Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-27T14:13:57.913Z Has data issue: false hasContentIssue false

The muricid gastropod subfamily Rapaninae: phylogeny and ecological history

Published online by Cambridge University Press:  08 February 2016

Geerat J. Vermeij
Affiliation:
Department of Geology and Center for Population Biology, University of California at Davis, Davis, California 95616. E-mail: [email protected]
Sandra J. Carlson
Affiliation:
Department of Geology, University of California at Davis, Davis, California 95616. E-mail: [email protected]

Abstract

Members of the neogastropod muricid subfamily Rapaninae are abundant, shallow-water predators whose phylogeny was previously investigated by Kool (1993b), who used mainly anatomical characters. In order to deepen understanding of the evolution of this important clade and to incorporate functional, ecological fossil evidence, we performed a phylogenetic analysis based on 34 shell characters in 45 genus-level taxa, including five muricid outgroups. Cladograms based on shell characters alone differed from those founded on anatomical features these analyses differed from the phylogenetic reconstruction combining all available morphological evidence. The preferred cladogram incorporates all evidence and reveals a “Thais group” and an “Ergalatax clade” that both emerge from the derived portion of a more primitive, paraphyletic group of other rapanines. The Ocenebrinae, the other four outgroup taxa three ergalataxine taxa all lie outside the rapanine clade that includes the remaining ergalataxines as a derived subclade.

We used the phylogenetic results to probe aspects of the ecological history of the Rapaninae. Our data imply that antipredatory shell defenses (elongated aperture, denticles on the inner side of the outer lip robust external spines and tubercles) evolved multiple times, mainly in post–early Miocene clades in the Indo–West Pacific region. These results support earlier nonphylogenetic inferences.

We compared known prey types and methods of predation of living rapanines with their distribution on our phylogenetic tree. The plesiomorphic mode of feeding in the Rapaninae is drilling of hard-shelled prey. Feeding by other means and on such soft-bodied prey as sipunculan and polychaete worms evolved several times independently among post–early Miocene rapanines in the Indo–West Pacific. Methods of predation on hard-shelled prey that involve edge-drilling or attack by way of the aperture also evolved independently several times, but did so throughout the geographical range of the subfamily.

Specialization for life on the upper shore occurred in at least eight lineages, all but two of which are confined to the Indo–West Pacific. Ecological diversification of the Rapaninae was therefore most common in the tropical Indo–West Pacific during and after early Miocene time. This diversification occurred in a setting of already high biological diversity and intense competition and predation.

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

Abe, N. 1989. Interactions between carnivorous gastropods and their sessile animal prey at a rocky intertidal shore. Physiological Ecology in Japan 26:138.Google Scholar
Adegoke, O. S. 1977. Stratigraphy and paleontology of the Ewekoro Formation (Paleocene) of southwestern Nigeria. Bulletins of American Paleontology 71(295):1379.Google Scholar
Bertness, M. D., and Cunningham, C. 1981. Crab shell-crushing predation and gastropod architectural defense. Journal of Experimental Marine Biology and Ecology 50:213230.Google Scholar
Beu, A. G. 1970. Taxonomic position of Lippistes pehuensis Marwick, with a review of the species of Concholepas (Gastropoda, Muricidae). Journal of the Malacological Society of Australia 2:3946.Google Scholar
