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Home , Fusitriton, Fusitriton oregonensis, Gastropod shell

SHORT PAPERS AND NOTES

BULLETIN OF MARINE SCIENCE, 31(4): 916-921,1981

PERIOSTRACUM OF THE GASTROPOD PUSITRITON OREGONENSIS: NATURAL INHIBITOR OF BORING AND ENCRUSTING ORGANISMS

David J, Bottjer

ABSTRACT The gastropod oregonensis has a thick, hairy , which inhibits set- tling and growth of many borers and epizoans, This inhibitory effect could contribute to the 's energetic efficiency by reducing energy utilized for repair of shell destruction caused by borers, and by reducing weight of encrusters carried during movement. Similarly, this deterrent to borers, and hence to shell weakening, could aid in resistance to predators which break the shell. Knowledge gained from studies of encruster inhibitor properties in molluscs may lead to development of a superior antifouling system.

The primary function of gastropod periostracum is to aid in secretion of the gastropod shell (Clark, 1976), However, gastropod periostracum commonly shows great structural variety, much of which may have secondary functions distinct from the process (Bottjer, 1977). A widely accepted notion is that thick gastropod periostracum functions as protection for the calcified shell against dissolution by acidic waters and boring organisms (Clark, 1976; Abbott, 1968). However, no detailed studies have been made to document secondary functions of gastropod periostracum. (Redfield), a mobile, predatory marine gastropod of the family (Smith, 1970), is characterized by a relatively thick, hairy periostracum. Thick periostracum with systematically-spaced hairs is common in cymatiids (Clench and Turner, 1957; Lewis, 1972). Preliminary observations of F. oregonensis recovered from dredge hauls revealed that many specimens had lost all or some of their periostracum, and that shell portions without periostracum seemed to have a greater number of borings and epizoans than those with intact periostracum (Fig. m,C). Subsequent investigations led to the evidence pre- sented in this report, which demonstrate that the thick, hairy periostracum of F. oregonensis functions to significantly inhibit the settling and growth of many epizoans with relatively large calcareous skeletons, as well as many borers that penetrate calcareous substrates. This inhibiting effect may contribute to increased energetic efficiency and increased resistance to predators for F. oregonensis.

MATERIALS AND METHODS

Fusitriton oregonensis, which dates back at least to the early Pliocene (Smith, 1970), has a recent geographic range around the northern Pacific from southern California to to northern Japan (Smith, 1970). It occurs from the intertidal to depths of 2300 m (Smith, 1970) on soft and hard substrates. Thirty F. oregonensis were dredged from the shallow subtidal (3 m) to the deep subtidal (200 m) around San Juan Island, Washington. These specimens were examined for shell surface type (three qualitatively determined types of periostracum and bare shell surface), as well as boring and epizoal organisms. F. oregonensis periostracum (Fig. I) is secreted in strips up to 4 mm wide laid overlapping like shingles towards the ; cumulative thickness of imbricated strips is generally

916 SHORT PAPERS AND NOTES 917

c

Figure I. Fusilrilon oregonensis shell surface types: A, Photomicrograph of surface of F. - ensis periostracum, showing oblique view of imbricated periostracal strips and portions of two rows of hairs; periostracal strips partially covered by sediment. Note bushy calcareous bryozoan just below upper right corner; B, F. oregonensis covered almost completely by periostracum, but with and several adapical whorls lost due to destruction by borers; C, F. oregonensis covered partially by periostracum, encrusted by Balanus crenalllS, and with apex and several adapical whorls lost due to destruction by borers. Scale for A = 1 mm; B-C = 4 em.

1-2 mm. Hairs, up to 7 mm long, extend systematically from these strips, taper from base to distal point, and form rows spaced at 1-7 mm which are oriented perpendicular to the plane of the aperture. Examined periostracum types include non-eroded, partially eroded with some hairs missing, and well- eroded with most hairs missing. Examined specimens include those naturally missing most periostracum, those with an almost full cover of periostracum, and those missing periostracum on the apex. Ninety degree rotations of whorls from the aperture to the apex (quarter whorls) were used as the basic examined units. Data from presence or absence of encrusting and boring organisms for each shell surface type on each quarter were compiled. These data were then computed as percent occurrence of the organism for each shell surface type in all the quarter whorls (Fig. 2). This admittedly normalizes the data to give the appearance that each portion of examined periostracum or bare shell had the same area. However, the results shown, although not reflecting absolute abundance, appear to accurately reflect abundance of epizoal and boring organisms among shell surface types. Terminology associated with the various processes of hard substrate penetration is currently un- settled (Warme and McHuron, 1978). In this paper "boring," "borings," and "borers" refer to all 918 BULLETIN OF MARINE SCIENCE, VOL, 31, NO, 4,1981

