Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T07:18:34.231Z Has data issue: false hasContentIssue false

Predation and Parallel Evolution: Recurrent Parietal Plate Reduction in Balanomorph Barnacles

Published online by Cambridge University Press:  08 February 2016

A. Richard Palmer*
Affiliation:
Department of Zoology, University of Alberta, Edmonton, Alberta T6G 2E9 and Bamfield Marine Station, Bamfield, British Columbia V0R 1B0, Canada

Abstract

Field and laboratory data indicate that all four species of Thais (Gastropoda, Muricacea) from rocky shores of the northeastern Pacific selectively attack barnacles at the margins of parietal (lateral) and opercular plates. Attacks are also more likely to be successful at plate margins. Such preferential attack and differential attack success may account for the evolutionary reduction in the number of parietal plates exhibited within seven of the eight families of balanomorph barnacles. Additional evidence suggests that predation by drilling gastropods may have also favored the evolution of strong external ribbing on these plates within some balanomorph lineages.

Radiation and plate reduction in the Balanomorpha occurred in concert with extensive radiation in muricacean gastropods, starting in the Late Cretaceous. Of the three skeletal conformations exhibited by open-surface dwelling barnacles (8, 6 and 4 parietal plates), only genera of the four-plated form have become proportionally more common in the Recent. Further, in a rather striking evolutionary experiment, a lineage of barnacles evolving free from gastropod predation retained primitive skeletal features. This supports the interpretation that predation by drilling gastropods has been an important selective force behind the widespread, parallel evolutionary tendency towards plate reduction in the Balanomorpha; a trend recognized by Darwin (1854), but for which he offered no explanation.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adegoke, O. S. and Tevesz, M. J. S. 1974. Gastropod predation patterns in the Eocene of Nigeria. Lethaia. 7:1724.CrossRefGoogle Scholar
Barnes, H., Reed, R., and Topinka, J. 1970. The behavior on impaction by solids of some common cirripedes and relation to their normal habitat. J. Exp. Mar. Biol. Ecol. 5:7087.CrossRefGoogle Scholar
Barnett, B. E. 1979. A laboratory study of predation by the dog-whelk Nucella lapillus on the barnacles Elminius modestus and Balanus balanoides. J. Mar. Biol. Assoc. UK. 59:299306.CrossRefGoogle Scholar
Berg, C. J. and Nishenko, S. 1975. Stereotypy of predatory boring behavior of Pleistocene naticid gastropods. Paleobiology. 1:258260.CrossRefGoogle Scholar
Berg, C. J. and Porter, M. E. 1974. A comparison of predatory behavior among the naticid gastropods Lunatia heros and L. triseriata and Polinices duplicatus. Biol. Bull. 147:469470.Google Scholar
Black, R. 1978. Tactics of whelks preying on limpets. Mar. Biol. 46:157162.CrossRefGoogle Scholar
Butler, P. A. 1953. The southern oyster drill. Proc. Natl. Shellfish Assoc. 44:6775.Google Scholar
Carefoot, T. 1977. Pacific Seashores. 208 pp. Univ. Washington Press; Seattle, Washington.Google Scholar
Carriker, M. R. 1959. Comparative functional morphology of the drilling mechanism in Urosalpinx and Eupleura (muricid gastropods). Proc. 15th Int. Congr. Zool. Lond. Pp. 373376.Google Scholar
Carriker, M. R. and van Zandt, D. 1972. Predatory behavior of a shell boring muricid gastropod. Pp. 157244. In: Winn, H. E. and Olla, B. L., eds. Behavior of Marine Animals, Vol. 1: Invertebrates. Plenum Press; New York.CrossRefGoogle Scholar
Carriker, M. R. and Yochelson, E. L. 1968. Recent gastropod boreholes and Ordivician cylindrical borings. Contrib. Paleontol., Geol. Surv. Prof. Pap. 593-B:B1–B26.Google Scholar
Chapmann, C. R. 1955. Feeding habits of the southern oyster drill Thais haemastoma. Proc. Natl. Shellfish Assoc. 46:169176.Google Scholar
Connell, J. H. 1961a. The effects of competition, predation by Thais lapillus, and other factors on natural populations on the barnacle Balanus balanoides. Ecol. Monogr. 31:61104.CrossRefGoogle Scholar
Connell, J. H. 1961b. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology. 42:710723.CrossRefGoogle Scholar