Beu, A. G., and Maxwell, P. A. 1990. Cenozoic Mollusca of New Zealand. New Zealand Geological Survey, Paleontological Bulletin 58:1518.Google Scholar
Black, R. 1978. Tactics of whelks preying on limpets. Marine Biology 46:157162.Google Scholar
Bogdanov, I. P. 1989. Morphological transformation in radula and protoconch of Oenopotinae Bogdanov, 1987. La Conchiglia 21:3547.Google Scholar
Bogdanov, I. P. 1990. Mollusks of Oenopotinae subfamily (Gastropoda, Pectinibranchia, Turridae) in the seas of the USSR. Fauna of USSR Mollusks, New Series 142, Vol. 5(3):1223. Nauk, Leningrad.Google Scholar
Bouchet, P., and Warén, A. 1985. Revision of the northeast Atlantic bathyal and abyssal Neogastropoda excluding Turridae (Mollusca, Gastropoda). Bollettino Malacologico Supplement 1:123296.Google Scholar
Bouchet, P., and Warén, A. 1986. Mollusca Gastropoda: taxonomical notes on tropical deep water Buccinidae with descriptions of new taxa. Mémoires du Muséum National d'Histoire Naturelle A 133:457499.Google Scholar
Bremer, K. 1994. Branch support and tree stability. Cladistics 10:295304.Google Scholar
Bull, J. J., Huelsenbeck, J. P., Cunningham, C. W., Swofford, D. L., and Waddell, P. J. 1993. Partitioning and combining data in phylogenetic analysis. Systematic Biology 42:384397.Google Scholar
Carriker, M. R., and Van Zandt, D. 1972. Predatory behavior of shell-boring muricid gastropods. Pp. 157244in Winn, H. E. and Olla, B. L., eds. Behavior of marine animals, Vol. I. Invertebrates. Plenum, New York.Google Scholar
Cernohorsky, W. O. 1976. The Mitridae of the world, Part I. The subfamily Mitrinae. Indo-Pacific Mollusca 3:273528.Google Scholar
Chapman, C. R. 1955. Feeding habits of the southern oyster drill, Thais haemastoma. Proceedings of the National Shell Fisheries Association 46:169186.Google Scholar
Clyde, W. C., and Fisher, D. C. 1997. Comparing the fit of stratigraphic and morphologic data in phylogenetic analysis. Paleobiology 23:119.Google Scholar
Connell, J. H. 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710723.Google Scholar
Cossmann, M., and Peyrot, M. A. 1924. Conchologie néogénique de l'Aquitaine. Actes de la Société Linnéenne de Bordeaux 75:71144, 193–318.Google Scholar
DeVries, T. J. 1995. Concholepas Lamarck, 1801 (Neogastropoda: Muricidae): a Neogene genus native to South America. Veliger 38:284297.Google Scholar
Duncan, S. de B., and Hughes, R. N. 1984. Behavioural components of prey-selection by dogwhelks, Nucella lapillus (L.), feeding on barnacles, Semibalanus balanoides (L.), in the laboratory. Journal of Experimental Marine Biology and Ecology 79:91103.Google Scholar
Edinger, E. N., and Risk, M. J. 1994. Oligocene-Miocene extinction and geographic extinction of Caribbean corals: roles of temperature, turbidity, and nutrients. Palaios 9:576598.Google Scholar
Eernisse, D. J., and Kluge, A. G. 1993. Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology. Molecular Biology and Evolution 10:11701195.Google Scholar
Farris, J. S. 1969. A successive approximations approach to character weighting. Systematic Zoology 18:374385.Google Scholar
Farris, J. S. 1982. Outgroups and parsimony. Systematic Zoology 31:328334.Google Scholar
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783791.Google Scholar
Fisher, D. C. 1980. The role of stratigraphic data in phylogenetic inference. Geological Society of America Abstracts with Programs 12(7):426.Google Scholar
Fisher, D. C. 1992. Stratigraphic parsimony. Pp. 124129in Maddison, W. P. and Maddison, D. R.MacClade: analysis of phylogeny and character evolution. Sinauer, Sunderland, Mass.Google Scholar
Fisher, D. C. 1994. Stratocladistics: morphological and temporal patterns and their relation to phylogenetic process. Pp. 103–12 in Grande, L. and Rieppel, O., eds. Interpreting the hierarchy of nature—from systematic patterns to evolutionary theories. Academic Press, San Diego.Google Scholar