NON- ERODED PARTIALLY-ERODED WELL- ERODED BARE SHELL PERIOSTRACUM N"BO PERIOSTRACUM N~B3 PERIOSTRACUM N~ 122 SURFACE

75

A 50

75

B 50

25

e 9 10 II 12 13 14 15 16 17 18 8 9 10 II 12 13 14 15 16 17 18 e 9 10 II 12 13 14 15 16 17 18 8 9 10 II 12 13 14 15 16 17 18

75

c 50

25

19 20 19 20 1920 1920 Figure 2. Distribution of epizoans and borers on Fusitriton oregonensis shell surface types. N is the number of occurrences of each shell surface type from the examined quarter whorls, A, Distri- bution of Group t organisms; includes I-saccamminid Foraminifera, 2-terebellid worm tubes, 3-sa- bellid worm tubes, 4-ascidians, 5-bushy calcareous bryozoans, 6-juvenile bivalves, 7-Sahel/aria worm tubes; B, Distribution of Group 2 organisms; includes 8-spionid worm borings (other than Polydof{/), 9-encrusting sponges, to-algal borings and grooves, II-the barnacle Balanus crenalus, 12-hydroids, I3-Spirorbis worm tubes, 14-serpulid worm tubes (other than Spirorhis). 15-clionid sponge borings, 16-encrusting red algae, 17-Polydof{/ worm borings, 18-the gastropod adunca; C, Distri- bution of Group 3 organisms; includes 19-encrusting bryozoans, 20-. Epizoans with non- mineralized skeletons include 4 and 12, those with lightly mineralized skeletons include 5 and 9, and those with completely mineralized (calcified) skeletons include I, 6, II, 13, 14, 16, 18, 19, and 20, Skeletons composed of sand-grain and shell-fragment aggregates held together by organic cements include 2,3, and 7.

organisms and their excavations which penetrate hard substrates, except those organisms and their excavations caused by drilling into shells in order to devour the contents (done by some gastropods, octopus, and perhaps members of other groups). Excavations by these shell-drilling organisms are herein termed "predatory borings."

RESULTS The boring and epizoan fauna can be divided into three groups (Fig. 2): (1) organisms that become less common as the periostracum deteriorates; (2) organ- isms that become more common as the periostracum deteriorates, or which are limited to bare shell surfaces; and (3) organisms which show no change in oc- currence between shell surface types. Group] (Fig. 2A) is composed of epizoans with either non-mineralized, lightly mineralized, or completely mineralized skel- etons, as well as skeletons composed of sand-grains and shell-fragment aggregates held together by organic cement. Observations on occurrence for these epizoans show that they use hairs of the periostracum for attachment (worms, ascidians), as "protection" from mechanical disruption by growing amongst them (saccam- minids), and become less common as the hair is eroded off. Epizoans with com- SHORT PAPERS AND NOTES 919 pletely mineralized skeletons are relatively small (juvenile bivalves, saccammin- ids). Although Group 2 (Fig. 2B) contains epizoans with non-mineralized and lightly mineralized skeletons, it is composed primarily of relatively large epizoans with completely mineralized (calcified) skeletons, and borers that penetrate calcareous substrates. Lack of a suitable substrate caused by presence of the soft, hirsute periostracum apparently inhibits settling and growth of these organisms. Group 3 (Fig. 2C) includes encrusting bryozoans and brachiopods. The en- crusting bryozoans are equally facile at encrusting hairs and bare shell surfaces. Brachiopods also attach to both periostracum and bare shell. To check for presence of borings under the periostracum, six of the previously examined Fusitriton oregonensis (all generally with non-eroded periostracum), were stripped of periostracum by immersion in a sodium hydroxide solution. Careful examination revealed patches of branching borings I to 2 ILm in diameter that appeared to be fungal (Golubic et aI., 1975), with no apparent apertures to the surface. Presence-absence data were compiled for twenty-three quarter whorls and percent presence computed as 63%. Boring fungids feed on the organic ma- terial in the shell (Golubic et aI., 1975) and have little or no communication with the shell exterior. The fungids may have reached the shell by first penetrating the periostracum. In any case, their contribution to destruction of the shell (outer 1- 2 ILm where they densely populate the shell) is minimal, and is several orders of magnitude less than that caused by spionid worms, c1ionid sponges, or algal grooves and borings. As mentioned previously, many Fusitriton oregonensis are found naturally without periostracum. Careful examination shows that they once had periostra- cum, for patches are commonly found in protected areas on the shell surface. Loss of periostracum appears to have been caused by abrasion during movement, as well as erosion by growth of attached barnacles. When settling on F. oregon- ensis, a Balanus crenatus generally survives only if it is on a hard shell surface. If this is a small patch of bare shell from which the periostracum has been eroded, the barnacle, as it grows outward, intrudes under the surrounding periostracum. This creates loose pieces of periostracum, which initiates further periostracum removal by abrasion during ordinary daily movement of the snail.

