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A Thesis Submitted to the Faculty of San Francisco State University in Partial Fulfillment of the Requirements for the Degree

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A Thesis Submitted to the Faculty of San Francisco State University in Partial Fulfillment of the Requirements for the Degree THE BEHAVIORAL ECOLOGY OF THE SCAPHOPOD MOLLUSC CADULUS ABERRANS: BURROWING MECHANISM AND RHYTHMICITY A thesis submitted to the faculty of San Francisco State University in partial fulfillment of the requirements for the degree Master of Science in Marine science by Jenifer Lynn Levitt san Francisco, California December, 1990 THE BEHAVIORAL ECOLOGY OF THE SCAPHOPOD MOLLUSC CADULUS ABERRANS: BURROWING MECHANISM AND RHYTHMICITY Jenifer Lynn Levitt san Francisco State University 1990 ABSTRACT The burrowing mechanism of Cadulus aberrans (Whiteaves) was studied to explain the mechanism by which this infaunal mollusc can burrow despite considerably less foot musculature than other infaunal molluscs. circadian burrowing rhythms and changes in burrowing depth measured at various times of the year are also described. Locomotion is described from observations of foot movement in seawater, and burrowing in submerged, sediment-filled, narrow aquaria • .Q. aberrans, unlike other burrowing molluscs, extends its foot by eversion. As the tubular foot is everted it is inserted into the sediment. Foot elongation involves hydraulic movement of hemocoelic fluid and not seawater. After complete elongation the distal pedal disk flares and establishes an anchorage. Contraction of four longitudinal pedal retractor muscles pulls the shell down over the foot. Complete burial, one body length, is accomplished in approximately 3 seconds. Cadulus aberrans burrows deeply, and extensively in the laboratory and in nature. This life style contradicts the generalizations from studies of Dentaliumspp. that scaphopods are only superficial burrowers. Time-lapse observations of burrowing were recorded on video tape and revealed a cycle of daily burial and nightly emergence. Burrowing depth was quantified by removal of scaphopods from six replicate, experimental aquaria in 4 em strata, over 1 1/2 years. Burrowing depth varied, sometimes animals were found throughout the depth strata to the greatest depth of 20 em. At other times most animals were within 4 em of the sediment surface. A possible explanation for the two burrowing trends is correlation with periods of gametogenic activity; shallow burrowing may occur during periods of high gametogenic activity. However not all data support this hypothesis. ~- aberrans was found throughout a 46 em deep box core from Monterey Bay, California, also indicating deep burrowing. I certify that the Abstract is a correct representation of the content of this thesis. [~ h...... ~ n- "-1- '"to Thomas M. Niesen Date (Chair, Thesis Committee) ACKNOWLEDGEMENTS Many people have contributed time, expertise and equipment to this endeavor. Drs. T. Niesen, M. Foster and w. Gilly were kind enough to sit on my thesis committee and guide me through the thesis process. Dr. R. Shimek provided insightful information about scaphopods. G. Steiner edited a draft. Several of my peers at Moss Landing Marine Laboratories helped with scaphopod sampling and sorting, particularly J. Wolgast and E. Sawyer. s. Baldridge and s. O'Neil were instrumental in locating reprints. Dr. J. Nybakken introduced me to the study of mollusks. M. Sylvan, of ucsc, greatly helped with data interpretation and statistical analyses. After the earthquake in october 1989, I found myself without a lab, functional experimental enclosures, or a desk, and with all my lab possessions packed in boxes in a warehouse. At this time it was the faculty and staff of the Hopkins Marine station who made it possible for me to continue working. In particular I wish to thank Judy Thompson for allowing me use of the water tables, and Bruce Hopkins for paving the way toward working in Gilly's lab and for continuously helping me with problems as they arose. Dr. w. Gilly provided desk and lab space, supplies, and guidance. M. and J. Lucero and F. Horrigan helped with inspiration, technical assistance and an occasional pizza. Dr. D. Mazia and c. Patton provided the time-lapse video equipment. Last and perhaps most importantly, Ilene Meyers, my mother, provided emotional support and helped me with literature searches. I whole heartily thank all these people and many others who contributed directly and indirectly to this thesis. This work has taught me not only about scaphopods but the joy and necessity of cooperation. Financial support was provided by the Myers Oceanographic and Marine Biology Trust and the Santa Barbara Shell Club. vi TABLE OF CONTENTS List of Figures ..................................... viii List of Tables ........................................ ix Chapter 1. The Mechanism of Locomotion Introduction ........................................... 