Fortunato, H. 1998. Reconciling observed patterns of temporal occurrence with cladistic hypotheses of phylogenetic relationship. American Malacological Bulletin 14:191200.Google Scholar
Fox, D. L., Fisher, D. C., and Leighton, L. R. 1999. Reconstructing phylogeny with and without temporal data. Science 284:18161819.Google Scholar
Fujioka, Y. 1985. Systematic evaluation of radular characters in Thaidinae (Gastropoda: Muricidae). Journal of Science of Hiroshima University, Series B, Division 1 31:255287.Google Scholar
Garrity, S. D., and Levings, S. C. 1981. A predator–prey interaction between two physically and biologically constrained tropical rocky shore gastropods: direct, indirect and community effects. Ecological Monographs 51:267286.Google Scholar
Gibson-Smith, J., Gibson-Smith, W., and Vermeij, G. J. 1997. Pacific Mexican affinities of new species of the gastropod genera Macron (Pseudolividae) and Neorapana (Muricidae) from the Cantaure Formation (early Miocene) of Venezuela. Veliger 40:358363.Google Scholar
Golikov, A. N., and Tzvetkova, N. L. 1972. The ecological principle of evolutionary reconstruction as illustrated by marine animals. Marine Biology 14:19Google Scholar
Gordillo, S. 1998. Trophonid gastropod predation on Recent bivalves from the Magellanic region. Pp. 251254in Johnston, P. A. and Haggart, J. W., eds. Bivalves: an eon of evolution. Paleobiological studies honoring Norman D. Newell. University of Calgary Press, Calgary.Google Scholar
Gordillo, S., and Auchástegui, S. N. 1998. Estrategias de depredación del gastrópodo perforador Trophon geversianus (Pallas) (Muricoidea: Trophoninae). Malacologia 39:8391.Google Scholar
Goryachev, V. N. 1987. On the revision of the gastropod superfamily Buccinoidea (Mollusca, Gastropoda, Hamiglossa) of the extratropical zone of the Northern Hemisphere. Pp. 3135in Starobogatov, Ya. I., Golikov, A. N. and Likharev, I. M., eds. Mollusks: results and perspectives of investigation. Eighth meeting on the investigation of mollusks, Abstract of communications. “Nauka” Publishing House, Leningrad. [In Russian.]Google Scholar
Harasewych, M. G. 1990. Studies on bathyal and abyssal Buccinidae (Gastropoda: Neogastropoda). 1. Metula fusiformis Clench and Aguayo 1941. Nautilus 104:120129.Google Scholar
Hitchin, R., and Benton, M. J. 1997. Congruence between parsimony and stratigraphy: comparisons of three indices. Paleobiology 23:2032.Google Scholar
Hoffman, D. L., and Weldon, P. J. 1978. Flight responses of two intertidal gastropods (Prosobranchia: Trochidae) to sympatric predatory gastropods from Barbados. Veliger 20:361366.Google Scholar
Houart, R. 1994. Some notes on the genus Spinidrupa Habe and Kosuge, 1966 (Muricidae: Ergalataxinae), with the description of Habromorula gen. nov. (Muricidae: Rapaninae) and four new species from the Indo–West Pacific. Iberus 12:2131.Google Scholar
Houart, R. 1995. The Ergalataxinae (Gastropoda, Muricidae) from the New Caledonia region with some comments on the subfamily and the description of thirteen new species from the Indo–West Pacific. Bulletin du Muséum National d'Histoire Naturelle, Série 4, Section A 16:245297.Google Scholar
Hughes, R. N., and Duncan, S. de B. 1984. Effect of dietary history on selection of prey, and foraging behaviour among patches of prey, by the dogwhelk, Nucella lapillus (L.). Journal of Experimental Marine Biology and Ecology 79:159172.Google Scholar
Ingham, R. E., and Zischke, J. A. 1977. Prey preferences of carnivorous intertidal snails in the Florida Keys. Veliger 20:4951.Google Scholar
Kantor, Yu. I. 1996. Phylogeny and relationships of Neogastropoda. Pp. 221230in Taylor, J. D., ed. Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford.Google Scholar