DISCUSSION AND CONCLUSIONS This is not the first report of a capacity in marine molluscs for inhibition of borers and encrusters. Scanland (1979) and Bottjer and Carter (1980) both dem- onstrated that bivalve periostracum can inhibit the settling and growth of borers and encrusters. In addition, Heptonstall (1970) suggested that the periostracum of the cephalopod Nautilus inhibits infestation by encrusters and borers. Various other mechanisms that inhibit borers and encrusters are widespread amongst . These have been summarized by Jackson (1977), and in- clude tentacles and nematocysts of cnidarians, avicularia of ectoprocts, and tox- icity of ascidians, cnidarians, and sponges. Secretion of such a periostracum may be energetically efficient: it leads to minimization of energy used for repair of shell destruction caused by borers (Fig. IB,C), and reduces the potential weight caused by encrustation (Fig. lC), thereby minimizing energy utilized in movement. In addition, reduction of shell weakening due to effects of borers could aid in deterring predators of Fusitriton oregonensis which break the shell, such as Cancer productus, the red rock crab (Vermeij, 1978). 920 BULLETIN OF MARINE SCIENCE, VOL. 31, NO.4, 1981

Specimens of Fusitriton oregonensis fresh from dredge hauls commonly are coated with a thin layer of sediment trapped by the hairy, irregular surface of the periostracum. This sediment layer may inhibit borers and epizoans, which need a stable substrate upon which to settle (Grant, 1966). Possibly, this trapping is the main function of the hairs. Alternately, the periostracal hairs may directly inhibit settling of borers and epizoans, much like the artificial surface described by Barnes and Powell (1950), whereby the barnacle Balanus crenatus and the serpulid worm Pomatoceros triqueter preferentially avoided growing on a surface densely covered with 1 mm long hairs. Although polychaete worms, clionid sponges, and algal borers are reported to have the ability to penetrate mollusc periostracum and other shell organic material (Warme, 1975), it is possible that the relatively thick periostracum of F. oregonensis inhibits these borers, which are most adept at penetrating calcareous substrates (Warme, 1975). The present study shows that the periostracum of Fusitriton oregonensis func~ tions to inhibit certain kinds of borers and epizoans. However, it is possible that epizoan and borer inhibition is not the most important secondary function of this periostracum but is only a useful by-product of to fulfill some other adaptive need or needs not examined in this study. For example, the trapped sediment between the periostracal hairs gives the a dark gray-green ap- pearance, so that it looks like a small rock fuzzily covered with algae. This blends in well with both soft and hard substrates, and may act as camouflage to predators relying upon visual perception of prey, such as the kelp greenling (Hexagrammos decagrammus), a predatory rockfish from the Puget Sound region which will bite the foot off F. oregonensis after it has dislodged the snail from its site of attach- ment (Palmer, 1977). Alternately, the thick periostracum may inhibit gastropod predatory boring, much like the layer found within the shells of cor~ bulid bivalves (Lewy and Samt1eben, 1979). In addition, it appears that during periods of rapid growth this snail advances the periostracum as much as one- quarter whorl, as described for other cymatiids (Laxton, 1970; 1971). For a short period of time this new portion of the is flexible, until it is sufficiently calcified by slow secretion of the underlying shell. By advance secretion of a thick periostracum this snail may be able to produce periods of growth more rapid than physiologically possible if growth was only by advancement of the mineralized shell. Further studies of the encruster and borer inhibitory function, as well as other functions of gastropod periostracum, are warranted. Such studies may produce more than just increased knowledge on periostracum. In order to develop better antifouling processes, much money and effort has been expended to understand both the physiology and ecology of fouling organisms as well as the antifouling properties of various structural materials and paint additives. Future research may show that utilization of encruster inhibitor properties of mulluscs, possibly combined with inhibitory properties of other epifaunal organisms (Jackson, 1977), may lead to development of a superior antifouling system.