1 Methods ................................................ 2 Results ................................................ 4 Discussion ............................................ 10 Chapter 2. Burrowing Rhythmicity Introduction .......................................... 15 Methods ............................................... 16 Results ............................................... 21 Discussion ......................................•.•... 3 3 Literature Cited ..•................................... 3 8 Vll LIST OF FIGURES Figure Page 1. Pedal Everson ..................... 6 2. Pedal Retraction .................. 7 3 . Burrowing Sequence ................ 9 4. Distributions in Ant Farms ........ 24 5. Time of Emergence ................. 30 6. Surface-stay Duration ............ 30 7. Distribution in Box Core .......... 3 2 viii LIST OF TABLES Table Page 1 . Burrowing Depth summary ••.••.•... 2 6 ix 1 Chapter 1 THE MECHANISM OF LOCOMOTION INTRODUCTION Molluscan burrowing through soft substrates usually combines muscular contraction with hydraulic hemocoel expansion (Trueman, 1969, 1975). Burrowing has been described for many bivalves, gastropods, and the scaphopod Dentalium. The bivalves use a combination of four muscle groups, circular, longitudinal, oblique, and adductor, and movement of both seawater and hemocoelic fluid to penetrate the substrate (Trueman et al., 1966; Trueman and Brown, 1985; Trueman, 1968a). Most burrowing gastropods use a variety of muscle groups and hemocoelic spaces, ranging from pedal plows to lobed cephalic shields (Brown, 1964; DeFresse, 1989), to form thrustable insertion appendages and expandable anchors. Other gastropods combine hydraulic-muscular mechanisms with ciliary movement or muscular pedal waves (Trueman, 1968b). Scaphopods in the order Dentaliida have a protrusible, muscular foot similar to the bivalves. The foot is equipped with longitudinal, circular and transverse muscles, that hydraulically erect epipodial lobes to form an anchorage in the substrate (Trueman 1968c). These scaphopods are shallow burrowers (Morton, 1959). The foot of scaphopods in the order Gadilida is considerably less muscular than those of the other burrowing molluscs. It contains two paired longitudinal muscles and lacks circular or other musculature, being predominantly a 2 longitudinally expandable hemocoel (Petitte-Fischer & Franc, 1968). Despite this muscular disadvantage, Cadulus aberrans has been found burrowing as deep as 30 em in its natural environment (Shimek, 1989, 1990), was found near the bottom of and throughout a 46 em deep box core sample (from Monterey Bay, California, 60 m water depth), and frequently burrowed to and from the bottoms of 20 em deep aquaria in the laboratory (personnel observation) . Here I describe the gadilid foot as observed in Cadulus aberrans and the mechanism of locomotion that allows this scaphopod to burrow to these depths. METHODS cadulus aberrans and the sediments in which they were found were collected using a Smith-Mcintyre grab in Monterey Bay, California (three kilometers off-shore from the Pajaro River in 60 m water depth). Other infauna were removed by washing the sample over a 1 mm mesh screen then sorting under a dissecting microscope. Both scaphopods and sediment were maintained in the laboratory where behavioral observations were made. Scaphopod movement was observed in finger bowls containing natural seawater. Back lighting, from beneath the bowl, allowed simultaneous observation of events within the translucent shell and at each aperture. A thin layer of sediment placed in the bowl (approximately 5 mm thick) allowed recording of burrowing initiation. McCormick blue 3 food coloring (McCormick Research & Development Labs, Hunt Valley, MD) mixed with seawater was injected next to active scaphopods to look for fluid flow between the mantle cavity and hemocoel . After each collection, the newly collected scaphopods were placed in experimental "ant-farms" (described in detail in chapter 2). Animals placed on the sediment immediately burrowed. Behavior was observed on the surface of and within sediment in these narrow, ant-farm style enclosures, placed in aquaria with continuous flowing sea water. All behavior was studied both by direct observation and video. The video equipment consisted of a Panasonic TV camera (model WV-lOOOA) and a Betamax video cassette recorder (model SL-2700). The image was observed simultaneously on a Panasonic video monitor (model TR-930). Burrowing is usually described in steps (Trueman, 1975) and the procession of steps constitutes a 'digging cycle.' 'Digging period' refers to the duration of burrowing activity from the initiation of activity until a stable position is reached and burrowing ceases. Pedal hemocoel volume (within the shell) and the volume of the fully extended foot were calculated to determine the volume of fluid needed to evert the
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