Kay, E. A. 1979. Hawaiian marine shells. Bishop Museum Press, Honolulu.Google Scholar
Kitching, I. J., Forey, P. L., Humphries, C. J., and Williams, D. M. 1998. Cladistics: the theory and practice of parsimony analysis, 2d ed.Oxford University Press, Oxford.Google Scholar
Kluge, A. G. 1989. A concern for evidence and a phylogenetic hypothesis for relationships among Epicrates (Boidae, Serpentes). Systematic Biology 38:125.CrossRefGoogle Scholar
Kluge, A. G., and Wolf, A. J. 1993. Cladistics: what's in a word? Cladistics 9:183200.Google Scholar
Kohn, A. J. 1990. Tempo and mode of evolution in Conidae. Malacologia 32:5567.Google Scholar
Kool, S. P. 1993a. The systematic position of the genus Nucella (Prosobranchia: Muricidae: Ocenebrinae). Nautilus 107:4357.Google Scholar
Kool, S. P. 1993b. Phylogenetic analysis of the Rapaninae (Neogastropoda: Muricidae). Malacologia 35:155259.Google Scholar
Kuroda, T., Habe, T., and Oyama, K. 1971. The sea shells of Sagami Bay, collected by His Majesty The Emperor of Japan. Biological Laboratory, Imperial Household. Maruzen, Tokyo.Google Scholar
Lozouet, P., and Le Renard, P. 1998. Les Coralliophilidae, Gastropoda de l'Oligocène et du Miocène inferieur d'Aquitaine (sud-ouest de la France): systématique et coraux hôtes. Géobios 31:171184.Google Scholar
Lozouet, P., Ledon, D., and Lesport, J.-F. 1994. Le genre Lindapterys (Neogastropoda, Muricidae): un exemple de disjunction de distribution en domaine tropical marin. Géobios 27:3950.Google Scholar
Luckens, P. A. 1975. Predation and intertidal zonation of barnacles at Leigh, New Zealand. New Zealand Journal of Marine and Fresh-Water Research 9:355378.Google Scholar
Maddison, W. P., and Maddison, D. R. 1992. MacClade: analysis of phylogeny and character evolution. Sinauer, Sunderland, Mass.Google Scholar
Maddison, W. P., Donoghue, M. J., and Maddison, D. R. 1984. Outgroup analysis and parsimony. Systematic Zoology 33:83103.Google Scholar
Marko, P., and Vermeij, G. J. 1999. Molecular phylogenetics and the evolution of labral spines among eastern Pacific ocenebrine gastropods. Molecular Phylogeny and Evolution 13:275288.Google Scholar
Martin, K. 1914. Die Fauna des Obereocäns von Nanggulan, auf Java. Sammlungen des Geologischen Reichs-Museums in Leiden, Neue Folge 2(4):107178.Google Scholar
Martin, K. 1921. Die Mollusken der Njalindungschichten. Sammlungen des Geologischen Reichs-Museums in Leiden, Neue Folge 1(2):446496.Google Scholar
Moran, M. J. 1985. Effects of prey density, prey size and predator size on rates of feeding by an intertidal predatory gastropod Morula marginalba Blainville (Muricidae), on several species of prey. Journal of Experimental Marine Biology and Ecology 90:97105.Google Scholar
Morton, B. 1994. Prey preference and method of attack by Rapana bezoar (Gastropoda: Muricidae) from Hong Kong. Pp. 309325in Morton, B., ed. The malacofauna of Hong Kong and southern China III. Hong Kong University Press, Hong Kong.Google Scholar
Moyer, J. T., Emerson, W. K., and Ross, M. 1982. Massive destruction of scleractinian corals by the muricid gastropod, Drupella, in Japan and the Philippines. Nautilus 96:6982.Google Scholar
Nakagawa, T. 1998. Miocene molluscan fauna and paleoenvironment in the Niu Mountains, Fukui Prefecture, central Japan. Science Reports, Institute of Geosciences, University of Tsukuba Section B 19:61185.Google Scholar
Nixon, K. C., and Carpenter, J. M. 1993. On outgroups. Cladistics 9:413426.Google Scholar
Olsson, A. A. 1931. Contributions to the Tertiary paleontology of northern Peru, Part IV. The Peruvian Oligocene. Bulletins of American Paleontology 17(63):97264.Google Scholar
Paine, R. T. 1966. Function of labial spines, composition of diet, and size of certain marine gastropods. Veliger 9:1724.Google Scholar