Connell, J. H. 1970. A predator-prey system in the marine intertidal region. I. Balanus glandula and several predatory species of Thais. Ecol. Monogr. 40:4978.Google Scholar
Cornman, I. 1963. Toxic properties of the saliva of Cassis. Nature. 200:8889.CrossRefGoogle Scholar
Darwin, C. 1854. A monograph on the subclass Cirripedia. The Balanidae, the Verrucidae, etc. 684 pp. Ray Soc.; London.Google Scholar
Day, J. A. 1969. Feeding of the cymatiid gastropod, Argobuccinum argus, in relation to the structure of the proboscis and secretions of the proboscis gland. Am. Zool. 9:909916.CrossRefGoogle Scholar
Dayton, P. K. 1971. Competition, disturbance and community organization: provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41:351389.CrossRefGoogle Scholar
Dubois, R. 1909. Recherches sur la pourpre et sur quelques autres pigments animaux. Arch. Zool. Exp. Gen. 5e Ser. 2:471490.Google Scholar
Dudley, E. C. and Vermeij, G. J. 1978. Predation in time and space: drilling in the gastropods Turritella. Paleobiology. 4:436441.CrossRefGoogle Scholar
Eaton, C. M. 1971. The reproductive and feeding biology of the prosobranch gastropod Fusitriton oregonensis (Redfield) (Cymatiidae). 39 pp. Unpubl. M.S. Thesis, Univ. Washington; Seattle, Washington.Google Scholar
Edwards, D. C. and Huebner, J. D. 1977. Feeding and growth rates of Polinices duplicatus preying on Mya arenaria at Barnstable Harbor, Massachusetts. Ecology. 58:12181236.CrossRefGoogle Scholar
Emlen, J. M. 1966. Time, energy and risk in two species of carnivorous gastropods. 128 pp. Ph.D. diss. Univ. Washington; Seattle, Washington.Google Scholar
Fischer-Piette, E. 1935. Histoire d'une mouliere. Bull. Biol. Fr. Belg. 69:152177.Google Scholar
Foster, B. A. 1971a. On the determinants of the upper limits of intertidal distribution of barnacles (Crustacea, Cirripedia). J. Anim. Ecol. 40:3348.CrossRefGoogle Scholar
Foster, B. A. 1971b. Desiccation as a factor in the intertidal zonation of barnacles. Mar. Biol. 8:1229.CrossRefGoogle Scholar
Galtsoff, P. S., Prytherch, H. F., and Engle, J. B. 1937. Natural history and methods of controlling the common oyster drills (Urosalpinx cinerea and U. caudata). U.S. Bur. Fish. Circ. No. 25, 24 pp.Google Scholar
Gruvel, J. A. 1903. Revision des Cirrhipedes appartenant a la collection du Museum d'Histoire Naturelle (Opercules). II. Partie systematique. Mus. Natl. Hist. Nat. Paris, Arch. ser. 4. 5:95170.Google Scholar
Hourbrick, J. R. and Fretter, V. 1969. Some aspects of the functional anatomy and biology of Cymatium and Bursa. Proc. Malacol. Soc. Lond. 38:415429.Google Scholar
Huang, C. L. 1971. Pharmacological properties of the hypobranchial gland of Thais haemastoma (Clench). J. Pharm. Sci. 60:18421846.CrossRefGoogle ScholarPubMed
Huang, C. L. 1972. Pharmacological investigations of the salivary gland of Thais haemastoma (Clench). Toxicon. 10:111117.CrossRefGoogle ScholarPubMed
Kozloff, E. N. 1974. Seashore life of Puget Sound, the Strait of Georgia, and the San Juan Archipelago. 282 pp. Univ. Washington Press; Seattle, Washington.Google Scholar
Kruger, P. 1940. Cirripedia. Pp. 1560. In: Bronns Klassen und Ordnungen des Tierreichs. Bd. 5. Crustacea Abt. 1. Buch 3, Tiel III. Leipzig.Google Scholar
Largen, M. J. 1967. The diet of the dog-whelk, Nucella lapillus (Gastropoda, Prosobranchia). J. Zool. Lond. 151:123127.CrossRefGoogle Scholar
Luckens, P. A. 1975. Predation and intertidal zonation of barnacles at Leigh, New Zealand. NZ J. Mar. Freshwat. Res. 9:355378.CrossRefGoogle Scholar
Menge, J. L. 1974. Prey selection and foraging period of the pre-daceous rocky intertidal snail Acanthina punctulata. Oecologia. 17:293316.CrossRefGoogle ScholarPubMed
Moore, H. B. 1938. The biology of Purpura lapillus. III. Life history and relation to environmental factors. J. Mar. Biol. Assoc. UK 23:6774.Google Scholar
Morgan, P. R. 1972a. Nucella lapillus (L) as a predator of edible cockles. J. Exp. Mar. Biol. Ecol. 8:4553.CrossRefGoogle Scholar
Morgan, P. R. 1972b. The influence of prey availability on the diet and predatory behaviour of Nucella lapillus (L). J. Anim. Ecol. 41:257274.CrossRefGoogle Scholar
Negus, M. 1975. An analysis of boreholes drilled by Natica catena (da Costa) in the valves of Donax vittatus (da Costa). Proc. Malacol. Soc. Lond. 41:353356.Google Scholar
