts in freshwater invertebrates (Trench, 1979). For example, zoochlorellae are known from the freshwater bivalves Anodonta cygnea and Unio picto- rum where they are confined to the tissues that receive maximum illu- mination, such as the posterior man- tle edge, siphons, and occasionally the FIGURE1 -Map of northwesternWashington with expanded view of San Juan Island(inset) foot. Zoochlorellae have also been indicating location of Friday Harbor Marine Laboratory and collection site of Clinocardium identified in marine molluscs. They nuttalliat False Bay. were reported as mantle endosym- bionts in the giant scallop, Placopec- ten magellanicus (Naidu and South, ognize such relationships in the fossil subset of both mantle and siphonal 1970; Naidu, 1971), and more re- record are re-evaluated in the dis- tissues containing symbionts was se- cently as endosymbionts in the man- cussion that follows. lected for examination by transmis- tle, siphon, and occasionally the foot sion electron microscopy (TEM) to of the heart cockle, Clinocardium MATERIALS AND METHODS investigate the nature of the symbi- nuttalli (Hartman and Pratt, 1976). ont in more detail. These tissues were In general, these associations involv- Individuals of Clinocardium nut- pre-fixed in 3% buffered glutaral- ing zoochlorellae have not been in- talli were collected by hand from the dehyde at the FHML and were later vestigated as extensively as those in- lower intertidal zone at False Bay, dehydrated, sectioned, and stained volving other algal endosymbionts. San Juan Island, Washington (Fig. according to standard techniques. The intimacy of algal-molluscan 1). Specimens came from the fine sand The TEM analyses were performed symbiotic associations varies from and silt tidal flat environment, within on a JEOL 100C instrument at facultative to obligate and from tran- about 0.3 m of mean low water. Clams VPI&SU, Blacksburg, Virgina. To sient to sustained. In most cases the with and without algal symbionts further aid in the identification of the relationships are presumed to be mu- were collected. The former were rec- algal symbiont, tissues were stained tualistic with the host benefitting ognized in the field by the green color for the presence of starch using Lu- from symbiont-derived photosyn- of the siphonal region, or in the case gol's solution. thates released inside its tissues. The of epifaunal individuals, by the The soft tissue