ACKNOWLEDGMENTS

This study was conducted at the University of Washington's Friday Harbor Marine Laboratory. I thank A, J. Kohn and G, J, Vermeij for helpful suggestions during the research, I also thank G, R. Clark for constructive comments on an earlier draft of this paper. Parts of this research were funded by a grant from the Department of Geology, Indiana University, Bloomington. SHORTPAPERSANDNOTES 921

LITERATURE CITED

Abbott, R. T. 1968. of . Golden Press, New York. 280 pp. Barnes, H., and H. T. Powell. 1950. Some observations on the effect of fibrous glass surfaces upon the settlement of certain sedentary marine organisms. J. Mar. BioI. Ass. U.K. 29: 299-320. Bottjer, D. J. 1977. The functional significance of well-developed periostracum in bivalves and gastropods. Geol. Soc. Amer. Abstr. 9: 244. ---, and J. G. Carter. 1980. Functional and phylogenetic significance of projecting periostracal structures in the Biva]via (). J. Paleont. 54: 200-216. Clark, G. R. 1976. Shell growth in the marine environment: approaches to the problem of marginal calcification. Amer. Zoo I. 16: 617-626. Clench, W. J., and R. D. Turner. 1957. The family Cymatiidae in the Western Atlantic. Johnsonia 3: 189-244. Golubic, S., R. D. Perkins, and K. J. Lukas. 1975. Boring microorganisms and microborings in carbonate substrates. Pages 229-259 in R. W. Frey, ed. The study of trace fossils. Springer- Verlag, New York. Grant, R. E. 1966. Spine arrangement and life habits of the productoid Waagenoconcha. J. Paleont. 40: 1063-1069. Heptonstall, W. B. 1970. Buoyancy control in ammonoids. Lethaia 3: 3]7-328. Jackson, J. B. C. 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Amer. Nat. III: 743-767. Laxton, J. H. 1970. Shell growth in some New Zealand Cymatiidae (: ). J. Exp. Mar. BioI. Ecol. 4: 250-260. ---. 1971. The relationship between the number of varices and total shell length in some New Zealand Cymatiidae. 13: 127-134. Lewis, H. 1972. Notes on the Distorsio (Cymatiidae) with descriptions of new . Nau- tilus 86: 27-50. Lewy, Z., and C. Samtleben. 1979. Functional morphology and pa]eonto]ogical significance of the conchiolin layers in corbulid pelecypods. Lethaia 12: 341-351. Palmer, A. R. 1977. Function of shell in marine gastropods: hydrodynamic destabilization in Ceratostoma foliatum. Science 197: 1293-1295. Scanland, T. B. 1979. The epibiota of Arca zebra and A rca imbricata: a community analysis. Veliger 21: 475-485. Smith, J. T. 1970. , distribution, and phylogeny of the cymatiid gastropods Argobuccinum, Fusitriton, Mediargo, and Priene. Bull. Amer. Paleont. 56: 445-573. Vermeij, G. J. 1978. Biogeography and adaptation. Harvard University Press, Cambridge. 332 pp. Warme, J. E. 1975. Borings as trace fossils, and the processes of marine bioerosion. Pages 181-227 in R. W. Frey, ed. The study of trace fossils. Springer-Verlag, New York. ---, and E. J. McHuron. 1978. Marine borers: trace fossils and geological significance. Pages 77-131 in P. B. Basan, ed. Trace fossil concepts. Society of Economic Paleontologists and Mineralogists, Tulsa.

DATE ACCEPTED: September 15, 1980.

ADDRESS: Department of Geological Sciences, University of Southern California, Los Angeles, California 90007.