Palmer, A. R. 1979. Fish predation and the evolution of shell sculpture: experimental and geographic evidence. Evolution 33:697713.Google Scholar
Palmer, A. R. 1982. Predation and parallel evolution: recurrent skeletal plate reduction in balanomorph barnacles. Paleobiology 8:3144.Google Scholar
Perry, D. M. 1985. Function of the shell spine in the predaceous rocky intertidal snail Acanthina spirata (Prosobranchia: Muricacea). Marine Biology 88:5158.Google Scholar
Ponder, W. F., and Vokes, E. H. 1988. A revision of the Indo–West Pacific fossil and Recent species of Murex s.s. and Haustellum (Mollusca: Gastropoda: Muricidae). Records of the Australian Museum 8(Suppl.):1160.Google Scholar
Radwin, G. E., and Wells, H. W. 1968. Comparative radular morphology and feeding habits of muricid gastropods from the Gulf of Mexico. Bulletin of Marine Science 18:7285.Google Scholar
Sanderson, M. J. 1995. Objections to bootstrapping phylogenies: a critique. Systematic Biology 44:299320.Google Scholar
Saul, L. R. 1996. Three new Turonian muricacean gastropods from the Santa Ana Mountains, southern California. Veliger 39:125135.Google Scholar
Schluter, D. 1996. Ecological causes of adaptive radiation. American Naturalist 148:S40S64.Google Scholar
Sleder, J. 1981. Acanthina punctulata (Neogastropoda, Muricacea): its distribution, activity, diet, and predatory behavior. Veliger 24:172180.Google Scholar
Smith, A. B. 1988. Patterns of diversification and extinction in early Paleozoic echinoderms. Palaeontology 31:799828.Google Scholar
Smith, A. B. 1994. Systematics and the fossil record: documenting evolutionary patterns. Blackwell Scientific, Oxford.Google Scholar
Spight, T. M., Birkeland, C., and Lyons, A. 1974. Life histories of large and small murexes (Prosobranchia: Muricidae). Marine Biology 24:229242.Google Scholar
Stone, H. M. I. 1998. On predator deterrence by pronounced shell ornament in epifaunal bivalves. Palaeontology 41:10511068.Google Scholar
Swofford, D. L. 1998. PAUP: phylogenetic analysis using parsimony (*and other methods), Version 4.0. Sinauer, Sunderland, Mass.Google Scholar
Taylor, J. D. 1976. Habitats, abundance and diets of muricacean gastropods at Aldabra Atoll. Zoological Journal of the Linnean Society 59:155193.CrossRefGoogle Scholar
Taylor, J. D. 1978. Habitats and diet of predatory gastropods at Addu Atoll, Maldives. Journal of Experimental Marine Biology and Ecology 31:83103.Google Scholar
Taylor, J. D. 1983. The food of coral-reef Drupa (Gastropoda). Zoological Journal of the Linnean Society 78:299316.Google Scholar
Taylor, J. D. 1984. A partial food web involving predatory gastropods on a Pacific fringing reef. Journal of Experimental Marine Biology and Ecology 74:273290.Google Scholar
Taylor, J. D. 1989. Diet of coral-reef Mitridae (Gastropoda) from Guam; with a review of other species of the family. Journal of Natural History 23:261278.Google Scholar
Taylor, J. D. 1990. Field observations of prey selection by the muricid gastropods Thais clavigera and Morula musiva feeding upon the intertidal oyster Saccostrea cucullata. Pp. 837855in Morton, B., ed. The marine flora and fauna of Hong Kong and southern China. Proceedings of the second international marine biological workshop, Hong Kong, 1986. Hong Kong University Press, Hong Kong.Google Scholar
Taylor, J. D., and Glover, E. 1999. Penetrating the defences: opercular drilling by Dicathais orbita (Mollusca: Gastropoda: Muricidae) on the turbinid gastropod Ninella torquata. Pp. 177198in Walker, D. I. and Wells, F. E., eds. The seagrass flora and fauna of Rottnest Island, Western Australia. Western Australian Museum, Perth.Google Scholar
Taylor, J. D., and Morton, B. 1996. The diets of predatory gastropods in the Cape d'Aguilar Marine Reserve, Hong Kong. Asian Marine Biology 13:141166.Google Scholar