Newman, W. A. 1967. A new genus of Chthamalidae (Cirripedia, Balanomorpha) from the Red Sea and Indian Ocean. J. Zool. Lond. 153:423435.Google Scholar
Newman, W. A. and Ladd, H. S. 1974. Origin of coral-inhabiting balanids (Cirripedia, Thoracica). Verhandl. Naturf. Ges. Basel. 84:381396.Google Scholar
Newman, W. A. and Ross, A. 1971. Antarctic Cirripedia. Am. Geophys. Union, Antarctic Res. Ser. 14:1257.Google Scholar
Newman, W. A. and Ross, A. 1976. Revision of the balanomorph barnacles; including a catalog of the species. San Diego Soc. Nat. Hist. Mem. 9:1108.Google Scholar
Newman, W. A., Zullo, V. A., and Withers, T. H. 1969. Cirripedia. In: Moore, R. C., ed. Treatise on Invertebrate Paleontology Pt. R. Arthropoda. 4(1):206295.Google Scholar
Paine, R. T. 1966. Function of labial spines, composition of diet, and size of certain marine gastropods. Veliger. 9:1724.Google Scholar
Paine, R. T. 1976. Size-limited predation: an observational and experimental approach with the Mytilus-Pisaster interaction. Ecology. 57:858873.CrossRefGoogle Scholar
Palmer, A. R. 1979. Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution. 33:697713.CrossRefGoogle ScholarPubMed
Palmer, A. R. 1980. A Comparative and Experimental Study of Feeding and Growth in Thaidid Gastropods. 320 pp. Ph.D. diss. Univ. Washington; Seattle, Washington.Google Scholar
Palmer, A. R. 1981. Do carbonate skeletons limit the rate of body growth? Nature. 292:150152.Google Scholar
Palmer, A. R. Submitted. Growth rates as a measure of food value in thaidid gastropods: assumptions and ecological implications. Ecology.Google Scholar
Pilsbry, H. R. 1916. The sessile barnacles (Cirripedia) contained in the U.S. National Museum, including a monograph of the American species. U.S. Natl. Mus. Bull. 93:1366.CrossRefGoogle Scholar
Radwin, G. E. and Wells, H. W. 1968. Comparative radular morphology and feeding habits of muricid gastropods from the Gulf of Mexico. Bull. Mar. Sci. 18:7285.Google Scholar
Reyment, R. A. 1967. Paleoethology and fossil drilling gastropods. Trans. Kansas Acad. Sci. 70:3350.CrossRefGoogle Scholar
Ricketts, E. F., Calvin, J., and Hedgepeth, J. W. 1968. Between Pacific Tides. 614 pp. Stanford Univ. Press; Stanford, California.Google Scholar
Ross, A. and Newman, W. A. 1967. Eocene Balanidae of Florida including a new genus and species with a unique plan of “Turtle Barnacle” organization. Am. Mus. Novitates. 2288:121.Google Scholar
Sohl, N. F. 1969. The fossil record of shell-boring by snails. Am. Zool. 9:725734.CrossRefGoogle Scholar
Spight, T. M. 1972. Patterns of change in adjacent populations of an intertidal snail, Thais lamellosa. 308 pp. Ph.D. diss. Univ. Washington; Seattle, Washington.Google Scholar
Stanley, S. M. and Newman, W. A. 1980. Competitive exclusion in evolutionary time: the case of the acorn barnacles. Paleobiology. 6:173183.CrossRefGoogle Scholar
Stephenson, T. A. and Stephenson, A. 1972. Life Between the Tidemarks on Rocky Shores. 425 pp. W. H. Freeman; New York.Google Scholar
Tanaka, Y. 1950. Injuring mechanisms of the oyster drill (Purpura clavigera) to young oysters (Ostrea gigas). Bull. Jap. Soc. Sci. Fish. 15:447457.CrossRefGoogle Scholar
Taylor, J. D., Morris, N. J., and Taylor, C. N. 1980. Food specialization and the evolution of predatory prosobranch gastropods. Paleontology. 23:375409.Google Scholar
Thomas, R. D. K. 1976. Gastropod predation on sympatric Neogene species of Glycymeris (Bivalvia) from the eastern United States. J. Paleontol. 50:488499.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution: gastropods, predators and grazers. Paleobiology. 3:245258.Google Scholar
Vermeij, G. J. 1978. Biogeography and Adaptation: Patterns of Marine Life. 416 pp. Harvard Univ. Press; Cambridge, Massachusetts.Google Scholar
Vermeij, G. J. 1980a. Drilling predation of bivalves in Guam: some paleoecological implications. Malacologia. 19:329334.Google Scholar
Vermeij, G. J. 1980b. Drilling predation in a population of the edible bivalve Anadara granosa (Arcidae). Nautilus. 94:123125.Google Scholar
Withers, T. H. 1953. Catalogue of Fossil Cirripedia. Vol. 3. Tertiary. 396 pp. Brit. Mus. (Nat. Hist.).Google Scholar
Wood, L. 1968. Physiological and ecological aspects of prey selection by the marine gastropod Urosalpinx cinerea (Prosobranchia: Muricidae). Malacologia. 6:267320.Google Scholar