Taylor, J. D., and Reid, D. G. 1984. The abundance and trophic classification of molluscs upon coral reefs in the Sudanese Red Sea. Journal of Natural History 18:175209.Google Scholar
Thomas, F. I. M., and Kohn, A. J. 1990. Trophic roles of co-occurring species of Drupa (Gastropoda: Muricidae) at Enewetak Atoll. Journal of Molluscan Studies 56:5762.Google Scholar
Titova, L. V. 1993. The early history of the North Pacific Ancistrolepidinae (Gastropoda, Buccinidae). Ruthenica 3:116.Google Scholar
Vermeij, G. J. 1974. Marine faunal dominance and molluscan shell form. Evolution 28:656664.Google Scholar
Vermeij, G. J. 1978. Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge.Google Scholar
Vermeij, G. J. 1980. Drilling predation in a population of the edible bivalve Anadara granosa. Nautilus 94:123125.Google Scholar
Vermeij, G. J. 1983. Intimate associations and coevolution in the sea. Pp. 311327in Futuyma, D. J. and Slatkin, M., eds. Coevolution. Sinauer, Sunderland, Mass.Google Scholar
Vermeij, G. J. 1987. Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J.Google Scholar
Vermeij, G. J. 1989. Interoceanic differences in adaptation: effects of history and productivity. Marine Ecology Progress Series 57:293305.Google Scholar
Vermeij, G. J. 1993. A natural history of shells. Princeton University Press, Princeton, N.J.Google Scholar
Vermeij, G. J. 1995. Morphology and possible relationships of Ecphora (Cenozoic Gastropoda: Muricidae). Nautilus 109:120126.Google Scholar
Vermeij, G. J. 1998a. Generic revision of the neogastropod family Pseudolividae. Nautilus 111:5384.Google Scholar
Vermeij, G. J. 1998b. New genera of Cenozoic muricid gastropods, with comments on the mode of formation of the labral tooth. Journal of Paleontology 72:855864.Google Scholar
Vermeij, G. J., and Currey, J. D. 1980. Geographical variation in the strength of thaidid snail shells. Biological Bulletin 158:383389.Google Scholar
Vermeij, G. J., and Kool, S. P. 1994. Evolution of labral spines in Acanthais, new genus, and other rapanine muricid gastropods. Veliger 37:414424.Google Scholar
Vermeij, G. J., and Kropp, R. K. 1995. A note on the muricid gastropod Muricodrupa jacobsoni in the Palau Islands. Festivus 27:8485.Google Scholar
Vermeij, G. J., and Signor, P. W. 1992. The geographic, taxonomic, and temporal distribution of determinate growth in marine gastropods. Biological Journal of the Linnean Society 47:233247.Google Scholar
Vokes, E. H. 1990. Cenozoic Muricidae of the western Atlantic region Part VIII—Murex s.s., Haustellum, Chicoreus, and Hexaplex; additions and corrections. Tulane Studies in Geology and Paleontology 23:196.Google Scholar
Vokes, E. H. 1996. Cenozoic Muricidae of the western Atlantic region, Part XI. The subfamily Ergalataxinae. Tulane Studies in Geology and Paleontology 29:2744.Google Scholar
Watrous, L. E., and Wheeler, Q. D. 1981. The out-group comparison method of character analysis. Systematic Zoology 30:111.Google Scholar
Wellington, G. M., and Kuris, A. M. 1983. Growth and shell variation in the tropical eastern Pacific intertidal gastropod genus Purpura: ecological and evolutionary implications. Biological Bulletin 164:518535.Google Scholar
West, L. 1986. Interindividual variation in prey selection by the snail Nucella (= Thais) emarginata. Ecology 67:798809.Google Scholar
West, L. 1988. Prey selection by the tropical snail Thais melones: a study of interindividual variation. Ecology 69:18391854.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
Woodring, W. P. 1973. Geology and paleontology of Canal Zone and adjoining parts of Panama: descriptions of Tertiary mollusks (additions to gastropods, scaphopods, pelycpods: Nuculidae to Malleidae). U.S. Geological Survey Professional Paper 306-E:453539.Google Scholar